Emerging Technologies and Management of Crop ...

Emerging Technologies and Management of Crop Stress Tolerance

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Emerging Technologies and Management of Crop Stress Tolerance A Sustainable Approach Volume 2

Edited by

Parvaiz Ahmad Saiema Rasool

AMSTERDAM • BOSTON • HEIDELBERG • LONDON NEWYORK • OXFORD • PARIS • SAN DIEGO SAN FRANCISCO • SINGAPORE • SYDNEY • TOKYO

Academic Press is an imprint of Elsevier

Academic Press is an imprint of Elsevier 525 B Street, Suite 1800, San Diego, CA 92101-4495, USA 32 Jamestown Road, London NW1 7BY, UK 225 Wyman Street, Waltham, MA 02451, USA Copyright r 2014 Elsevier Inc. All rights reserved. No part of this publication may be reproduced, stored in a retrieval system, or transmitted in any form or by any means electronic, mechanical, photocopying, recording or otherwise without the prior written permission of the publisher. Permissions may be sought directly from Elsevier’s Science & Technology Rights, Department in Oxford, UK: phone (144) (0) 1865 843830; fax (144) (0) 1865 853333; email: [email protected]. Alternatively, visit the Science and Technology Books website at www.elsevierdirect.com/rights for further information. Notice No responsibility is assumed by the publisher for any injury and/or damage to persons, or property as a matter of products liability, negligence or otherwise, or from any use or, operation of any methods, products, instructions or ideas contained in the material herein. Because of rapid advances in the medical sciences, in particular, independent verification of diagnoses and drug dosages should be made. British Library Cataloguing-in-Publication Data A catalogue record for this book is available from the British Library Library of Congress Cataloging-in-Publication Data A catalog record for this book is available from the Library of Congress ISBN: 978-0-12-800875-1 For information on all Academic Press publications visit our website at elsevierdirect.com Printed and bound in the United States of America 14 15 16 17 18 10 9 8 7 6 5 4 3 2 1

Dedication

This book is dedicated to

Hakim Abdul Hameed (19081999) Founder of Jamia Hamdard (Hamdard University) New Delhi, India


Contents Preface ............................................................................................................................................... xvii Acknowledgments .............................................................................................................................. xix About the Editors................................................................................................................................ xxi List of Contributors .......................................................................................................................... xxiii

CHAPTER 1

Improvement of Legume Crop Production Under Environmental Stresses Through Biotechnological Intervention .................................. 1 Adeena Shafique, Sammia Rehman, Azka Khan and Alvina Gul Kazi

1.1 Introduction ................................................................................................................ 1 1.2 Major stresses affecting legume crop production ..................................................... 2 1.3 Biotic stresses for legumes ........................................................................................ 2 1.3.1 Fungi ................................................................................................................ 2 1.3.2 Foliar diseases.................................................................................................. 3 1.3.3 Plant viruses..................................................................................................... 3 1.3.4 Insects and pests .............................................................................................. 4 1.3.5 Parasitic weeds ................................................................................................ 5 1.4 Biotechnological interventions for biotic stress tolerance in legumes ..................... 5 1.4.1 Focus on fungal stress ..................................................................................... 5 1.5 Abiotic stresses in legumes........................................................................................ 8 1.5.1 Drought ............................................................................................................ 9 1.5.2 Salinity ........................................................................................................... 10 1.5.3 Temperature ................................................................................................... 10 1.6 Biotechnological interventions for abiotic stress tolerance in legumes ................. 10 1.6.1 Soybean.......................................................................................................... 11 1.6.2 Cowpea .......................................................................................................... 15 1.7 Conclusion and future prospects.............................................................................. 16 References ........................................................................................................................ 17

CHAPTER 2

Abiotic Stress Tolerance in Plants ....................................................... 23 P.S. Sha Valli Khan, G.V. Nagamallaiah, M. Dhanunjay Rao, K. Sergeant and J.F. Hausman

2.1 Introduction .............................................................................................................. 23 2.2 Plant responses to abiotic stresses ........................................................................... 24 2.3 Proteomic analysis of responses to abiotic stresses ................................................ 25

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2.3.1 Water stress.................................................................................................... 26 2.3.2 Imbalances in mineral nutrition .................................................................... 37 2.3.3 Heavy metal stress......................................................................................... 41 2.3.4 Salt stress ....................................................................................................... 45 2.3.5 Temperature stress......................................................................................... 47 2.4 Conclusion and future prospects.............................................................................. 55 References ........................................................................................................................ 56

CHAPTER 3

Arbuscular Mycorrhiza in Crop Improvement under Environmental Stress .............................................................................. 69 Mohammad Abass Ahanger, Abeer Hashem, Elsayed Fathi Abd-Allah and Parvaiz Ahmad

3.1 3.2 3.3 3.4

Introduction .............................................................................................................. 69 Diversity of arbuscular mycorrhizal fungi .............................................................. 71 Effect of arbuscular mycorrhizal fungi on soil fertility .......................................... 72 Arbuscular mycorrhizal fungi and environmental stresses in plants ...................... 73 3.4.1 Arbuscular mycorrhizal fungi and water stress ............................................ 74 3.4.2 Arbuscular mycorrhizal fungi and salinity stress ......................................... 75 3.4.3 Arbuscular mycorrhizal fungi and pathogen attack...................................... 77 3.4.4 AMF and herbicides and pesticides .............................................................. 78 3.5 Ion transport in plants under stress and the role of arbuscular mycorrhizal fungi ..................................................................................................... 79 3.6 Arbuscular mycorrhizal fungi and mineral nutrition .............................................. 79 3.6.1 Phosphorus..................................................................................................... 80 3.6.2 Nitrogen ......................................................................................................... 80 3.6.3 Potassium and K1/Na1 ratio......................................................................... 81 3.6.4 Calcium.......................................................................................................... 82 3.6.5 Magnesium..................................................................................................... 82 3.7 Conclusion and future prospects.............................................................................. 82 References ........................................................................................................................ 83

CHAPTER 4

Role of Endophytic Microbes in Mitigation of Abiotic Stress in Plants........................................................................................ 97 Amrita Kasotia and Devendra Kumar Choudhary

4.1 Introduction .............................................................................................................. 97 4.2 Endophyte diversity ................................................................................................. 98 4.3 Sustainable use of endophytes and habitat-imposed abiotic stress....................... 100 4.4 Conclusion and future prospects............................................................................ 102 Acknowledgments .......................................................................................................... 103 References ...................................................................................................................... 103

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Plant Growth-Promoting Bacteria Elicited Induced Systemic Resistance and Tolerance in Plants ................................................... 109 Shekhar Jain, Anookul Vaishnav, Amrita Kasotia, Sarita Kumari and Devendra Kumar Choudhary

5.1 Introduction ............................................................................................................ 109 5.2 PGPB-elicited response of plants against biotic stress ......................................... 110 5.3 PGPB-produced elicitors of ISR against biotic stress........................................... 114 5.3.1 Siderophore.................................................................................................. 114 5.3.2 Antibiotics.................................................................................................... 115 5.3.3 Volatiles ....................................................................................................... 115 5.4 PGPB-elicited plant response against abiotic stress.............................................. 117 5.5 Conclusion and future prospects............................................................................ 120 Acknowledgments .......................................................................................................... 121 References ...................................................................................................................... 121

CHAPTER 6

Arbuscular Mycorrhizal Fungi and Metal Phytoremediation: Ecophysiological Complementarity in Relation to Environmental Stress........................................................................ 133 Patrick Audet

6.1 Introduction ............................................................................................................ 133 6.1.1 Metal phytoremediation............................................................................... 134 6.1.2 Objectives .................................................................................................... 135 6.2 Arbuscular mycorrhizal fungi and plant stress tolerance...................................... 136 6.2.1 Enhanced metal/nutrient uptake .................................................................. 138 6.2.2 Metal/nutrient biosorption and precipitation............................................... 141 6.2.3 Soil particulate microaggregation ............................................................... 143 6.3 Adopting arbuscular mycorrhizal plants into metal phytoremediation ................ 145 6.3.1 Plantsoil experimental perspectives ......................................................... 146 6.3.2 The burden of metal stress and the dilemma of resource allocation ......... 150 6.4 Conclusion and future prospects............................................................................ 152 Acknowledgments .......................................................................................................... 153 References ...................................................................................................................... 153

CHAPTER 7

Biological Control of Fungal Disease by Rhizobacteria under Saline Soil Conditions ............................................................... 161 Dilfuza Egamberdieva, Abeer Hashem and Elsayed Fathi Abd-Allah

7.1 7.2 7.3 7.4

Introduction ............................................................................................................ 161 Salinity and plant pathogens.................................................................................. 162 Plant growth-promoting rhizobacteria ................................................................... 163 Biological control................................................................................................... 164

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7.5 Mechanisms of action of plant growth-promoting rhizobacteria.......................... 166 7.6 Conclusion and future prospects............................................................................ 168 References ...................................................................................................................... 169

CHAPTER 8

Crop Plants under Saline-Adapted Fungal Pathogens: An Overview ................................................................................................. 173 Murat Dikilitas and Sema Karakas

8.1 Introduction ............................................................................................................ 173 8.2 Effects of salinity on crop plants........................................................................... 174 8.3 Effects of salinity on fungi .................................................................................... 176 8.3.1 Negative effects of salinity on fungal growth ............................................ 176 8.3.2 Positive effects of salinity on fungal growth .............................................. 179 8.3.3 Negative effects on plant growth of salinity in combination with fungi ... 180 8.4 Behavior of saline-adapted fungi........................................................................... 182 8.5 Pathological defense mechanisms under salt stress .............................................. 183 8.6 Pathological responses of salt-tolerant plants ....................................................... 184 8.7 Conclusion and future prospects............................................................................ 184 Acknowledgment ........................................................................................................... 185 References ...................................................................................................................... 185

CHAPTER 9

Preventing Potential Diseases of Crop Plants Under the Impact of a Changing Environment ..................................................... 193 Memoona Ilyas, Khola Rafique, Sania Ahmed, Sobia Zulfiqar, Fakiha Afzal, Maria Khalid, Alvina Gul Kazi and Abdul Mujeeb-Kazi

9.1 Introduction ............................................................................................................ 193 9.2 Major crops and techniques for preventing hazardous stress ............................... 194 9.2.1 Wheat ........................................................................................................... 194 9.2.2 Maize ........................................................................................................... 199 9.2.3 Rice .............................................................................................................. 201 9.2.4 Barley........................................................................................................... 203 9.2.5 Cotton........................................................................................................... 205 9.3 Conclusion and future prospects............................................................................ 206 References ...................................................................................................................... 207

CHAPTER 10 Plant Responses to Metal Stress: The Emerging Role of Plant Growth Hormones in Toxicity Alleviation ................................ 215 Savita Gangwar, Vijay Pratap Singh, Durgesh Kumar Tripathi, Devendra Kumar Chauhan, Sheo Mohan Prasad and Jagat Narayan Maurya 10.1 Introduction ............................................................................................................ 215

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10.2 Sources of heavy metal pollution .......................................................................... 216 10.3 Transport and distribution of metal in plants ........................................................ 216 10.4 Heavy metal toxicity in plants ............................................................................... 218 10.4.1 Direct effects .............................................................................................. 218 10.4.2 Indirect effects............................................................................................ 220 10.5 Plant defense systems............................................................................................. 221 10.5.1 Enzymatic antioxidants .............................................................................. 222 10.5.2 Nonenzymatic antioxidants........................................................................ 227 10.6 Plant growth hormones .......................................................................................... 229 10.7 Role of plant growth hormones under stress ......................................................... 230 10.7.1 Behavior of auxins under stress................................................................. 230 10.7.2 Behavior of gibberellic acids under stress................................................. 231 10.7.3 Behavior of cytokinins under stress........................................................... 233 10.8 Conclusion and future prospects............................................................................ 235 Acknowledgments ............................................................................................................ 236 References......................................................................................................................... 236

CHAPTER 11 Reactive Nitrogen Species and the Role of NO in Abiotic Stress .................................................................................... 249 ´ ´ Jan Sumaira, Nad’a Wilhelmova, ´ Dagmar Prochazkov a, ˇ ´ a´ Daniela Pavl´ıkova´ and Jirina Szakov 11.1 11.2 11.3 11.4 11.5 11.6 11.7 11.8

Introduction............................................................................................................. 249 The reactive nitrogen species................................................................................. 249 Drought stress ......................................................................................................... 250 Waterlogging stress ................................................................................................ 251 High temperature stress .......................................................................................... 252 Low temperature stress........................................................................................... 253 Salinity stress.......................................................................................................... 254 Heavy metal stress.................................................................................................. 254 11.8.1 Cadmium .................................................................................................... 255 11.8.2 Copper ........................................................................................................ 256 11.8.3 Arsenic........................................................................................................ 256 11.8.4 Zinc............................................................................................................. 257 11.9 Air pollutants .......................................................................................................... 257 11.10 Exposure to high light conditions .......................................................................... 257 11.11 UV-B radiation ....................................................................................................... 258 11.12 Conclusion and future prospects ............................................................................ 259 Acknowledgments............................................................................................................... 259 References........................................................................................................................... 260

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CHAPTER 12 Role of Tocopherol (Vitamin E) in Plants: Abiotic Stress Tolerance and Beyond .......................................................................... 267 Mirza Hasanuzzaman, Kamrun Nahar and Masayuki Fujita 12.1 12.2 12.3 12.4 12.5

Introduction ............................................................................................................ 267 Chemistry and types of tocopherol ........................................................................ 268 Tocopherol biosynthesis and accumulation in plants............................................ 270 The role of tocopherol in plant growth and physiology........................................ 272 Tocopherol and abiotic stress tolerance................................................................. 274 12.5.1 Salinity........................................................................................................ 275 12.5.2 Drought....................................................................................................... 276 12.5.3 Extreme temperature .................................................................................. 277 12.5.4 Metal toxicity ............................................................................................. 278 12.5.5 Ozone.......................................................................................................... 279 12.5.6 UV radiation............................................................................................... 279 12.6 The antioxidative role of tocopherol in plants ...................................................... 279 12.7 Conclusion and future prospects............................................................................ 282 Acknowledgments ............................................................................................................ 282 References......................................................................................................................... 282

CHAPTER 13 Land and Water Management Strategies for the Improvement of Crop Production......................................................... 291 Gabrijel Ondrasek, Zed Rengel, Dragutin Petosic and Vilim Filipovic 13.1 Introduction ............................................................................................................ 291 13.2 Strategies for improving crop production in water-deficient agroecosystems ..... 292 13.2.1 Improvement of crop production in rain-fed agriculture .......................... 292 13.2.2 Improving crop production in irrigated agriculture................................... 296 13.3 Strategies for improving crop production in (transiently) waterlogged agroecosystems....................................................................................................... 299 13.3.1 Types of waterlogging and the impact on crop production ...................... 299 13.3.2 Agriculture under waterlogging conditions of hydromorphic soils: a Croatian case study ................................................................................. 302 13.3.3 Crop production improvement in waterlogged agroecosystems ............... 302 13.4 Conclusion and future prospects............................................................................ 309 Acknowledgments ............................................................................................................ 310 References......................................................................................................................... 310

CHAPTER 14 Integrating Physiological and Genetic Approaches for Improving Drought Tolerance in Crops............................................... 315 Ahmad Ali, Zeshan Ali, Umar M. Quraishi, Alvina Gul Kazi, Riffat N. Malik, Hassan Sher and Abdul Mujeeb-Kazi 14.1 Introduction............................................................................................................. 315

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14.2 14.3 14.4 14.5 14.6 14.7 14.8

Drought stress in changing environments.............................................................. 319 Water deficit as a major abiotic factor limiting crop yields ................................. 320 Crop growth and response to water deficits .......................................................... 320 Osmotic adjustment during drought stress............................................................. 322 Methodologies for screening genotypes under drought stress .............................. 322 Key physiological attributes for targeted breeding programs ............................... 323 Precise phenotyping for drought-tolerance attributes............................................ 325 14.8.1 Near-infrared spectroscopy ........................................................................ 325 14.8.2 Canopy spectral reflectance ....................................................................... 325 14.8.3 Magnetic resonance imaging and nuclear magnetic resonance ................ 325 14.8.4 Digital imaging platforms .......................................................................... 326 14.9 Identification and characterization of drought-related genes and QTLs .............. 326 14.9.1 QTL and association mapping for drought tolerance................................ 327 14.9.2 Candidate genes associated with drought tolerance.................................. 328 14.10 Proteomic studies.................................................................................................... 330 14.11 Breeding approaches for developing drought-tolerant superior germplasm ......... 331 14.11.1 Marker-assisted selection......................................................................... 331 14.11.2 Genome-wide selection............................................................................ 331 14.12 Conclusion and future prospects ............................................................................ 332 References........................................................................................................................... 336

CHAPTER 15 The Use of Chlorophyll Fluorescence Kinetics Analysis to Study the Performance of Photosynthetic Machinery in Plants .............................................................................. 347 Hazem M. Kalaji, Anjana Jajoo, Abdallah Oukarroum, Marian Brestic, Marek Zivcak, Izabela A. Samborska, Magdalena D. Cetner, Izabela Łukasik, Vasilij Goltsev, Richard J. Ladle, Piotr Da˛browski and Parvaiz Ahmad 15.1 15.2 15.3 15.4

Introduction ............................................................................................................ 347 Chlorophyll a fluorescence and the heterogeneity of PSII ................................... 349 Analysis of chlorophyll fluorescence kinetics....................................................... 350 Examples of successful applications of ChlF measurements................................ 351 15.4.1 Drought....................................................................................................... 351 15.4.2 Salinity........................................................................................................ 356 15.4.3 Heavy metals .............................................................................................. 358 15.4.4 Nutrient deficiency..................................................................................... 359 15.4.5 Photosynthetically active radiation............................................................ 363 15.4.6 Temperature................................................................................................ 367 15.4.7 Ozone.......................................................................................................... 369 15.4.8 Herbicides................................................................................................... 370 15.5 Conclusion and future prospects............................................................................ 370 Abbreviations.................................................................................................................... 371 References......................................................................................................................... 372

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CHAPTER 16 Manipulating Osmolytes for Breeding Salinity-Tolerant Plants...... 385 Noushina Iqbal, Shahid Umar and Rahat Nazar 16.1 16.2 16.3 16.4 16.5

Introduction ............................................................................................................ 385 Salinity-induced ionic and osmotic stress and tolerance mechanisms ................. 386 General description of osmolytes .......................................................................... 388 The role of inorganic osmolytes in salinity tolerance........................................... 389 Organic osmolytes in salinity tolerance................................................................. 391 16.5.1 Proline in salinity tolerance ....................................................................... 391 16.5.2 Glycinebetaine in salinity tolerance .......................................................... 392 16.5.3 Carbohydrates and salinity tolerance......................................................... 393 16.6 Conclusion and future prospects............................................................................ 395 Acknowledgments ............................................................................................................ 395 References......................................................................................................................... 395

CHAPTER 17 Osmolyte Dynamics: New Strategies for Crop Tolerance to Abiotic Stress Signals ...................................................................... 405 Resham Sharma, Renu Bhardwaj, A.K. Thukral, Neha Handa, Ravdeep Kaur and Vinod Kumar 17.1 Introduction ............................................................................................................ 405 17.2 Osmoprotectants in plants ...................................................................................... 406 17.2.1 Sugars and polyols ..................................................................................... 406 17.2.2 Amino acids, peptides, and amines ........................................................... 409 17.2.3 Quaternary ammonium compounds ........................................................... 411 17.3 Metabolic expression and exogenous application of osmoprotectants under abiotic stresses.............................................................................................. 412 17.3.1 Temperature stress ..................................................................................... 412 17.3.2 Water deficit............................................................................................... 414 17.3.3 Salinity stress ............................................................................................. 416 17.3.4 Heavy metal stress ..................................................................................... 418 17.3.5 Pesticide toxicity ........................................................................................ 419 17.4 Conclusion and future prospects............................................................................ 420 References......................................................................................................................... 421

CHAPTER 18 The Emerging Role of Aquaporins in Plant Tolerance of Abiotic Stress .................................................................................... 431 ˇ Nada Surbanovski and Olga M. Grant 18.1 Introduction ............................................................................................................ 431 18.2 Aquaporins.............................................................................................................. 432 18.2.1 Structure and water-conducting properties of aquaporins......................... 432 18.2.2 Plant aquaporins ......................................................................................... 433

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18.2.3 Aquaporins in the plantwater relationship.............................................. 434 18.2.4 Aquaporins’ response to abiotic stress ...................................................... 436 18.2.5 Aquaporins in tolerance of abiotic stress .................................................. 439 18.3 Conclusion and future prospects............................................................................ 440 References......................................................................................................................... 441

CHAPTER 19 Prospects of Field Crops for Phytoremediation of Contaminants ..................................................................................... 449 Poonam, Renu Bhardwaj, Resham Sharma, Neha Handa, Harpreet Kaur, Ravdeep Kaur, Geetika Sirhindi and A.K. Thukral 19.1 19.2 19.3 19.4 19.5

Introduction ............................................................................................................ 449 Contaminants in soil, water, and plants................................................................. 450 Phytoremediation: a green technology .................................................................. 452 Field crops as hyperaccumulators and their potential for phytoremediation........ 453 Facilitated phytoextraction in crops....................................................................... 455 19.5.1 Chelating agents ......................................................................................... 455 19.5.2 Growth-promoting bacteria and mycorrhizae............................................ 459 19.5.3 Plant growth regulatory substances ........................................................... 460 19.5.4 Molecular techniques ................................................................................. 462 19.6 Conclusion and future prospects............................................................................ 463 References......................................................................................................................... 463

CHAPTER 20 Sustainable Soil Management in Olive Orchards: Effects on Telluric Microorganisms ...................................................................... 471 Adriano Sofo, Assunta Maria Palese, Teresa Casacchia and Cristos Xiloyannis 20.1 Introduction ............................................................................................................ 471 20.2 Sustainable management systems .......................................................................... 472 20.3 Using in situ compost production .......................................................................... 476 20.4 Conclusion and future prospects............................................................................ 477 References......................................................................................................................... 478

CHAPTER 21 The Vulnerability of Tunisian Agriculture to Climate Change ........ 485 Mohsen Mansour and Mohamed Hachicha 21.1 Introduction ............................................................................................................ 485 21.2 Tunisia’s agricultural constraints ........................................................................... 486 21.2.1 Climate ....................................................................................................... 486 21.2.2 Water resources and distribution ............................................................... 486 21.2.3 Agricultural characteristics ........................................................................ 490

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21.3 The impact of climate change on wheat production in Tunisia’s semiarid region ....................................................................................................... 491 21.4 Climatic change parameters that influence evapotranspiration in central Tunisia’s coastal region ......................................................................................... 493 21.5 Conclusion and future prospects............................................................................ 497 References......................................................................................................................... 498 Index .................................................................................................................................................. 501

Preface Before the onset of agriculture, Man was a forager. Man used wild animals and plants to aid survival. This was the only issue to satisfy his hunger. Some 10,000 years ago, Man started to live in groups around the world, beginning to gather and cultivate cereals, along with domesticated animals for meat, milk, skin, etc. From that period, agriculture became the most important part of life. The changes from a nomadic to very settled way of life form started due to early agricultural practices. Now you can see how much development has taken place in agriculture. We have every possible type of machinery, a multitude of technologies, and the latest methods to produce more and more food. But no matter how developed we are, there are still people suffering from malnutrition in developing and underdeveloped countries. Soil, from which we cultivate our food, is decreasing in size as well as in fertility, all because of environmental fluctuations. Biotic and abiotic stresses are increasing to an alarming rate, thus affecting the soil fertility, turning once-cultivable land into uncultivated. The environmental stresses also affect plant growth and development and ultimately lead to decreases in crop yields worldwide. Another problem to tackle in this modern developed world is population growth. The human race is increasing at such a pace that in coming years, the population on this planet will be too big to satisfy its hunger. In an attempt to combat this grave situation, scientists around the globe started a mission to develop plants that can give higher yields and can also grow on the marginal lands. These scientists have developed the latest technologies and methods to fight back against these stresses that affect the yield. The latest techniques will help us understand the molecular, physiological, and biochemical pathways that can be manipulated to meet our agricultural needs. In this regard we have compiled a two-volume work from different scientists around the world to give insights into this new breed of technology. Emerging Technologies and Management of Crop Stress Tolerance: Volume II Sustainable Agriculture throws light on the different recent technologies used for the development of crop yield under a multitude of environmental stresses and other recent methods to be used for this purpose. This volume comprises 21 chapters and a brief outline of each chapter is given below. Chapter 1 is regarding the improvement of legume crop production under environmental stresses through biotechnological intervention. Here the author discusses the major stresses affecting legume crop production and biotechnological interventions to resist biotic and abiotic stress in legumes. Chapter 2 discusses abiotic stress tolerance in plants, looking at the insights that have come from proteomics. The topics such as plant responses to abiotic stresses and proetomic analysis of plant responses to abiotic stresses is well explained by the authors. Chapters 38 deal with different endophytic microbes, plant growth-promoting bacteria and mycorrhiza in alleviating the abiotic stress in plants. The role of antimycorrhizal fungi in phytoremediation of heavy metals is also discussed. The biological control of fungal disease by rhizobacteria under saline soil conditions is also well explained. Chapter 9 deals with prevention of potential diseases of crop plants under the impact of changing environment. Here the authors have discussed major crops and techniques involved in the

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prevention of hazardous stress to crops. Chapter 10 discusses plant responses to metal stress, in particular the emerging role of plant growth hormones (auxins, gibberellins and cytokinins) in toxicity alleviation. Chapter 11 deals with reactive nitrogen species and role of nitrous oxide in mitigating the effect of abiotic stress. Chapter 12 explains the role of tocopherol (vitamin E) in plants in abiotic stress tolerance and beyond. The chemistry and types of tocopherol, tocopherol biosynthesis and accumulation in plants is also explained. Chapter 13 throws light on land and water management strategies for the improvement of crop production. Here, the authors explain strategies for the improvement of crop production in waterdeficient and water-logging agroecosystems. Chapter 14 discusses integrating physiological and genetic approaches for improving drought tolerance in crops. Here in this chapter, authors have explained drought stress in changing environments and the response to water deficits, evaluation methodologies for screening genotypes under drought stress and key physiological attributes for targeted breeding programs. Chapter 15 deals with the use of chlorophyll fluorescence kinetics analysis to study the performance of photosynthetic machinery in plants. Here the authors discuss chlorophyll fluorescence and the heterogeneity of PSII, the analysis of chlorophyll fluorescence kinetics, and give examples of successful applications of chlorophyll fluorescence measurements. Chapters 16 and 17 are about osmotic and ionic stress induced by abiotic stress in plants. The role of different inorganic and organic osmolytes in mitigation of abiotic stress is also discussed. Chapter 18 deals with emerging role of aquaporins in plant tolerance to abiotic stress. The structure and water conducting properties of aquaporins, and their place in plant-water relations is also discussed very well. Chapter 19 explains the prospects of field crops being used for phytoremediation of contaminants. Here the authors have discussed contaminants in soil, water and plants, and potential for phytoremediation. Chapter 20 deals with sustainable soil management in olive orchards, in particular the effects on telluric microorganisms. Finally, Chapter 21 throws light on vulnerability of Tunisian agriculture to the changing climate. This volume is the compilation of different perspectives from around the globe that directly or indirectly lead us to understand the mechanism of plant stress tolerance and mitigation of these dangerous stresses through sustainable methods. This volume will be beneficial for students, teachers of colleges and universities, environmentalists and also for those working in agro-industries. We have left no stone unturned in giving the final shape to this volume. However, we feel that there might be room for improvement, and in this regard we seek indulgence and feedback from the readers so that we can keep their comments in mind for coming volumes. We are very much thankful to our contributors who have devoted their valuable time in preparing their chapters and bearing the editors’ corrections and suggestions as well. We owe our gratitude to Nancy Maragioglio (Acquisitions Editor, Elsevier), Carrie Bolger (Editorial Project Manager, Life Sciences, Elsevier), Melissa Read (Freelance Project Manager, Elsevier) and all the other staff members of Elsevier, who were directly or indirectly associated with the project for their constant help, valuable suggestions and timely publication of this volume. Parvaiz Ahmad Saiema Rasool

Acknowledgments We acknowledge all the contributors of this volume for their valuable contributions. Parvaiz Ahmad also acknowledges the Higher Education Department, Government of Jammu and Kashmir, India for their support.

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About the Editors Dr. Parvaiz Ahmad is Senior Assistant Professor in the Department of Botany at Sri Pratap College, Srinagar, Jammu and Kashmir, India. He has completed his postgraduated study in Botany in 2000 at Jamia Hamdard, New Delhi, India. After receiving a Doctorate degree from the Indian Institute of Technology, Delhi, India, he joined the International Centre for Genetic Engineering and Biotechnology, New Delhi, in 2007. His main research area is Stress Physiology and Molecular Biology. He has published more than 35 research papers in peer-reviewed journals and 29 book chapters. He is also an editor of 12 volumes (1 with Studium Press Pvt. India Ltd., New Delhi, India, 8 with Springer USA and 3 with Elsevier USA). He is a recipient of the Junior Research Fellowship and Senior Research Fellowship by CSIR, New Delhi, India. Dr. Ahmad has been awarded the Young Scientist Award under the Fast Track scheme in 2007 by the Department of Science and Technology, Government of India. Dr. Ahmad is actively engaged in studying the molecular and physio-biochemical responses of different agricultural and horticultural plants under environmental stress. Dr. Saiema Rasool is currently teaching plant science in the Education department, Government of Jammu and Kashmir India. Dr. Rasool completed her Masters in Botany at Jamia Hamdard New Delhi, India in 2007, specializing in plant stress physiology. She has eight research publications to her credit, published in various international and national journals of repute. She has also published 7 book chapters in international published volumes from publishers such as Springer, Elsevier and Wiley. At present, her research interests are mainly focused on the development of abiotic stress tolerant plants and the physiological and biochemical responses of crop plants to a range of biotic and abiotic stresses.

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List of Contributors Elsayed Fathi Abd-Allah Plant Production Department, College of Food and Agricultural Sciences, King Saud University, Riyadh, Saudi Arabia Fakiha Afzal Atta-ur-Rahman School of Applied Biosciences, National University of Sciences and Technology, Islamabad, Pakistan Mohammad Abass Ahanger School of Studies in Botany, Jiwaji University, Gwalior MP India Parvaiz Ahmad Department of Botany, S. P. College, Srinagar, Jammu and Kashmir, India Sania Ahmed Pir Mehr Ali Shah Arid Agriculture University, Rawalpindi, Pakistan Ahmad Ali Center for Plant Sciences and Biodiversity, University of Swat, Khyber Pakhtunkhwa, Pakistan Zeshan Ali Ecotoxicology Research Institute, National Agricultural Research Centre, Islamabad, Pakistan Patrick Audet Northern Forestry Centre, Canadian Forestry Service, Natural Resources Canada, Edmonton, Canada Renu Bhardwaj Department of Botanical and Environmental Sciences, Guru Nanak Dev University, Punjab, India Marian Brestic Department of Plant Physiology, Faculty of Agrobiology and Food Resources, Slovak Agricultural University, Nitra, Slovak Republic Teresa Casacchia Freelance Nutritionist, Presidente Associazione, Nutrizione Umana, Cosenza, Italy Magdalena D. Cetner Department of Plant Physiology, Faculty of Agriculture and Biology, Warsaw University of Life Sciences, Warsaw, Poland Devendra Kumar Chauhan Department of Botany, University of Allahabad, Allahabad, India Devendra Kumar Choudhary Department of Science, Faculty of Arts, Science and Commerce, Mody University of Science and Technology, Lakshmangarh, Sikar, Rajasthan, India

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Piotr Da˛browski Department of Environmental Improvement, Warsaw University of Life Sciences, Warsaw, Poland Murat Dikilitas Department of Plant Protection, Faculty of Agriculture, Harran University, S. Urfa, Turkey Dilfuza Egamberdieva Faculty of Biology and Soil Sciences, National University of Uzbekistan, Tashkent, Uzbekistan Vilim Filipovic University of Zagreb, Faculty of Agriculture, Zagreb, Croatia Masayuki Fujita Laboratory of Plant Stress Responses, Department of Applied Biological Science, Faculty of Agriculture, Kagawa University, Kita-gun, Kagawa Savita Gangwar Department of Plant Science, MJP Rohilkhand University, Uttar Pradesh, India Vasilij Goltsev Department of Biophysics and Radiobiology, Faculty of Biology, St. Kliment Ohridski University of Sofia, Sofia, Bulgaria Olga M. Grant UCD Forestry, School of Agriculture and Food Science, University College Dublin, Dublin, Ireland Mohamed Hachicha National Institute on Rural Engineering Water and Forest, Tunis, Tunisia Neha Handa Department of Botanical and Environmental Sciences, Guru Nanak Dev University, Punjab, India Mirza Hasanuzzaman Department of Agronomy, Faculty of Agriculture, Sher-e-Bangla Agricultural University, Dhaka, Bangladesh Abeer Hashem Botany and Microbiology Department, College of Science, King Saud University, Riyadh, Saudia Arabia J.F. Hausman Department Environment and Agro-biotechnologies, Centre de Recherche Public, Belvaux, Luxembourg Memoona Ilyas Pir Mehr Ali Shah Arid Agriculture University, Rawalpindi, Pakistan


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Noushina Iqbal Department of Botany, Jamia Hamdard, New Delhi, India Shekhar Jain Department of Science, Faculty of Arts, Science and Commerce, Mody University of Science and Technology, Lakshmangarh, Sikar, Rajasthan, India Anjana Jajoo School of Life Sciences, Devi Ahilya University, Indore, India Hazem M. Kalaji Department of Plant Physiology, Faculty of Agriculture and Biology, Warsaw University of Life Sciences, Warsaw, Poland Sema Karakas Department of Soil Science and Plant Nutrition, Faculty of Agriculture, Harran University, S. Urfa, Turkey Amrita Kasotia Department of Science, Faculty of Arts, Science and Commerce, Mody University of Science and Technology, Lakshmangarh, Sikar, Rajasthan, India Harpreet Kaur Department of Botanical and Environmental Sciences, Guru Nanak Dev University, Punjab, India Ravdeep Kaur Department of Botanical and Environmental Sciences, Guru Nanak Dev University, Punjab, India Alvina Gul Kazi Atta-ur-Rahman School of Applied Biosciences, National University of Sciences and Technology, Islamabad, Pakistan Maria Khalid Atta-ur-Rahman School of Applied Biosciences, National University of Sciences and Technology, Islamabad, Pakistan Azka Khan Atta-ur-Rahman School of Applied Biosciences, National University of Sciences and Technology, Islamabad, Pakistan Vinod Kumar Department of Botanical and Environmental Sciences, Guru Nanak Dev University, Punjab, India Sarita Kumari Department of Science, Faculty of Arts, Science and Commerce, Mody University of Science and Technology, Lakshmangarh, Sikar, Rajasthan, India

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Richard J. Ladle Institute of Biological and Health Sciences, Federal University of Alagoas, Maceio´, Brazil; School of Geography and the Environment, University of Oxford, Oxford, UK Izabela Łukasik Racławicka 106, 02-634 Warsaw, Poland Riffat N. Malik Environmental Biology and Ecotoxicology Laboratory, Department of Environmental Sciences, Faculty of Biological Sciences, Quaid-i-Azam University, Islamabad, Pakistan Mohsen Mansour Regional Research Centre on Horticulture and Organic Agriculture, Chott Meriem, Tunisia Jagat Narayan Maurya Department of Plant Science, MJP Rohilkhand University, Uttar Pradesh, India Abdul Mujeeb-Kazi Wheat Wide Crosses, National Institute of Biotechnology and Genetic Engineering, Faisalabad, Pakistan G.V. Nagamallaiah Department of Botany, Yogi Vemana University, Kadapa, India Kamrun Nahar Department of Agricultural Botany, Faculty of Agriculture, Sher-e-Bangla Agricultural University, Dhaka, Bangladesh; Laboratory of Plant Stress Responses, Department of Applied Biological Science, Kagawa University, Kita-gun, Kagawa Rahat Nazar Department of Botany, Jamia Hamdard, New Delhi, India Gabrijel Ondrasek University of Zagreb, Faculty of Agriculture, Zagreb, Croatia Abdallah Oukarroum ´ ´ Quebec ´ Department of Chemistry and Biochemistry, University of Quebec, Montreal, Assunta Maria Palese Dipartimento delle Culture Europee e del Mediterraneo: Architettura, Ambiente, Universita´ degli Studi della Basilicata, Matera, Italy Daniela Pavlı´kova´ Faculty of Agrobiology, Food and Natural Resources, Czech University of Life Sciences Prague, Prague, Czech Republic Dragutin Petosic University of Zagreb, Faculty of Agriculture, Zagreb, Croatia


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Poonam Department of Botanical and Environmental Sciences, Guru Nanak Dev University, Punjab, India ´ Dagmar Prochazkov a´ Institute of Experimental Botany, Academy of Sciences of the Czech Republic, Prague, Czech Republic Sheo Mohan Prasad Ranjan Plant Physiology and Biochemistry Laboratory, Department of Botany, University of Allahabad, Allahabad, India Umar M. Quraishi Department of Plant Sciences, Faculty of Biological Sciences, Quaid-i-Azam University, Islamabad, Pakistan M. Dhanunjay Rao Department of Botany, Yogi Vemana University, Kadapa, India Khola Rafique Pir Mehr Ali Shah Arid Agriculture University, Rawalpindi, Pakistan Sammia Rehman Atta-ur-Rahman School of Applied Biosciences, National University of Sciences and Technology, Islamabad, Pakistan Zed Rengel School of Earth and Environment, University of Western Australia, Perth, Western Australia Izabela A. Samborska Department of Plant Physiology, Faculty of Agriculture and Biology, Warsaw University of Life Sciences, Warsaw, Poland K. Sergeant Department Environment and Agro-biotechnologies, Centre de Recherche Public, Belvaux, Luxembourg P.S. Sha Valli Khan Department of Botany, Yogi Vemana University, Kadapa, India Adeena Shafique Atta-ur-Rahman School of Applied Biosciences, National University of Sciences and Technology, Islamabad, Pakistan Resham Sharma Department of Botanical and Environmental Sciences, Guru Nanak Dev University, Punjab, India Hassan Sher Center for Plant Sciences and Biodiversity, University of Swat, Khyber Pakhtunkhwa, Pakistan

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Vijay Pratap Singh Government R.P.S P.G. College, Baikunthpur, India Geetika Sirhindi Department of Botany, Punjabi University, Punjab, India Adriano Sofo Freelance Nutritionist, Presidente Associazione ‘Nutrizione Umana’, Cosenza, Italy Jan Sumaira Department of Botany, Jamia Hamdard, New Delhi, India ˇ Nada Surbanovski Research and Innovation Centre, Fondazione Edmund Mach, San Michelle all’Adige, Trentino, Italy ´ Jiˇrina Szakov a´ Faculty of Agrobiology, Food and Natural Resources, Czech University of Life Sciences Prague, Prague, Czech Republic A.K. Thukral Department of Botanical and Environmental Sciences, Guru Nanak Dev University, Punjab, India Durgesh Kumar Tripathi Department of Botany, University of Allahabad, Allahabad, India Shahid Umar Department of Botany, Jamia Hamdard, New Delhi, India Anookul Vaishnav Department of Science, Faculty of Arts, Science and Commerce, Mody University of Science and Technology, Lakshmangarh, Sikar, Rajasthan, India Nad’a Wilhelmova´ Institute of Experimental Botany, Academy of Sciences of the Czech Republic, Prague, Czech Republic Cristos Xiloyannis Dipartimento delle Culture Europee e del Mediterraneo: Architettura, Ambiente, Universita´ degli Studi della Basilicata, Matera, Italy Marek Zivcak Department of Plant Physiology, Faculty of Agrobiology and Food Resources, Slovak Agricultural University, Nitra, Slovak Republic Sobia Zulfiqar Pir Mehr Ali Shah-Arid Agriculture University, Rawalpindi, Pakistan

CHAPTER

Improvement of Legume Crop Production Under Environmental Stresses Through Biotechnological Intervention

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Adeena Shafique, Sammia Rehman, Azka Khan and Alvina Gul Kazi

1.1 Introduction With more than 20,000 species, legumes are the third largest family of higher plants. Owing to their important biological features, legumes represent the most valuable food sources consumed globally, ensuring food security to almost every part of the world. Because of their importance for humans and animals, legumes complement cereal crops as a source of dietary protein and contribute substantially to total protein intake, mainly in vegetarian diets. Legumes have an intriguing array of features, the most conspicuous being their ability to fix atmospheric nitrogen to ammonia through their interaction with specific soil-borne bacteria, the rhizobia, consequently ameliorating soil fertility (Gonzalez-Rizzo et al., 2009). Such symbiotic interactions also help them to thrive in harsh and fragile environments. As such, legumes are a pivotal component of the ecosystem and sustainable agriculture worldwide and are of immense importance for providing food to the ever-growing population. Legumes are also a significant source of fodder and are grown on a large scale in the semiarid tropics (SAT) including Africa, Asia, and Latin America. Legumes provide mineral micronutrients and macronutrients (Grusak, 2002; Wang et al., 2003; Le et al., 2007) as well as health-promoting secondary metabolites (Deavours and Dixon, 2005; Sato et al., 2007). Many of these metabolites are known to protect plants against ambush by pathogens and pests (He and Dixon, 2000). To improve the productivity of legumes, biological and mechanistic key phenotypic features of the plants have been studied during the last decade. The productivity of legume crops, however, has not been significantly increased due to biotic as well as abiotic stress constraints for at least 50 years (FAO, 2012). Research in the past few years has focused on model legumes, which have subsequently resulted in the establishment of extensive genetic and genomic resources. Studies have also discovered critical genes in the symbiotic pathways and stress responses. For example, studying the germplasm of Medicago truncatula resulted in identification of the genes crucial to responses to stress (de Zélicourt et al., 2012).

P. Ahmad (Ed): Emerging Technologies and Management of Crop Stress Tolerance, Volume 2. DOI: http://dx.doi.org/10.1016/B978-0-12-800875-1.00001-6 © 2014 Elsevier Inc. All rights reserved.

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CHAPTER 1 Improvement of Legume Crop Through Biotechnological Intervention

1.2 Major stresses affecting legume crop production Biotic and abiotic stresses equally affect legume crop production but getting rid of all stress is not practically feasible. The most common approach to eliminating biotic stressors includes mortalitybased strategies. In almost all cases, this technique puts serious selection pressure on the subject (e.g., pests), leading to evolution that makes legumes more tolerant and adaptable to a given pressure. Stress can be defined as a physiological mechanism that can cause yield loss in crops. A number of stressors team up to cause stress in plants. On a larger scale, removing stress can be more helpful for increasing crop production compared to eradicating a stressor, or a couple of stressors, alone.

1.3 Biotic stresses for legumes Biotic stress is defined as a stress that is caused in plants due to damage instigated by other living organisms, including fungi, bacteria, viruses, parasites, weeds, insects, and other native or cultivated plants (Newton et al., 2011). All around the world in dry lands, the major food crops cultivated and consumed are grain legumes. A key threat to development and growth of these crucial crops is the ever-changing climate. The legume crops can be affected by climate in two ways (Kudapa et al., 2013): (1) increased crop susceptibility to novel diseases and (2) increased prevalence of diseases, parasites, and pests. There is a rising consensus that these issues may, in the future along with increasing abiotic stresses, add up to disease and pest pressure. Most grain legumes have a very low resistance to diseases and a narrow genetic base. It is important to conduct research on these crops to determine ways to improve their development. Fortunately, recent biotechnological tools and other approaches that facilitate plants’ responses against deadly diseases have benefited grain legume research significantly. Improving grain legume production globally requires inspection of various genes to select them for genetic engineering so that plants can be made more disease resistant (Licourt et al., 2011). Many of the diseases found in legume crops can be managed by better resistance, and because there is a high variability in legume pathogens, combined methods of resistance are required.

1.3.1 Fungi As fungi cannot make their own food, they develop certain strategies to obtain it from either living or dead organisms. Some consume wood and dead leaves, while others cultivate a mutual relationship with living plants. There is another group of fungi—the phytopathogenic fungi—that steal food from plants through attack and parasitism. The ascomycetes and basidiomycetes groups of fungi are the majority of plant pathogenic strains. Parasitic fungi attack almost all plant organs. A parasitic fungus can enter the plant’s body by making a hole in the epidermis or through the stomata, and its spores in the air attack leaves. Some can grow within roots and block the waterconducting cells’ xylem, resulting in a wilted plant. Table 1.1 provides some examples of important phytopathogenic plants along with diseases and affected organs. The effect of aerial fungal diseases on crop yield varies according to cropping region and years, but some fungi cause diseases in all legume-producing countries and can lead to extensive damage both in quantity and quality.

1.3 Biotic stresses for legumes

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Table 1.1 Fungal Infections in Plant Organs Parasitic Fungi

Plant Organ

Disease

Amillaria sp. Phytophthora, rhizoctonia, and pythium Epichloe typhina Phragmidium Taphrina confusa

Roots Roots and stem Stem Leaves Flowers

Root rot Damping off diseases Choke disease Rust Flower and leaf distortion

Table 1.2 Genus Uromyces Infects a Number of Legume Crops Fungus

Host Legume

U. U. U. U. U. U.

Chickpea Common beans Alfalfa Pea Cow pea Faba bean, lentils

ciceris—arietini appendiculatus striatus pisi vignae viciae fabae

1.3.2 Foliar diseases In legume-producing countries, the major limiting factors are the foliar diseases caused by biotrophic fungi (e.g., downy mildews, powdery mildews, rust). Fungal diseases, such as rot in the root, stem, or crown and vascular wilt and blight, are normally found in legumes. Climate plays an important role in determining which type of rust species may prevail in a region. Erysiphe pisi, for example, causes powdery mildew and is prevalent in regions with dry, hot days and cool nights, whereas Peronospora viciae, the agent for downy mildew, prevails in regions with cool maritime climates. Rust species target grain and forage legumes, especially the genus Uromyces. Table 1.2 shows a number of rust species along with the host legumes. Ascochyta rabie, one of the top necrotrophic fungi, causes Ascochyta blight in a number of grain legumes (e.g., pea and chickpea). Another widespread foliar disease, botrytis gray mold, is caused by Botrytis cinerea. In a survey in Queensland, Australia, it was found that Medicago sp. were parasitized by fungi such as Colletotrichum trifolii, Oidium sp., Stemphylium vesicarium, Uromyces striatus, and Uromyces anthyllidis, and Pseudopeziza medicaginis, Colletotrichum destructivum, and Rhizoctonia solani caused disease in Ornithopus sp. and Oidium sp. in Trifolium subterraneum (Mackie et al., 1999). On annual medics, the most frequently observed and prevalent disease was rust (Mackie et al., 1999).

1.3.3 Plant viruses Just the same as animal viruses, plant viruses are obligate intracellular parasites because they lack the machinery required to self-replicate without a host. They consist of a protein coat (capsid) that

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surrounds the genome (DNA/RNA). Most plant viruses are either ssRNA or dsRNA; very few are ssDNA and no dsDNA plant virus has been discovered yet. Due to the presence of a cell wall, it is difficult for a plant virus to move within plant cells. Virus transmission among plants can be horizontal through an external source (e.g., insects, nematodes, plasmodiophorids, seeds, pollens) or vertical from parent to young plant (i.e., via seed infection). Common symptoms presented by plants when infected with a virus include changes in leaf color (mottling, mosaic, vein clearing, leaf spots), changes in leaf morphology (rolling, curling, distortion, puckering, enation), and others (stunting, reduced yield, stem pitting). Every year billions of dollars are lost due to decrease in crop yield through virus infection. Plant viruses cause physiological and metabolic changes that show symptoms. These symptoms may involve direct or indirect effects that disrupt the host physiology (Conti et al., 2012). Most legume crop yield drops are caused by viruses. Cowpea is infected by the blackeye cowpea mosaic strain of bean common mosaic viruses. It is a noteworthy seed-borne virus that is transmitted among plants by infected seeds and aphids (Udayashankar et al., 2010). According to surveys carried out in 2009, it was confirmed that viruses, such as beet western yellow, alfalfa mosaic, pea seed-borne mosaic, bean yellow mosaic, cucumber mosaic, subterranean clover stunt, and soybean dwarf, are found in western Victoria and in South Australia. The most prevalent is the bean leafroll virus (BLRV). The potential vector for the transmission of BLRV was found to be Acyrthosiphon kondoi (Peck et al., 2012). Based on research in Nepal, sweet bean was found to be infected with the bean common mosaic necrotic virus causing symptoms including leaf and mottle deformation, necrosis, severe mosaic, leaf curling, malformation of pods and leaves, and leaf size reduction with an incidence percentage of 60 to 70% (Pudashini et al., 2013). Bean golden mosaic virus (BGMV) causes golden mosaic in the common bean. In Latin America, BGMV is a major limiting factor for bean production because it causes extensive yield losses (Aragaõ et al., 2013). Peanut stem necrosis disease and sterility mosaic disease have also affected a number of grain legumes around the world. Plant viruses are spreading every year due to their evolution and increased vector population. The diversity among legume-infecting viruses is on the rise due to interspecies and intergenera genomic recombination (Atkinson and Urwin, 2012).

1.3.4 Insects and pests Any organism (animal or plant) that is a competitor of humanity is called a pest. Insects, such as thrips, mealy bugs, aphids, scale insects, and spider mites, are some of the common examples of plant-infecting insects. They cause damage to plants by feeding as vectors directly (disease transmission) and providing infection sites to disease-causing agents. About 940% of crop yield loss is caused in the Indo-Gangetic plain by insect pests (together or alone). In this area, damage to plant leaves, stems, pods, and flowers is the result of various pests: leaf folder (Hedylapta indicator), blister beetle (Mylabris pustulata Thunberg), girdle beetle (Obereopsis brevis), green bug (Nezara viridula L.), and tobacco caterpillar (Spodoptera litura Fab.). Important pests that harm grain legumes include aphids (e.g., Aphis glycine); pod borers (e.g., Helicoverpa armigera and H. Punctigera), which target legumes that normally grow in cool seasons; and weevils (e.g., Apiom godmani and Zabrodes subfasciatus), which target legumes that

1.4 Biotechnological interventions for biotic stress tolerance in legumes

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grow in warm weather. More than 5000 species of thrips exist in the world out of which only 14 species belonging to genera Thrips and Frankliniella have been identified as vectors of the toposvirus (Riley et al., 2011).

1.3.5 Parasitic weeds The forage and grain legumes in West Asia and the Mediterranean region are infected by some broomrape species such as Orobanche foetida, Orobanche crenata, and Phelipanche aegyptiaca. Almost all the leguminous plants are infected by Orobanche crenata (Ho¨niges et al., 2012). Orobanche foetida, prevalent in the Mediterranean region, parasitizes wild herbaceous legumes (e.g., faba bean). It has caused yield losses in the range of 66 to 90% in the Beja region of Tunisia (Abbes et al., 2009). Parasitic weeds, Alectra vogelii and Striga gesnerioides, have been shown to decrease legume crop yield in semiarid zones of sub-Saharan Africa.

1.4 Biotechnological interventions for biotic stress tolerance in legumes To face hostile conditions, scientists and researchers have tried to build resistance against diseases in crops as part of breeding programs. Those initiated to improve crop breeds have been failing mainly because knowledge about plants’ mechanism to fight stress is quite limited and the study of genetic variations is insufficient. The modern plant-breeding era requires molecular approaches. Biotechnology has advanced in recent years and traditional breeding practices are now being replaced by methods to fight stress, be it biotic or abiotic (Basu, 2012). The most desirable method to fight biotic stresses in legumes is genetic resistance because it requires no chemicals—that is, it is environmentally friendly and has also proved to be very effective during the past few years. The basis of resistance along with related quantitative trait loci (QTL) have been identified (Libault et al., 2009; Kudapa et al., 2013; Varshney and Kudapa, 2013). Yield improvement has been achieved using breeding programs such as pure line breeding, population breeding, and mutation breeding. Hybridization techniques to grow more tolerant plants have also been implemented recently. The combination of modern breeding and the use of genomic tools has led to the production of superior legume varieties and reduced breeding cycles.

1.4.1 Focus on fungal stress Fungal foliar diseases are a major threat to legumes and cause immense yield loss. Although pests also affect crops’ productivity, their overall impact on yield loss is quite low compared to that caused by pathogenic fungi. Fungi are also difficult to deal with because they can infect just about any part of the plant at any stage of its life. More than 50% of loss in chickpeas is caused by the fungal disease Ascochyta blight in North Africa, West Asia, and the Mediterranean regions (Pande et al., 2009). Foliar diseases also cause up to 40% yield losses in alfalfa fields. Examples of legumes, along with fungal stresses and strategies to fight them, are discussed next.

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1.4.1.1 Chickpea Chickpea (Cicer arietinum L.) is consumed widely as a rich source of protein all around the world and is ranked third among the most important food legumes (Jain et al., 2013). Its cultivation is done on a large scale as it has a major market in south Asian countries (e.g., India and Bangladesh) (Hossain et al., 2011). Having the genome size of 738 Mb, chickpea is a self-pollinated (diploid) crop (Varshney et al., 2009) and is mainly cultivated in South Asia, the Middle East, North Africa, North and Central America, and the Mediterranean regions. Chickpea seeds consist of 24.6% protein, 64.6% carbohydrate, and vitamins (Abu-Salem and Abou, 2011). They also contain minerals such as magnesium, calcium, potassium, zinc, phosphorus, and iron. Fungi, viruses, bacteria, mycoplasmas, and nematodes are among the major pathogens of chickpea that cause economic losses globally (Nene et al., 2012). Ascochyta rabiei, a necrotrophic ascomycete fungus, causes a very lethal soil-borne and foliar disease in chickpea called Ascochyta blight. This fungus produces enzymes (e.g., cutinase, pectinase, and xylanase) to degrade the plant cell wall. It also produces toxins, for example, Solana pyrones A, B, C, and phytotoxins that kill host tissue. To counter Ascochyta’s attack, chickpea naturally produces an acidic fluid secreted from glandular trichome. Chickpea also very rapidly produces some antifungal chemicals—isoflavones and phytoalexins—that have resistance against this pathogen.

1.4.1.1.1 Resistance to Ascochyta blight Identification of resistant germplasm and the study of genetics in order to produce resistant chickpea varieties is a crucial step to fight this disease. More than one gene controls resistance to Ascocyhta blight in chickpea. Based on inheritance studies, two complementary recessive genes have been shown to make chickpea resistant (Deschamps et al., 2010; Ali et al., 2011; Hiremath et al., 2011). Ascochyta blight-associated QTL markers, double podding, and a simple sequence repeat (SSR) map are being used for chickpea molecular breeding. Ascochyta blight is a complex trait so its molecular breeding is done by QTL selection in a segregating progeny. The strategy used is marker-assisted backcrossing (MAB). Factors, such as flanking or closely linked markers, number of backcrossings, population size, and number and position of markers for background selection, are important aspects that determine MAB effectiveness (Taran et al., 2013). Ascochyta rabiei has high variability due to the presence of a sexual phase (i.e., Didymella rabiei). The use of resistant varieties of chickpea has also put selection pressure on this fungus; it produces three pathotypes—pathotypes I, II, and III—with virulence specificities in certain chickpea cultivars. A new pathotype IV has been confirmed that is said to be highly devastating (Imtiaz et al., 2011). Wild gene pools are being searched for and efforts are being made to utilize a combination of minor and major genes in the breeding program. Based on genetic analysis, three genes of chickpea, which are present on linkage groups II and IV in the genetic makeup, have been identified that give resistance against this deadly pathogen. Modern approaches have been used to isolate and clone the possible genes that confer resistance. Bacterial artificial chromosome (BAC) libraries are among these methods. If the genes are characterized properly, in the future they can serve as diagnostic markers for Ascocyhta blight. Gene markers can also be used for marker-assisted selection (MAS) to make chickpea more resistant to Ascochyta blight. Some of the examples include randomly amplified polymorphic DNA (RAPD) markers and inter-specific-sequence-repeat (ISSR) markers as well as isozyme markers.

1.4 Biotechnological interventions for biotic stress tolerance in legumes

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A CaETR-1 sequence (conferring resistance against Ascochyta blight) has been characterized by sequencing chickpea genome in two varieties with accession P1359075 and FLIP84-92c. The genetic position of this sequence has also been determined and is said to be in the LG IV region in QTLAR1 (Madrid et al., 2012).

1.4.1.2 Alfalfa Alfalfa (Medicago sativa) is a major forage legume that is grown worldwide. After corn and soybean, alfalfa has been ranked third (in dollar value) in the United States. Being important for crop rotation due to its symbiotic nitrogen-fixation capability, alfalfa also serves as hay and pasture for animals. Forage production drops every year because of certain pathogens (e.g., pests and fungi) that infect alfalfa. Understanding molecular and genetic mechanisms to introduce resistance into alfalfa breeds can help to control the diseases. Alfalfa is an autotetraploid (2n 5 4 3 5 32) and has an outcrossing nature; its genetic system is interactable so its close relative, Medicago truncatula, is commonly used to study resistance in alfalfa. A major stress to all the legumes is a result of fungal and oomycete pathogens. In the past, germplasms of M. truncatula have been collected to identify different responses against pathogens. Studies have been done on (1) identification of defense genes and related QTL responsible for resistance in the host and (2) resistance mechanisms from the cellular to the molecular level. Anthracnose is a plant disease caused by a fungus called Colletotrichum trifolli. This disease is considered to be very destructive and widespread around the globe. It starts off with stem and leaf lesions, progresses to form root and crown rot, and later results in plant death. It can cause about 25 to 30% loss (Yang et al., 2007). Moreover, interaction of this deadly disease with the environment and other diseases increases stress on the host plant. C. trifolli races 1 and 2 were identified in North America in 1979, race 3 in 1982, and race 4 in Australia and the United States in 2003 and 2006, respectively. Studies show that two dominant genes, An1 and An2, control resistance to C. trifolli in alfalfa—An1 for race 1 and An2 for both races 1 and 2. In the past, An1 has been also shown to contribute to resistance against race 4 (Mackie et al., 2007; Tesfaye et al., 2007). These authors also mapped the QTL associated with resistance in autotetraploid alfalfa against C. trifolli races 1, 2, and 4.

1.4.1.2.1 Resistance to anthracnose As a reaction to anthracnose pathogenesis, alfalfa gives both compatible (induced resistance) and incompatible (hypersensitive) reactions. Alfalfa produces pterocarpen and isoflavonoid phytoalexins after the fungus attacks it. Not much is known about the mechanisms used by the host for pathogen recognition and triggering responses against it. If characterization and cloning experiments are carried out, only then can we comprehend the complex mechanism of host recognition and move forward toward disease control in the alfalfa species. One limitation to producing resistant cultivars of alfalfa is the emergence of new pathotypes of C. trifolli. Single major genes have been found to give resistance to M. truncatula against C. trifolii and P. medicaginis by RCT1 and the rnpm1 gene, respectively. The RCT1 gene of M. truncatula has been transferred to alfalfa and has been shown to give it resistance against anthracnose. A major cause of plant mortality is Collectotrichum crown rot disease. Studies have shown that if selection is done for stem anthracnose resistance, it will also contribute to resistance against

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Collectotrichum crown rot. The increase in anthracnose resistance is accomplished by the “recurrent selection method.” Resistant breeds have been grown in North America, Europe, and Australia. Random insertional mutagenesis of C. triffoli was done using Agrobacterium-mediated transformation in order to study its gene function (Takahara et al., 2004). Insertional mutagenesis has been used in the past to study all genes related to pathogenesis; for example, genes having the function of cell wall destruction, infectious structure formation, toxin production, or overcoming the host defense system. Among all techniques for random mutagenesis, Agrobacterium tumefacien-mediated transformation proved to be the best to analyze genes of filamentous fungi.

1.4.1.2.2 Use of Medicago truncatula to study resistance to other pathogenic fungi The quantitative trait loci rendering resistance to Medicago truncatula are being mapped, especially resistance to fungal pathogens including U. striatus, P. trifoilum, E pisi, and so on. Scientists are trying to identify molecular mechanisms using transcriptomic and proteomic approaches (BustosSanmamed et al., 2013). Resistance against A. enteiches has been studied in which the subtractive suppression hybridization (SSH) library has been used. It showed that pathogen-related proteins of group 10 (PR10) and proteins related to abscisic acid signaling are crucial to give resistance to legumes against fungal diseases. Study of comparative proteomics and the use of the gene-silencing approach have proved that PR10 silencing increases plants’ resistance by antagonistically inducing other pathogenesis-related (PR) genes. Using the macroarray technique, the expression profiles of 92 genes important for resistance in M. truncatula have been compared. Anderson et al. (2005) noted the important role of pathogenesis-related proteins, especially PR10, in making the plant resistant. Macroarray experiments have shown that there is an up-regulation of a high number of genes that act on the membrane in resistant Medicago plants and vice versa in the susceptible strain. Postgenomic strategies to overcome fungal diseases (e.g., M. pinodes and U. striatus) also have been used. Ongoing research gives us hope that plants can be made disease-tolerant by enhancing their resistance, but there are still some hurdles to cross. Long genetic distance between identified genetic markers and resistance QTLs, lack of codominant markers, and an overall lack of information limits the use of genetic markers to introduce resistance into plants. Table 1.3 summarizes the biotic stresses affecting the legume crops along with the biotechnological interventions for their improvement.

1.5 Abiotic stresses in legumes Abiotic stresses, such as heat, drought, salinity, cold, waterlogging, frost, chilling, herbicides and pesticides, and others, have been hampering legume productivity and making grounds for enormous loss of economically important crops each year. Among all the abiotic stresses, the most devastating are extreme temperature, water deficit, high salinity, and submergence that affect all stages of plant growth and development. Extreme temperatures (e.g., intense heat and frost) hinder potential crop yield (Feldmann et al., 2009). As an increasingly limited resource, water scarcity has affected crop production in many parts of the world. In addition to water scarcity, millions of hectares in humid regions in South and

1.5 Abiotic stresses in legumes

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Table 1.3 Major Fungal Stresses to Chickpea and Alfalfa Crops Stress

Legume Crop Affected

Legume Organ Affected

Ascochyta blight (AB)

Chickpea

Anthracnose

Alfalfa

Leaf, stem, and pod Seed (if severe) Stem

Technique Molecular breeding for resistance Molecular breeding for resistance

Note: The modern biotechnological technique to overcome these stresses is enhancing crop resistance via molecular breeding.

Southeast Asia are left uncultivated or have very low productivity due to salinity (FAO, 2012). Further, crops exposed to abiotic stresses are more prone to weeds, pests, and diseases, which considerably lowers the potential yield (Feldmann et al., 2009). To cope with scarce water resources, agricultural research institutes have put efforts into optimizing water availability for irrigation and to determining alternative sources of water. Generally traditional approaches are used by the breeders of legume crops. They grow different varieties and cross them to evaluate the best progenies with varying abilities to withstand stress constraints (Li et al., 2010). Then the best adaptable varieties are selected and applied to grow crops in fields exposed to stresses. Nevertheless, biotechnologists have a broader vision to produce genetically engineered crops using advanced genome sequencing and genotyping technology for far better yield. Crops may also survive for longer periods even under adverse abiotic stresses. Because they grow in dynamic and uncontrolled environments, often an array of stresses impedes the development of plants. Abiotic stress constraints have been a serious issue to major legume crops (e.g., soybean, groundnut, peanut, pigeon pea, and chickpea), decreasing yield stability of the SAT regions that includes 55 developing countries. It is estimated that only 10% of arable land is listed under the nonstress category, implying that the other 90% for crop production undergoes one or more environmental stresses resulting in dramatic decreases in potential yield (Dita et al., 2006). Various abiotic stress constraints are discussed in detail in the next section.

1.5.1 Drought Among all abiotic stress constraints, drought, or limited water, for all legume crops is of immense significance. Drought negatively influences economically important legume crops such as soybean, groundnut, and peanut (Xoconostle-Cazares et al., 2011). Being a serious dilemma, drought needs to be dealt with for potentially better legume production. Biotechnological tools provide practical alternatives for the production of sustainable drought-tolerant plants, a promising solution to alleviate the issues of water limitation (Hamidou et al., 2013). To attain the objectives for

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drought-tolerant varieties, biotechnologists have exploited molecular tools to study the biological basis of drought tolerance (Agbicodo et al., 2009).

1.5.2 Salinity Salinity has been a serious threat to agriculture; it affects crop growth and yield particularly in the arid and semiarid regions of the world. Soil salinization has rendered many acres of land unusable and poses a serious threat to food security (Duzan et al., 2004). Salinity has a major effect on legume biology as it affects the legume symbiotic interaction with soil bacteria that results in nitrogen fixation (Dolferus et al., 2011). Salt stress particularly affects nodule formation and reduces both the number of nodules and the amount of nitrogen fixed. Salt stress can also cause water deficit in plants resulting in secondary oxidative stress. These effects disturb the plants’ normal physiology and development. There is a dire need to devise strategies to help with the production of salt-resistant crops (Sobhanian et al., 2011).

1.5.3 Temperature Cold is yet another stress that perturbs legumes’ biology. Low temperature affects growth and development and disturbs the normal functioning of metabolic and physiological processes of legumes. Heat stress has also been a substantial challenge for the breeders of legume crops (Kumar et al., 2012). Transitory or constant increases in temperature variability cause a number of morphoanatomical modifications that affect the growth and production of many warm season legume crops (e.g., chickpea, cowpea, and groundnut) all around the world. It is estimated that the global air temperature has increased by 0.65 C over the last century. Rising temperature has turned out to be a global concern, and it is assumed that by the end of this century, an increase in higher temperatures may result in more vulnerable crops (Qu et al., 2013). The adverse effects of heat stress on economically important crops can be alleviated through the generation of thermotolerant crops using different biotechnological approaches.

1.6 Biotechnological interventions for abiotic stress tolerance in legumes Abiotic stresses equally impede crop growth and yield and have detrimental effects on normal plant physiology. It is imperative to improve crop growth using biotechnological approaches. Expanding population density and increasing demand of legume crops for food purposes worldwide has motivated the community of researchers to initiate an intensive effort to develop legume crops that are more resistant to abiotic stresses. Unfortunately, many of the stresses are more likely to occur in developing countries because climatic conditions seriously constrain legume productivity in subSaharan Africa and many parts of the Indian subcontinent. The economic states of these countries restrict the use of resource-intensive inputs, including irrigation systems and advanced fertilizers that help counteract the aforementioned constraints. An important solution to this problem is that the next generation of improved legume crop genotypes must be better equipped with endogenous capabilities to tolerate abiotic stresses (Varshney et al., 2009).

1.6 Biotechnological interventions for abiotic stress tolerance in legumes

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Recent advances in plant functional genomics and meticulous understanding of molecular mechanisms that control certain genes play a crucial role in the survival of crops in extreme environments. These advances have led to the development of innovative and advanced mitigating strategies for the improvement of legume crops with abiotic stress-tolerance characteristics.

1.6.1 Soybean Soybean (Glycine max) is an inexpensive vegetable protein and oil source. It is used as a staple food in the diet for humans and animal husbandry. Cultivation of soybean is done in more than 100 countries and territories around the world, with a total estimated occupied area of more than 92.5 million ha and a stable yield of 217.6 million metric tons each year (average yield of 2346 kg/ha). The major producers of soybean are the United States, Brazil, and Argentina, accounting for nearly 81% of global yield. Other top producers are China, India, Paraguay, Canada, Bolivia, Ukraine, and Indonesia. A remarkable reduction in the potential yield of soybean seeds (B2450%) has been reported through greenhouse and field studies in different regions and at various times (Ku et al., 2013). Different hybrids of soybean require 450 to 700 mm of water during the growing season. Water deficiency affects the flowering and post-flowering stages the most. Many morphological changes in the vegetative part and the reduction in seed quantity and quality of soybean under drought stress have been studied extensively (Ku et al., 2013). Interestingly, drought stress during flower induction, flowering, pod formation, and pod filling stages of growth has not seemed to affect the protein or oil content of soybean seeds. Further, drought has a very slight effect on the composition of fatty acid; however, high temperatures reduce the polyunsaturated content (Manavalan et al., 2009). The genomics of soybean have been studied many times because of its agronomic importance and demand. Modern molecular biology and genetics have facilitated the identification of many recent molecular markers and some functional genes related to drought tolerance in soybean (Ku et al., 2013).

1.6.1.1 Response to drought Soybean, the same as other plants, has numerous defense mechanisms that enhance tolerance to water deficiency (Soleimanzadeh et al., 2010). These mechanisms either induce or repress the expression of different genes, which helps plants adapt to stress constraints (Le et al., 2012a). In the initial events of plant responses to drought, stress signals are sensed and subsequent signaling pathways are activated, resulting in the activation of various molecular, biochemical, and physiological responses (Le et al., 2012b).

1.6.1.1.1 Biotechnological intervention for drought resistance The genetic makeup of soybean germplasm differs due to spatial adaptations to diverse habitats. The diversity of the germplasm has expedited the productivity of soybean plants that are more resistant to drought. Wild soybean exhibits higher allelic diversity and has better sexual compatibility compared to cultivated soybean (Singh et al., 2013). Wild soybean has served as a good genetic source and has been exploited through conventional breeding to produce varieties with several drought-tolerant characteristics. Conventional breeding, being a tedious and laborious method, needs to be replaced by prompt and efficient biotechnological techniques (Ku et al., 2013). Biotechnological approaches emphasizing the development of transgenic crops in conditions akin

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to the field, along with focusing the reproductive stages, will greatly help improve the chances to produce stress-tolerant soybean crops (Boboye et al., 2011).

1.6.1.1.2 Marker-assisted selection for drought resistance Molecular biology and genetics have helped to overcome the problems associated with conventional breeding for the development of drought-resistant soybean. The latest genomics tools, availability of genomic sequences, and germplasm resources for soybean research along with transgenic technologies help with the genetic improvement of soybean. These approaches have become an economically attractive option for efficient soybean breeding (Gao et al., 2011). Marker-assisted selection has been an important plant breeding method during the last 20 years. It decreases variance among the selected trait, thus increasing the heritability of selectable traits as well as the rate of genetic gain. This enables the soybean plant to promote breeding by selecting lines only with a desired trait phenotype and is a desirable method of selection (Neus, 2010). The use of genomic analysis helps to identify DNA regions specifically related to agronomic traits in crops. The so-called molecular markers have greatly revolutionized breeding methods (Kumar et al., 2009). Many markers for the analysis of genetic diversity have been developed. Novel opportunities to manipulate QTLs to develop drought-resistant cultivars through biotechnological tools have positively facilitated breeding strategies for crop improvement (Le et al., 2012a). Transcriptomic tools are also being applied for the breeding of legume crops under various environmental abiotic stresses. Soybean has been more extensively studied for this purpose among all the legumes and, according to Legume Information System data, more than 1.3 million expressed sequence tags (ESTs) have been developed from various cDNA libraries (Lucas et al., 2011). Access to the immense number of ESTs and bacterial chromosome (BAC) sequences has been assisted by the discovery of new single-nucleotide polymorphism (SNP) and simple sequence repeat (SSR) markers in soybean, leading to the construction of high-resolution genetic maps (Reddy et al., 2012). Recent genomic studies have shown that the soybean species has an exceptionally high linkage disequilibrium (low recombination frequency). Therefore, marker-assisted breeding is a promising approach for the development of drought-resistant soybean. More than 200,000 tagged SNPs have also been identified for this purpose (Lam et al., 2012). Genotype and environment and the interaction of these two are key factors that determine the drought resistance phenomena of a certain crop. So MAS based on genotype could greatly increase the breeding efficiency of the soybean cultivar (Manavalan et al., 2009) Quantitative trait loci, which are related to drought resistance, are important for marker-assisted selection. A large number of QTLs have been identified for various traits related to agronomic, physiological, seed composition, and biotic and abiotic parameters in soybean (Muchero et al., 2009). However, only a few QTLs associated with drought tolerance have been reported to date. In this technique, DNA markers closely linked to the target QTLs are employed to accelerate the selection of progeny lines by reducing some of the time needed for phenotypic characterization (Ku et al., 2013). For instance, delayed wilting response of canopy is linked with drought tolerance (Carter et al., 2006). Four QTLs related to this trait associated with 16 SSR markers have also been mapped (Bhatnagar et al., 2005). One quantative trait loci identified in all tested environments is therefore a promising candidate for marker-assisted breeding for the delayed canopy wilting trait in different environments, including soil type and moisture level inadequacy (Du et al., 2009).


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1.6.1.2 Genetic engineering The database of genomic sequences from various plant species, including legume crops, is available. Their availability along with advanced microarray technologies have enabled researchers to identify genes associated with drought responses in a number of plant species including both model plants (e.g., Arabidopsis) (Matsui et al., 2008) and crops such as rice (Oryza sativa) (Degenkolbe et al., 2009). The complete soybean genomic sequence was elucidated several years ago by Schmutz (2010). Subsequently, the 66 K Affymetrix Soybean Genome Array platform was designed; it contains all the soybean genes annotated by the Glyma1 model. These available genetic resources have opened the way to developing drought-tolerant transgenic soybean through genetic engineering (Le et al., 2012a). Microarray is a high throughput approach used for screening and predicting the functioning of candidate genes. In one study by Le et al. (2012a), the overall transcriptome-wide changes in soybean leaves under drought conditions were observed with microarray analysis using the 66 K Affymetrix Soybean GeneChip. Drought stress was imposed on soybean plants from the late vegetative stage, V6, until the early bloom reproductive stage R1 and full bloom stage R2; the differential expression of genes under late vegetative conditions was studied. The duration from late vegetative to the end of full bloom stage is known to affect potential yield. This gives rise to the need to explore the mechanism of soybean response to drought stress during this period. The microarray data showed modifications at transcription levels of various well-known functional and regulatory genes, including transcription factors, kinases, heat shock proteins, late embryogenesis-abundant proteins, osmoprotectant biosynthesis-related proteins, hormone-related proteins, transporters, and detoxification enzymes. Comparative expression analysis of V6 and R2 microarray datasets was performed to find out the conserved and nonconserved sets of genes involved in regulation of drought response in different stages of plant development. This analysis was then expanded to the species level to identify conserved and species-specific drought-responsive genes in soybean and Arabidopsis by comparing soybean transcriptome datasets and those of drought-stressed Arabidopsis leaves. Research on the functions of the NAC Transcription Factor family members and genes involved in metabolism and signaling pathways of various hormones under drought stress has resulted in extensive analysis of the GmNAC Transcription Factor family and the hormone-related gene category. This analysis eventually provided excellent candidates for in-depth characterization and a basic foundation for the future development of enhanced drought-tolerant transgenic soybeans (Le et al., 2012b). Genetic engineering of a plant with transcription factors that regulate the expression of several genes related to abiotic stress defense is a promising strategy to develop drought tolerance in legume plants. Dehydration-responsive element-binding (DREB) is one of the important transcription factors, which specifically recognizes and binds as a single molecule to so-called drought, cold, and salt stressor responsive promoter elements with specific consensus sequences. DREB plays a central role in abiotic stress responses and regulates a large number of target stressresponsive genes. Due to the potential for combating abiotic stress in plants, DREBs have become popular for use in genetic engineering to ameliorate abiotic stress tolerance in many plant species (Morran et al., 2011). The performance of soybean plants overexpressing the TF DBEB1 A under drought conditions in the field and in the greenhouse was evaluated in a study by Rolla de Paiva et al. (2013).

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Although the DREB protein plants did not outperform the cultivars, BR16, in terms of yield, some components were increased when drought was introduced during the vegetative stage; for example, the number of seeds, the number of pods with seeds, and the total number of pods. The greenhouse data suggested that the higher survival rates of DREB plants is due to lower transpiration rates under well-watered conditions. Identification of ideal candidate genes that can improve drought tolerance but do not have a yield penalty when introduced into the soybean genome is one of the critical hurdles faced by the genetic engineering approach (Umezawa et al., 2006). Rapid gain-of-function experiments using heterologous model plant systems (tobacco, Arabidopsis, and rice) have been employed to screen for potential candidate genes. Instead of lower efficiency, established systems of soybean transformation were reported (Liu et al., 2009); this allows direct assessment of the protective functions of both native and heterologous genes in soybean. Some promising results using this approach have been observed, although all of them are at the experimental stage. AtMYB44 is a R2R3-type MYB transcription factor from A. thaliana that participates in the abscisic acid-mediated abiotic stress signaling pathways (Jung et al., 2008). Ectopic expression of AtMYB44 in soybean has been shown to improve drought tolerance and yet suffered from the reduced growth phenotype under normal conditions (Seo et al., 2012). Another transgenic soybean plant expressing the AtP5CR gene (encoding L-Δ1-pyrroline-5-carboxylate reductase) has resulted in increased tolerance to drought stress with significantly higher relative water content (Ku et al., 2013). The NTR1 gene from Brassica campestris, which encodes a jasmonic acid carboxyl methyltransferase, introduced into soybean resulted in increased accumulation of methyl jasmonate, thus enhanced tolerance toward dehydration during seed germination (Ku et al., 2013). Overexpression of the soybean gene GmDREB3 encodes a DREB transcription factor, which has been shown to enhance drought resistance along with the accumulation of proline (Ku et al., 2013). Because cytokinins (CKs) mediate several cellular responses to drought stress, drought-resistant cultivars may be generated by targeted control of cytokine metabolism. Through genetic engineering of various genes encoding cytokines, CK levels were manipulated to enhance drought tolerance in soybean cultivars. From the soybean genome, 14 cytokine biosynthetic (isopentenyltransferase, GmIPT) and 17 cytokine degradative (CK dehydrogenase, GmCKX) genes were identified. The GmIPT and GmCKX genes were compared with the Arabidopsis corresponding parts that brought out their similar architecture. The major events observed under abiotic stress were GmCKX up-regulation with reduced cytokine levels. It was found that the expression of 12 GmCKX genes was indeed up-regulated by dehydration in R2 roots (reproductive stage). Overall, the expression of soybean cytokine metabolic genes in various tissues during different stages of growth seemed to be highly responsive to water deficit (Le et al., 2012a). Along with the elevated expression of RNA-type GmIPT genes in soybean, minor concentrations of cis-zeatin and related compounds were discovered. The systematic analysis of the GmIPT and GmCKX families has provided significant insight into the CK metabolism in soybean under water-deficit conditions. This information has empowered scientists to understand the molecular mechanisms involving the metabolism and homeostasis of cytokines in various tissues at distinctive developmental stages under both normal and drought situations (Le et al., 2012a). Based on knowledge of these molecular mechanisms, suitable modulation of CK levels may be a promising approach for the genetic engineering of economically important soybean crops with better drought tolerance (Le et al., 2012b).


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Even though numerous genes associated with plants’ response to drought have been identified and characterized, they need to be further employed with different biotechnological tools to develop drought-tolerant plants. The successful production of drought-tolerant crops has been limited despite technologies that have provided novel opportunities. Nevertheless, triumph in generating some drought-resistant cultivars through genetic manipulation has been achieved, taking into account the low number of transgenic crops introduced into the market so far.

1.6.2 Cowpea Cowpea (Vigna unguiculata) is an important food and animal feed crop widely cultivated worldwide. The ability to withstand water deficit and adapt to warm weather makes cowpea a potential crop of drier regions (Vadez et al., 2012). Cowpea is an important legume crop grown in semiarid tropical areas in 45 countries in Asia, Africa, Europe, the United States, and Central and South America. An estimated 14.5 million ha of land is used for planting of cowpea each year. The sub-Saharan African region accounts for about 84% and the remaining countries account for 14% of cowpea production. The productivity of cowpea has not seen sustained growth over the last two decades because of various abiotic stress constraints. Heat stress has become a serious problem for cowpea cultivation. High temperatures along with drought have remarkably reduced the stable yield of cowpea (Devasirvatham et al., 2012).

1.6.2.1 Effect of heat High temperatures affect cowpea growth and hinder reproductive development the most (i.e., flowering and pod set). An increase in night temperature greater than 17 C significantly reduces both pod set and grain yield (Selvaraj et al., 2011). The main effects of high temperature on cowpea’s growth occur in the late night during the flowering stage, resulting in pollen sterility and anther indehiscence (Fischer, 2011). However, a high temperature along with drought cause protein and lipid degradation and generate reactive oxygen species (ROS) in cowpea (Diouf, 2011). Problems imposed by heat stress in cowpea production are being resolved by breeding. To minimize the adverse effects of heat on the growth of cowpea along with the increased global temperature, genomics and biotechnological tools need to be used to generate thermotolerant cowpea crops (Krishnamurthy et al., 2011).

1.6.2.1.1 Responses to heat stress The detrimental effects of heat stress are exacerbated by water deficit. The two stresses together make the cowpea plant more prone and invulnerable to other environmental stress constraints. Heat stress impacts the reproductive growth of cowpea and also produces secondary stresses (e.g., osmotic and oxidative) (Devasirvatham et al., 2012). To cope with heat stress, cowpea has some molecular and physiological mechanisms to reduce the number of the harmful effects of high temperatures. Through these molecular mechanisms, expression of many genes has altered and synthesized an array of stress-related proteins, such as heat shock proteins, participating in different pathways as a stress-tolerance strategy (Wahid et al., 2007). Many enzymes, nonenzyme proteins, antioxidants, and hormones are produced to resist high temperatures (Qu et al., 2013).

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1.6.2.1.2 Biotechnological interventions for heat stress Recent development of a consensus genetic map and efficient selection of cowpea through molecular breeding have remarkably assisted in the generation of heat-tolerant phenotypes. Moreover, there is a need to leverage the latest biotechnological tools to replace conventional breeding for the production of more resistant cowpea capable of surviving in marginal environments (Kumar et al., 2012). Elevated temperature has been the most substantial challenge to cowpea breeders because heat injury during the reproductive stages of development results in sterilized pollen with no fruit set. Inheritance of this trait and procedures for delivering resources for breeding cowpea with increased resistance to heat is being studied extensively (Mitchell et al., 2013). Quantitative trait loci analysis was performed using 141 individual plants from a recombinant population created from a cross between cowpea CB27 and IT82E-18 varieties; 9% of the cowpea genome is represented by five regions. They include 11.5 to 18.1% of the phenotypic variation, and these regions are tagged with 48 transcript-derived SNP markers (Muchero et al., 2011). Favorable alleles of tolerance-associated haplotypes for four of these regions were contributed by CB27, while tolerance represented by the fifth QTL was denoted by a more sensitive parent, IT82E. Combinations of fifth QTL (Cht-5) with any of the first four QTLs seemed to be more positively correlated with heat tolerance than the combination of any other two QTLs. Haplotypes associated with thermotolerance have been shown to be tagged with many SNP markers, which may be the basis for marker-assisted breeding for heat-tolerant cowpea. Combination of QTL in different breeding lines has been used to approach the mass potential of favorable haplotypes with the increased aptitude to set pods during high temperatures. In the soybean genome, there are some homologous regions that contain many important genes for heat tolerance. These genes also include several heat shock transcription factors (TFs), heat shock proteins, and proline transporters. Syntenic regions of the soybean genome were investigated to find potential candidate genes for heat tolerance (Lucas et al., 2013). Analyzing candidate regions of the genes known to take part in stress responses may support a consortium between genotype and phenotype. These candidate genes can provide a basic structure to carry out cloning and characterization of fundamental genetic factors. Because cowpea lacks the high-quality reference genome, information may be gathered by assessing synteny with some of the more extensively studied species. A number of studies have shown a relationship between the cowpea genome and several important model plants and crop species. Arabidopsis, Medicago truncatula, and Glycine max have shown plenty of gene annotations among these species (Lucas et al., 2011). Reference genome resources not only have appeared to be useful for cowpea studies but also have assisted some of the more closely related common beans (Phaseolus vulgaris) or mung beans (Vigna radiata) in improving the legume comparative genomics (Mitchell et al., 2013). Table 1.4 summarizes the abiotic stresses affecting the aforementioned legumes and the biotechnological interventions for their improvement.

1.7 Conclusion and future prospects Legumes are the most valued plants owing to their immense importance for humans and animals as food and forage sources, their soil ameliorative features, and their ability to thrive under delicate environmental conditions. Because of their key role in agriculture, efforts to improve legumes

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Table 1.4 Abiotic Stresses Affecting Legumes and Biotechnological Interventions Stress

Legume Crop Affected

Legume Organ Affected

Technique

Drought

Soybean

Leaf, stem, and pod

Heat

Cowpea

Pollen, anthers

Molecular breeding through MAS Genetic engineering Molecular breeding through MAS

began as early as 1960 using traditional breeding tools. In spite of these tremendous efforts, research in recent years has been directed to finding out gene pools and resources and to developing legume models to better equip these indispensable plants against environmental stressors. Model legumes have been instrumental in contributing to the knowledge of plantpathogen interactions. Medicago truncatula, in particular, has been remarkable for the identification of several pathogen-resistant genes and developing resistance to abiotic stresses. Although biotechnological interventions have been influential in overcoming the problems faced by legume crops, there is a substantial area for the improvement and development of better varieties that can adapt to numerous stresses, both biotic and abiotic through more significant research. Over the years, biotechnology has emerged as an instrumental tool to overcome stresses in plants. It is now possible to target almost any legume crop for genetic improvement with the help of such tools. For biotechnology to make its mark, it is essential to apply classical breeding methods and new interventions to the most pressing and appropriate problems. Molecular breeding is an essential part of modern biotechnology. The study of quantitative genetics has led to the identification of molecular markers to increase resistance of legumes to their respective pathogens. Enhancing resistance in both chickpea and alfalfa crops has proved to be successful; however, there are still some bottlenecks to overcome. A few of these bottlenecks are: lack of understanding with regard to plant stress mechanisms, genetic variation, and gene combination for crop improvement. To make molecular breeding a major success, agriculturists need to integrate the scientific fields— that is, research and expertise in genomics, statistics, stress biology, laboratory techniques, and field-based breeding practices (Moose and Mumm, 2008).

References Abbes, Z., Kharrat, M., Simier, P., 2009. Osmoregulation and nutritional relationships between Orobanche foetida and faba bean. Plant Signal. Behav. 4 (4), 336338. Abu-Salem, F.M., Abou, E.A., 2011. Physico-chemical properties of tempeh produced from chickpea seeds. Arab. J. Am. Sci. 7, 107118. Agbicodo, E.M., Fatokun, C.A., Muranaka, S., Visser, R.G.F., Van der, C., Linden, G., 2009. Breeding drought tolerant cowpea: constraints, accomplishments, and future prospects. Euphytica 167, 353370. Ali, Q., Ahsan, M., Basra, S.M.A., Elahi, M., Javid, N., Ahmed, W., 2011. Management of Ascochyta blight (Ascochyta rabiei) disease of chickpea (Cicer ariatinum L.). Int. J. Agro Vet. Med. Sci. 5 (2), 164183. Anderson, J.P., Thatcher, L.F., Singh, K.B., 2005. Plant defence responses: conservation between models and crops. Funct. Plant Biol. 32, 2134.

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Aragaõ, F.J.L., EOPL, Nogueira, Tinoco, M.L.P., Faria, J.C., 2013. Molecular characterization of the first commercial transgenic common bean immune to the Bean golden mosaic virus. J. Biotechnol. 166 (12), 4250. Atkinson, N.J., Urwin, P.E., 2012. The interaction of plant biotic and abiotic stresses: from genes to the field. J. Exp. Bot. 63 (10), 35233544. Basu, U., 2012. Identification of molecular processes underlying abiotic stress plants,adaptation using “Omics” technologies. In: Benkeblia, N. (Ed.), Sustainable Agriculture and New Technologies. CRC Press, Boca Raton, FL, pp. 149172. Bhatnagar, S., King, C.A., Purcell, L., Ray, J.D., 2005. Identification and mapping of Quantitative Trait Loci associated with crop response to water-deficit stress in soybean [Glycine Max (L.) Merr.]. The ASA-CSSA-SSSA International annual meeting poster abstract, November 6–10, 2005, Salt Lake City, UT, USA. Boboye, B.E., Ogundeji, B.A., Evbohoin, H., 2011. Mutational search for high temperature (60 C) tolerant variant of Rhizobium species CWP G34A. Adv. Biosci. Biotechnol. 2, 255262. Bustos-Sanmamed, P., Mao, G., Deng, Y., Elouet, M., Khan, G.A., Bazin, J., et al., 2013. Overexpression of miR160 affects root growth and nitrogen-fixing nodule number in Medicago truncatula. Funct. Plant Biol. 40, 12081220. Carter Jr., T.E., Orf, J., Purcell, L., Specht, J., Chen, P., Sinclair, T., et al., 2006. Tough times, tough plants— new soybean genes defend against drought and other stresses. In: American Seed Trade Association Conference Proceedings. Alexandria, VA. Conti, G., Rodriguez, M.C., Manacorda, C.A., Asurmendi, S., 2012. Transgenic expression of Tobacco mosaic virus capsid and movement proteins modulate plant basal defense and biotic stress responses in Nicotiana tabacum. J. Am. Phytopathol. Soc. 25 (10), 13701384. de Zélicourt, A., Diet, A., Marion, J., Laffont, C., Ariel, F., Moison, M., et al., 2012. Dual involvement of a Medicago truncatula NAC transcription factor in root abiotic stress response and symbiotic nodule senescence. Plant J. 70, 220230. Deavours, B.E., Dixon, R.A., 2005. Metabolic engineering of isoflavonoid biosynthesis in alfalfa. Plant Physiol. 138, 22452259. Degenkolbe, T., Do, P.T., Zuther, E., Repsilber, D., Walther, D., et al., 2009. Expression profiling of rice cultivars differing in their tolerance to long-term drought stress. Plant Mol. Biol. 69, 133153. Deschamps, S., Rota, M., Ratashak, J.P., Biddle, P., Thureen, D., Farmer, A., et al., 2010. Rapid genome-wide single nucleotide polymorphism discovery in soybean and rice via deep resequencing of reduced representation libraries with the Illumina Genome Analyzer. Plant Genome 3 (10), 5368. Devasirvatham, V., Gaur, P.M., Mallikarjuna, N., Raju, T.N., Trethowan, R.M., Tan, D.K.Y., 2012. Effect of high temperature on the reproductive development of chickpea genotypes under controlled environments. Funct. Plant Biol. 39, 10091018. Diouf, D., 2011. Recent advances in cowpea [Vigna unguiculata (L.) Walp.] “omics” research for genetic improvement. Afr. J. Biotechnol. 10 (15), 28032810. Dita, M.A., Rispail, N., Prats, E., Rubiales, D., Singh, K.B., 2006. Biotechnology approaches to overcome biotic and abiotic stress constraints in legumes. Euphytica 147, 124. Dolferus, R., Ji, X., Richards, R.A., 2011. Abiotic stress and control of grain number in cereals. Plant Sci. 181 (4), 331341. Du, W., Wang, M., Fu, S., Yu, D., 2009. Mapping QTLs for seed yield and drought susceptibility index in soybean (Glycine max L.) across different environments. J. Genet. Genomics 36 (12), 721731. Duzan, H.M., Zhou, X., Souleimanov, A., Smith, D.L., 2004. Perception of Bradyrhizobium japonicum Nod factor by soybean [Glycine max (L.) Merr.] root hairs under abiotic stress conditions. J. Exp. Bot. 55, 26412646.

References

19

Feldmann, F., Alforld, D.V., Furk, C., 2009. Crop plant resistance to biotic and abiotic factors: current potential and future demands. Proceedings of the Third International Symposium on Plant Protection and Plant Health in Europe. Julus Ku¨hn-Institut, Berlin-Dahlem, Germany. Fischer, R.A., 2011. Wheat physiology: a review of recent developments. Crop Past. Sci. 62, 95114. Food and Agricultural Organization of the United Nation (FAO), 2012. FAO Statistical Database. FAOSTAT, Geneva. Gao, S.Q., Chen, M., Xu, Z.S., Zhao, C.P., Li, L., Xu, L., et al., 2011. The soybean GmbZIP1 transcription factor enhances multiple abiotic stress tolerances in transgenic plants. Plant Mol. Biol. 7, 537553. Gonzalez-Rizzo, S., Laporte, P., Crespi, M., Frugier, F., 2009. Legume Root Architecture: A Peculiar Root System. Blackwell Publishing, Oxford, pp. 239287. Grusak, M.A., 2002. Photochemicals in plants: genomics-assisted plant improvement for nutritional and health benefits. Curr. Opin. Biotechnol. 13, 508511. Hamidou, F., Halilou, O., Vadez, V., 2013. Assessment of groundnut under combined heat and drought stress. J. Agron. Crop Sci. 199, 111. He, X.Z., Dixon, R.A., 2000. Genetic manipulation of isoflavone 7-O-methyltransferase enhances biosynthesis of 4’-O-methylated isoflavonoid phytoalexins and disease resistance in alfalfa. Plant Cell 12, 16891702. Hiremath, P.J., Farmer, A., Cannon, S.B., Woodward, J., Kudapa, H., Tuteja, R., et al., 2011. Large-scale transcriptome analysis in chickpea (Cicer arietinum L.), an orphan legume crop of the semi-arid tropics of Asia and Africa. Plant Biotechnol. J. 9 (8), 922931. Ho¨niges, A., Ardelean, A., Xi, X., Yoneyam, K., Yoneyam, K., Wegmann, K., 2012. Towards understanding orobanche host-specificity. Romanian Agric. Res. 29, 313322. Hossain, S., Panozzo, J., Pittock, C., Ford, R., 2011. Quantitative Trait Loci analysis of seed coat color components for selective breeding in chickpea (Cicer arietinum L.). Can. J. Plant Sci. 91 (1), 4955. Imtiaz, M., Abang, M., Malhotra, R.S., Ahmed, S., Bayaa, B., Udupa, S.M., et al., 2011. Pathotype IV, a new and highly virulent pathotype of Didymella rabiei, causing Ascochyta blight in chickpea in Syria. Am. Phytopathol. Soc. 95 (9), 11921193. Jain, M., Misra, G., Patel, R.K., Priya, P., Jhanwar, S., Khan, A.W., et al., 2013. A draft genome sequence of the pulse crop chickpea (Cicer arietinum L.). Plant J. 74 (5), 715729. Jung, C., Seo, J.S., Han, S.W., Koo, Y.J., Kim, C.H., Song, S.I., et al., 2008. Overexpression of AtMYB44 enhances stomatal closure to confer abiotic stress tolerance in transgenic Arabidopsis. Plant Physiol. 146 (2), 623635. Krishnamurthy, L., Gaur, P.M., Basu, P.S., Chaturvedi, S.K., Tripathi, S., Vadez, V., et al., 2011. Large genetic variation for heat tolerance in the reference collection of chickpea (Cicer arietinum L.) germplasm. Plant Genet. Resour. 9, 5961. Ku, Y.S., Au-Yeung, W.K., Yung, K.L., Li, M.H., Wen, C.Q., Liu, X., et al., 2013. Drought stress and tolerance in soybean. In: Board, J.E. (Ed.), A Comprehensive Survey of International Soybean ResearchGenetics, Physiology, Agronomy and Nitrogen Relationship. InTech, pp. 209237. Kudapa, H., Ramalingam, A., Nayakoti, S., Chen, W., Zhuang, W., Liang, X., et al., 2013. Functional genomics to study stress responses in crop legumes: progress and prospects. Funct. Plant Biol. 40 (12), 12211233. Kumar, P., Gupta, V.K., Misra, A.K., Modi, D.R., Pandey, B.K., 2009. Potential of molecular markers in plant biotechnology. Plant Omics J. 2 (4), 141162. Kumar, S., Thakur, P., Kaushal, N., Malik, J.A., Gaur, P., Nayyar, H., 2012. Effect of varying high temperatures during reproductive growth on reproductive function, oxidative stress and seed yield in chickpea genotypes differing in heat sensitivity. Arch. Agron. Soil Sci. 59, 823843.

20


Lam, H.M., Xu, X., Liu, X., Chen, W., Yang, G., Wong, F.L., et al., 2012. Resequencing of 31 wild and cultivated soybean genomes identifies patterns of genetic diversity and selection. Nat. Genet. 42 (12), 10531059. Le, B.H., Wagmaister, J.A., Kawashima, T., Bui, A.Q., Harada, J.J., Goldberg, R.B., 2007. Using genomics to study legume seed development. Plant Physiol. 144 (2), 562574. Le, D.T., Aldrich, D.L., Valliyodan, B., Watanabe, Y., Ha, C.V., 2012a. Evaluation of candidate reference genes for normalization of quantitative RT-PCR in soybean tissues under various abiotic stress conditions. PLoS ONE 7 (9), e46487. Le, D.T., Nishiyama, R., Watanabe, Y., Tanaka, M., Seki, M., et al., 2012b. Differential gene expression in soybean leaf tissues at late developmental stages under drought stress revealed by genome-wide transcriptome analysis. PLoS ONE 7 (11), e49522. Li, X., Shen, X., Li, J., Eneji, E., Li, Z., Tian, X., et al., 2010. Coronatine alleviates water deficiency stress on winter wheat seedlings. J. Integr. Plant Biol. 52 (7), 616625. Libault, M., Joshi, T., Stacey, G., 2009. Legume transcription factor genes: what makes legumes so special? Plant Physiol. 151 (3), 9911001. Licourt, A., Diet, A., Marion, J., Laffont, C., Ariel, F., Moison, M., et al., 2011. Dual involvement of a Medicago truncatula NAC transcription factor in root abiotic stress response and symbiotic nodule senescence. Plant J. 70, 220230. Liu, M., Yang, J., Cheng, Y., An, L., 2009. Optimization of soybean (Glycine max (L.) Merrill) in planta ovary transformation using a linear minimal gus gene cassette. J. Zhejiang Univ.-Sci. 10 (12), 870876. Lucas, M.R., Diop, N.N., Wanamaker, S., Ehlers, J.D., Roberts, P.A., Close, T.J., 2011. Cowpea-soybean synteny clarified through an improved genetic map. Plant Genome 4, 218225. Lucas, M.R., Elhers, J.D., Huynh, B., Diop, N.N., Roberts, P.A., Close, T.J., 2013. Markers for breeding heattolerant cowpea. Mol. Breed. 31, 529536. Mackie, J.M., Lloyd, D.L., Ryley, M.J., Irwin, J.A.G., 1999. Fungal diseases of temperate annual pasture legumes in southern Queensland. Aust. J. Exp. Agric. 39 (6), 699707. Mackie, J.M., Musial, J.M., Armour, D.J., Phan, H.T.T., Ellwood, S.E., Aitken, K.S., et al., 2007. Identification of QTL for reaction to three races of Colletotrichum trifolii and further analysis of inheritance of resistance in autotetraploid lucerne. Theor. Appl. Genet. 114, 14171426. Madrid, E., Rajesh, P.N., Rubio, J., Gil, J., Millán, T., Chen, W., 2012. Characterization and genetic analysis of an EIN4-like sequence (CaETR-1) located in QTLAR1 implicated in Ascochyta blight resistance in chickpea. Plant Cell Rep. 31 (6), 10331042. Manavalan, L.P., Guttikonda, S.K., Tran, L.P., Nguyen, H.T., 2009. Physiological and molecular approaches to improve drought resistance in soybean. Plant Cell Physiol. 50 (7), 12601276. Matsui, A., Ishida, J., Morosawa, T., Mochizuki, Y., Kaminuma, E., et al., 2008. Arabidopsis transcriptome analysis under drought, cold, high-salinity and ABA treatment conditions using a tiling array. Plant Cell Physiol. 49, 11351149. Mitchell, R., Lucas, J., Ehlers, D., Huynh, B.L., Diop, N.N., Roberts, P.A., et al., 2013. Markers for breeding heat-tolerant cowpea. Mol. Breed. 31, 529536. Moose, S.P., Mumm, R.H., 2008. Molecular plant breeding as the foundation for 21st century crop improvement. Plant Physiol. 147 (3), 969977. Morran, S., Eini, O., Pyvovarenko, T., Parent, B., Singh, R., Ismagul, A., et al., 2011. Improvement of stress tolerance of wheat and barley by modulation of expression of DREB/CBF factors. Plant Biotechnol. J. 9 (2), 230249. Muchero, W., Diop, N.N., Bhat, P.R., Fenton, R.D., Wanamaker, S., Pottorff, M., et al., 2009. A consensus genetic map of cowpea [Vigna unguiculata (L.) Walp.] and synteny based on EST-derived SNPs. Proc. Natl. Acad. Sci. U.S.A. 106 (43), 1815918164.

References

21

Muchero, W., Ehlers, J.D., Close, T.J., Roberts, P.A., 2011. Genic SNP markers and legume synteny reveal candidate genes underlying QTL for Macrophomina phaseolina resistance and maturity in cowpea [Vigna unguiculata (L.) Walp.]. BMC Genomics 12, 8. Nene, Y.L., Reddy, M.V., Haware, M.P., Ghanekar, A.M., Amin, K.S., Pande, S., et al., 2012. Field diagnosis of chickpea diseases and their control. Information Bulletin No. 28. Neus, J.D., 2010. Marker assisted selection for seed yield in soybean [Glycine max (L.) Merr.] plant row yield trails. Crop Sci. 48, 16491664. Newton, A.C., Johnson, S.N., Gregory, P.J., 2011. Implications of climate change for diseases, crop yields and food security. Euphytica 179, 318. Pande, S., Sharma, M., Kumari, S., Gaur, P.M., Chen, W., Kaur, L., et al., Integrated Foliar Diseases Management of Legumes. International Conference on Grain Legumes, Kanpur, India. Peck, D.M., Habili, N., Nair, R.M., Randles, J.W., Koning, C.T., Auricht, G.C., 2012. Bean leafroll virus is widespread in subterranean clover (Trifolium subterraneum L.) seed crops and can be persistently transmitted by bluegreen aphid (Acyrthosiphon kondoi Shinji). Crop. Sci. 63 (9), 902908. Pudashini, B.J., Shahid, M.S., Natsuaki, K.T., 2013. First report of Bean common mosaic necrosis virus (BCMNV) Infecting sweet bean in Nepal. Am. Phytopathol. Soc. 97 (2), 290. Qu, A.L., Ding, Y.F., Jiang, Q., Zhu, C., 2013. Molecular mechanisms of the plant heat stress response. Biochem. Biophys. Res. Commun. 432 (2), 203207. Reddy, D.S., Bhatnagar-Mathur, P., Vadez, V., Sharma, K.K., 2012. Grain legumes (soybean, chickpea, and peanut): Omics approaches to enhance abiotic stress tolerance. In: Tuteja, N., Gill, S.S., Tiburcio, A.F., Tuteja, R. (Eds.), Improving Crop Resistance to Abiotic Stress. Wiley-VCH Verlag GmbH & Co. KGaA, Weinheim, Germany, pp. 303305. Riley, D.G., Joseph, S.V., Srinivasan, R., Diffie, S., 2011. Thrips vectors of tospoviruses. J. Integr. Pest Manage. 2 (1), 110. Rolla de Paiva, A.A., de Fátima Correâ Carvalho, J., Fuganti-Pagliarini, R., Engels, C., do Rio, A., Marin, S.R., et al., 2013. Phenotyping soybean plants transformed with rd29A:AtDREB1A for drought tolerance in the greenhouse and field. Transgenic. Res. 23 (1), 7587. Sato, S., Nakamura, Y., Satoshi Tabata, S., 2007. Genome sequencing and genome resources in model legumes. Plant Physiol. 144 (2), 588593. Schmutz, J., Cannon, S.B., Schlueter, J., Ma, J., Mitros, T., et al., 2010. Genome sequence of the palaeopolyploid soybean. Nature 463, 178183. Selvaraj, M.G., Burow, G., Burke, J.J., Belamkar, V., Puppala, N., Burow, M.D., 2011. Heat stress screening of peanut (Arachis hypogaea L.) seedlings for acquired thermo tolerance. Plant Growth Regul. 65, 8391. Seo, J.S., Sohn, H.B., Noh, K., Jung, C., An, J.H., Donovan, C.M., et al., 2012. Expression of the Arabidopsis AtMYB44 gene confers drought/salt-stress tolerance in transgenic soybean. Mol. Breed. 29, 601608. Singh, P., Nedumaran, S., Ntare, B.R., Boote, K.J., Singh, N.P., Srinivas, K., et al., 2013. Potential benefits of drought and heat tolerance in groundnut for adaptation to climate change in India and West Africa. Eur. J. Agron. Part B 123137. Sobhanian, H., Aghaei, K., Komatsu, S., 2011. Changes in the plant proteome resulting from salt stress: toward the creation of salt-tolerant crops? J Proteomics 74, 13231337. Soleimanzadeh, H., Habibi, D., Ardakani, M.R., Paknejad, F., Rejali, F., 2010. Response of sunflower (Helianthus annus L.) to drought stress under different potassium levels. World Appl. Sci. J. 8 (4), 443448. Takahara, H., Tsuji, G., Kubo, Y., Yamamoto, M., Toyoda, K., Inagaki, Y., et al., 2004. Agrobacterium tumefaciens-mediated transformation as a tool for random mutagenesis of Colletotrichum trifolii. J. Gen. Plant Pathol. 70, 9396.

22


Taran, B., Warkentin, T.D., Vandenberg, A., 2013. Fast track genetic improvement of Ascochyta blight resistance and double podding in chickpea by marker-assisted backcrossing. Theor. Appl. Genet. 126, 16391647. Tesfaye, M., Liu, J., Vance, C.P., 2007. Genomic and genetic control of phosphate stress in legumes. Plant Physiol. 144 (2), 594603. Udayashankar, A.C., Nayaka, S.C., Kumar, H.B., Mortensen, C.N., Shetty, H.S., Prakash, H.S., 2010. Establishing inoculum threshold levels for bean common mosaic virus strain black eye cowpea mosaic infection in cowpea seed. Afr. J. Biotechnol. 9 (53), 89588969. Umezawa, T., Fujita, M., Fujita, Y., Yamaguchi-Shinozaki, K., Shinozaki, K., 2006. Engineering drought tolerance in plants: discovering and tailoring genes to unlock the future. Curr. Opin. Plant Biotechnol. 17 (2), 113122. Vadez, V., Jens, D.B., Warkentin, T., Asseng, S., Ratnakumar, P., Rao, K.P.C., et al., 2012. Adaptation of grain legumes to climate change: a review. Agron. Sustain. Dev. 32, 3144. Varshney, R.K., Kudapa, H., 2013. Legume biology: the basis for crop improvement. Funct. Plant Biol. 40 (12), vviii. Varshney, R.K., Close, T.J., Singh, N.K., Hoisington, D.A., Cook, D.R., 2009. Orphan legume crops enter the genomics era. Curr. Opin. Plant Biol. 12, 202210. Wahid, A., Gelani, S., Ashraf, M., Foolad, M.R., 2007. Heat tolerance in plants: an overview. Environ. Exp. Bot. 61, 199223. Wang, T.L., Domoney, C., Hedley, C.L., Casey, R., Grusak, M.A., 2003. Can we improve the nutritional quality of legume seeds? Plant Physiol. 131 (3), 886891. Xoconostle-Cazares, B., Ramirez-Ortega, F.A., Flores-Elenes, L., Ruiz-Medrano, R., 2011. Drought tolerance in crop plants. Am. J. Plant Physiol. 5, 241256. Yang, S., Gao, M., Deshpande, S., Lin, S., Roe, B.A., Zhu, H., 2007. Genetic and physical localization of an anthracnose resistance gene in Medicago truncatula. Theor. Appl. Genet. 116, 4552.

CHAPTER

Abiotic Stress Tolerance in Plants Insights from Proteomics

2

P.S. Sha Valli Khan, G.V. Nagamallaiah, M. Dhanunjay Rao, K. Sergeant and J.F. Hausman

2.1 Introduction Plants are confronted with abiotic stress factors, such as low water availability (drought), excess water (flooding/waterlogging), extremes of temperatures (cold, chilling, frost, heat), salinity, mineral deficiency, and toxicity, throughout their lives. It is predicted because of climate change that these abiotic stresses may become more intense and frequent. Climate change, whether naturally ensuing or due to anthropogenic activities, causes incredible challenges for agriculture worldwide. The emission of heat-trapping greenhouse gases (GHGs) increases the atmospheric concentration of CO2 as well as other GHGs. For example, according to Raman et al. (2012), methane (CH4) and nitrous oxides (NOx) are responsible for the significant increases in global temperature observed during the second half of the twentieth century, as reported by the International Panel on Climate Changes (IPCC, 2007). Climate models predict that the ambient air temperature of the Earth will likely rise 0.03 C or more per year in the future. The effects of global warming will not be restricted to increasing mean annual temperatures around the globe, but also will result in more extreme and more frequent hot and cold periods. The frequency and amplitude of temperature fluctuations will have profound consequences on rainfall patterns, natural ecosystems, agriculture, wildlife, and life in general (World Wide Fund for Nature, 2008). Consequently, because of rising temperatures and frequent flooding events for several decades, fertile agricultural land and crop yields may decrease rapidly, especially in the mid-latitudes (Kundzewicz et al., 2005). On the other hand, the population explosion has resulted in a higher demand for food and other natural resources. In addition to these factors, anthopogenic activities may lead to an increased abundance of soil, water, and air pollutants, factors that plants must cope with. A 2007 Food and Agriculture Organization (FAO) report stated that only 3.5% of the global land area is not affected by some environmental constraint. Moderate estimates propose that more than 90% of the land in rural areas is affected by abiotic stress factors at some point during the growing season (Cramer et al., 2011). Thus, understanding stress responses is essential when attempting to breed stress-resistant cultivars that can withstand abiotic stressors and in order to feed the growing population.


23

24

CHAPTER 2 Abiotic Stress Tolerance in Plants

2.2 Plant responses to abiotic stresses A stressor can be described as any factor that is outside the normal range of homeostatic control in a given organism. Once this threshold is surpassed, an organism is stressed and mechanisms are activated at molecular, biochemical, physiological, and morphological levels. The activation of the mechanisms can result in the establishment of a new physiological state and homeostasis is reestablished. The adverse effects of abiotic stresses bring about alterations in plant metabolism, growth, and development—ultimately, leading to plant death (Jogaiah et al., 2013). This is a particular concern in agriculture where stress-related alterations in plant development, growth, and productivity limit yield and can result in unacceptable economic losses. It has been estimated that abiotic stresses may limit crop production by as much as 70% and that many crops perform at only 30% of their genetic potential with regard to yield (Boyer, 1982). Plants can sense, respond to, and tolerate abiotic stresses in several ways; they are dynamic and complex and both elastic (reversible) and plastic (irreversible) (Cramer et al., 2011). Additionally, plant responses to stress are dependent on the tissue or organ affected by the stress, as well as its intensity and duration. Some plants (e.g., ephemerals) escape the effects of stress by completing their life cycle during less stressful periods. Alternatively, plants have evolved mechanisms to resist stress through either avoidance or tolerance. Stress avoidance necessitates mechanisms that isolate plant cells from the stressful conditions. This strategy minimizes the impact of it even though the stress is present in the environment. Stress-tolerant plants establish a new metabolic homeostasis in response to stress and thereby can continue to grow without suffering stress-induced injury. Tolerance mechanisms are coordinated and fine-tuned by adjusting growth, development, and cellular and molecular activities (Levitt, 1980). Stress adaptation and acclimation are two different ways of achieving tolerance to a particular stress. Stress adaptation encompasses heritable adaptations in structure or function thus enhancing plants’ ability to thrive in the stressful environment. Stress acclimation, on the other hand, means plants change in nonheritable physiological ways over their life span. These modifications are achieved through gradual exposure to the stress and permit that plant to survive and reproduce in stressful environments. The sensing of abiotic stress conditions induces signaling cascades that activate ion channels, kinase cascades, production of reactive oxygen species (ROS), and accumulation of plant hormones. These signals, ultimately, induce expression of specific subsets of genes that lead to the assembly of the overall defensive reaction (Figure 2.1). Significant progress has been made in understanding the physiological, cellular, and molecular mechanisms of plant responses to environmental stress factors (Hadiarto and Tran, 2011). The detection of a stressful condition results in variations in gene expression, causing changes in the composition of plant transcriptome, proteome, and metabolome. The advent of the novel “omic” technologies permits researchers to investigate the complex interplay between the plant and its metabolism; likewise, this allows the identification of the transcriptional, proteomic, and metabolic networks linked to stress perception and response. The investigation of changes in plant proteome is extremely important because proteins, unlike transcripts, are direct effectors of the stress response. Proteins not only include enzymes that catalyze changes in metabolite levels, but also include components of the transcription and translation machinery and molecules that are important for maintenance of the plant cells’ structure. The proteome-level description of plants’ reactions on exposure to stress conditions therefore

2.3 Proteomic analysis of responses to abiotic stresses

Abiotic stresses

25

Secondary stresses

lonic stress

Oxidative stress

Osmotic stress

Mechanical stress

Heat

Signal sensing Cold Heavy metals

Signal transduction

Mineral nutrition imbalance

Transcription

Salinity

Stress responsive genes / Proteins expression

Drought

Flooding

Cell death

Acclimation survival

FIGURE 2.1 Plant responses to abiotic stresses.

significantly contributes to our understanding of the physiological mechanisms underlying their stress tolerance (Kosova et al., 2011).

2.3 Proteomic analysis of responses to abiotic stresses The term “proteome” (PROTEins expressed by genOME) represents the survey of the expression of all proteins in cells/tissues/organisms at a given time and condition (Wilkins et al., 1996). Proteomics has several advantages over the genome-based technologies because it directly focuses on functional molecules rather than genetic code or mRNA abundance. Proteomics has been applied to the field of crop abiotic stress-tolerance research for comparative analyses of different proteomes. The most common case involves comparison of proteomes isolated from nonstressed (control) plants and the corresponding proteomes under stress conditions. Other cases include comparison of proteomes from two different genotypes or plant species with contrasting levels of tolerance to a given stress factor (e.g., Arabidopsis thaliana as a plant species sensitive to salt stress versus Thellungiella halophila as a plant species tolerant to salt stress). The studies aimed at the comparison of several proteomes generally use 2-DE (2 dimensional gel electrophoresis) followed by protein identification using mass spectrometry (MS) analysis. Several reviews concerning plant proteome responses to various abiotic stress factors have been published (Vitamvas et al., 2007a; Timperio et al., 2008; Kosova et al., 2011; Nanjo et al., 2011a; Hakeem et al., 2012a; Komatsu and Hossain, 2013).

26


In the following subsections of this chapter, studies dealing with plant proteome changes in response to the impact of several abiotic stress factors—water (drought, flooding/waterlogging), salinity, excessive or deficient levels of mineral nutrients, enhanced concentrations of heavy metals, and temperature extremes (cold and heat)—are summarized and, where possible, we provide an update to information about the contribution of proteomic studies for unraveling the mechanisms underlying plants’ stress responses.

2.3.1 Water stress Water has many chemical and physical properties that make it an appropriate medium in which life can exist. It is vital to a plant because water is the most abundant compound in the cytosol where important biochemical reactions take place, and its hydraulic properties impel cell expansion and offer a structural foundation to cells. From a practical standpoint, water stress is a major abiotic stress factor that limits crop production worldwide. Water stress may arise through either limited water availability (i.e., a condition known as drought) or an excess of water (i.e., a condition known as waterlogging). Plant species are highly variable with respect to their optimum environments and their susceptibility to water availability extremes.

2.3.1.1 Drought stress Drought is the main abiotic stressor around the world and drastically reduces grain yields. It devastatingly influences the capability to meet the food demands of an ever-increasing global population (Tester and Langridge, 2010). Drought stress is associated with water deficit and cellular dehydration. Plant adaptation to drought is a multifaceted trait involving morphological, physiological, and biochemical changes. The effects of drought have been studied for a long time from the whole plantplant population level to physiological, biochemical, and molecular levels. Resistance to drought stress is bestowed by the proteins, which play a key role in stress signaling, transcription regulation, cellular detoxification, protection of macromolecules, and an array of other cellular processes (Tester and Langridge, 2010). Through the study of the dynamically translated portion of the genome, the use of proteomic methods can provide evidence for molecular events that remain hidden during DNA or mRNA analysis. The proteomic technologies have now been applied to identify the mechanisms connected with drought stress and tolerance in several plants (Table 2.1). Salekdeh et al. (2002a) conducted a leaf proteomic analysis in two varieties of rice, cv. CT9993 and cv. IR62266, during drought stress and recovery and found that 42 proteins showed differential expression in two cultivars. The proteomic study revealed the increased abundance of four novel proteins: S-like RNase homologue, actin depolymerizing factor, and Rubisco activase with a decrease in the isoflavone reductase-like protein (Salekdeh et al., 2002b). Proteomic analysis of rice leaf sheath during drought stress suggested that the actin depolymerizing factor is one of the target proteins induced by drought stress (Ali and Komatsu, 2006). The proteomic analysis led to the identification of 109 differentially regulated proteins associated with transcriptional regulation, chromatin remodeling, signaling and gene regulation, cell defense and rescue, and protein degradation (Choudhary et al., 2009). A proteomic approach was applied for the identification of differential expression of proteins and phosphoproteins induced by water stress in O. sativa (Ke et al., 2009) using a proteomic approach. Of the 18 proteins detected, three highly abundant ones were related to the chloroplast,

Table 2.1 Summary of Proteomic Analysis of Plant Responses to Drought Stress Plant

Variety and Tissue

Proteomic Approach

IPs

Reference

Arachis hypogea

Leaf proteins

49

Kottapalli et al. (2009)

Beta vulgaris L.

Genotype 7112 and genotype 7219 RGS-003 (s), SLM-003 (r)

1 and 2-DE/MALDI-TOF-MS 2DE/Q-TOF MS/MS 2DE/LC-MS/MS

79

Hajheidari et al. (2005)

2DE/MALDI-TOF-MS

35 (s) 32 (r) 75 91

Mohammadi et al. (2012a)

2DE/MALDI-TOF-MS

134 750

Bhushan et al. (2011) Zhao et al. (2011)

2DE/LC-MS/MS

158

Bedon et al. (2012)

2DE/MALDI-TOF-MS

Mohammadi et al. (2012b)

Brassica napus L. Cicer arientinum L.

Cyanodon dactylon (L.) Pers X Cyanodon transvaalensis Burtt Davy Eucalyptus spp. Glycine max

Hordeum vulgare

Musa spp Oryza sativa L.

ICCV-2 nucleus Seedlings JG-62 extracellular matrix cv. Tifway C2999 leaves

Irrigated and natural leaves, stems Leaf, hypocotyl, root

2DE/LC-MS/MS 2DE/Pro-Q Diamond dye/LC-MS/MS

(r) (h) (l) (L) (R)

Subba et al. (2013a) Subba et al. (2013b)

Golden promise, Basrah roots and leaves

DIGE/MALDI-TOF-MS

Golden promise leaves Genotype 004186 (s) Genotype 004223 (r) shoots Arta, Keel leaves Leaves cv.CT9993, cv. IR2266 leaves Rain fed low land versus upland leaf sheath Nuclear proteome Extracellular matrix

2DE/LC-MS-MS 2DE/MALDI-TOF-MS

32 13 12 24 45 45

2D-DIGE/MALDI-TOF-MS 2DE-DIGE/MALDI-TOF-MS 2DE/MALDI-TOF-MS 2DE/MALDI-TOF-MS

99 18 42 12

Rollins et al. (2013) Vanhove et al. (2012) Salekdeh et al. (2002a) Ali and Komatsu 2006)

2DE/LC-ESI-MS/MS 2DE/MALDI-TOF-MS

109 100

Choudhary et al. (2009) Pandey et al. (2010)

Wendelboe-Nelson and Morris (2012) Ghabooli et al. (2013) Kausar et al. (2013)

(Continued)

Table 2.1 (Continued) Plant

Phaseolus vulgaris L. Pisum sativum Populus catahayna Rehder

Populus catahayana X P. kangdingensis C Wang et Tung Populus deltoides Populus X euramericana Populus deltoids X Populus nigra Solanum tuberosum Triticum aestivum L.

Variety and Tissue

Proteomic Approach

IPs

Reference

Peduncle (upper most internode)

2DE-PAGE analysis

31

Seedlings cv. IR64 cv. IR64 Tiber (r) Starozagorski cern (s) Embryonic axis Populations from wet and dry regions, leaves Male and female cuttings Leaves

2DE/MALDI-TOF-MS 2DE/nanoLC-MS/MS 2DE/LC-MS-MS 2DE-DIGE/LC-MS/MS

60 900 93 58 (T) 64 (SC) 139 40

Muthurajan et al. (2011) Shu et al. (2011) Mirzaei et al. (2012) Jaiswal et al. (2013) Zadraznik et al. (2013)

2DE/MALDI-TOF-MS 2DE/

64

Zhang et al. (2010a) Yang et al. (2010)

Leaves cv. Agathe F. and Clima leaves

2DE/nanospray LC-MS/MS 2DE/MALDI-TOF/MS 2DE/MALDI-TOF/MS

398 62

Plomion et al. (2006) Bonhomme et al. (2009) Bonhomme et al. (2009)

2DE/MALDI-TOF-TOF/MS 2DE/MALDI-TOF/TOF 2DE/MALDI-TOF/MS

12 57 140

Zhang et al. (2013) Hajheidari et al. (2007) Kamal et al. (2010)

2DE/MALDI-TOF/MS 2DE/nano-LC-MS/MS

135 159

Bazargani et al. (2011) Ford et al. (2011)

2DE/MALDI-TOF-MS

93 (R) 65 (L) 28 68 122

Peng et al. (2009)

Ninlang 182 Grain China 108, Yemon 78, Norin 61, Kantou 107, grain Grain Kukri (s) Excalibur (r) RAC875 (r) cv. Jinan 177 root and leaf Ningchun 4, Chinese spring, grain Kauz (r) Janz (s), grain

2DE/MALDI-TOF-MS 2DE/MALDI-TOF-MS

2DE/MALDI-TOF-MS 2DE/MALDI-TOF-TOF-MS 2DE/MALDI-TOF-MS

Wang et al. (2012) Xiao et al. (2009)

Ge et al. (2012) Jiang et al. (2012)

(Continued)

Table 2.1 (Continued) Plant

Variety and Tissue

Proteomic Approach

IPs

Reference

Triticum durum Quercus ilex

Seedlings Leaf Leaf

2DE/MALDI-TOF/MS 2DE/LC-MS-MS 2DE/Tandem mass spectra

36 4 14

Subsp. ballota (Desf.) Samp leaf

2DE/MALDI-TOF/TOF-MS/MS

Leaf cv. Chardonnay and cv. Carbernet Sauvign on, shoot tips Berry tissues (skin and pulp) Shoot tips Xylem sap Leaf

2D-DIGE/MALDI-TOF--MS 2de/MALDI-TOF-TOF

12.4% Spots 191

Caruso et al. (2009) Jorge et al. (2006) Echevarria-Zomeno et al. (2009) Valero-Galvan et al. (2013) Sergeant et al. (2011) Vincent et al. (2007)

90 472 31 58

Grimplet et al. (2009) Cramer et al. (2013) Alvarez et al. (2008) Hu et al. (2009)

30 18 36 82

Benesova et al. (2012) Zhang et al. (2010b) Yang et al. (2011) Horn et al. (2013) Shi et al. (2013) Kang et al. (2012)

Quercus robur L. Vitis vinifera L.

Zea mays L.

Carissa spinarum Triticum aestivum L. Arabidopsis thaliana Cyanodon dactylon Triticum aestivum L.

Leaf Leaf Grain Plastid Whole plant Seedlings

2DE-PAGE 2de/nano-LC-MS/MS 2DE/MALDI-TOF-MS 2DE/Peptide mass fingerprinting 2DE/iTRAQ analysis 2DE/MALDI-TOF-MS 2-DE/MALDI-TOF-MS 2DE-DIGE/MALDI-TOF-MS 2DE/MALDI-TOF-MS 2DE/MALDITOF-TOF

30


LEA and SOD, whereas the protein precursor of Rieske Fe-S was of lower abundance. Of the 10 phosphoproteins identified in response to drought, 7 had not been previously reported under conditions of water stress. This study suggested the involvement of presently unidentified proteins in the mechanisms that regulate responses to drought stress (Ke et al., 2009). Proteomic analysis revealed the differential expression of 100 extracellular matrix proteins involved in carbohydrate metabolism, cell defense and rescue, cell wall modification, cell signaling, and molecular chaperons (Pandey et al., 2010). In another study, Shu et al. (2011) examined the response of rice seedlings to drought stress and identified 60 proteins that respond to drought. Translation-related proteins were down-regulated, proteins associated with protein folding were up-regulated, and several proteins involved in carbohydrate metabolism showed differential expressions (Shu et al., 2011). A proteomic approach was adopted to identify how drought-exposed root tissues alter the proteome of adjacent wet roots by hormone signals and how wet roots reciprocally affected dry roots hydraulically (Mirzaei et al., 2012). Quantitative label-free shotgun proteomic analysis of four kinds of roots resulted in the detection of 1487 nonredundant proteins, with close to 900 proteins existing in each treatment (Mirzaei et al., 2012). An evaluation of the proteomics of dehydration response in the rice nucleus was undertaken by comparing a dehydration-sensitive cultivar, IR-64, with a dehydration-tolerant cultivar, cv. Rasi (Jaiswal et al., 2013). This study identified 93 dehydration-responsive proteins, suggesting that a significant number are capable of interacting with each other. Hajheidari et al. (2007) studied proteomic changes in wheat grain in three genotypes in response to drought stress. The study identified 57 proteins, most of them being known thioredoxin (Trx) targets, establishing a link between drought and oxidative stress. Various other researchers have conducted proteomic studies with wheat during drought stress (Caruso et al., 2009; Kamal et al., 2010; Bazargani et al., 2011; Yang et al., 2011). These studies revealed the abundance of a small subset of proteins that are drought responsive, comprising 77 (Yang et al., 2011) and 33 (Kamal et al., 2010) in grains, 82 in stem (Bazargani et al., 2011), and 21 in the first leaf (Caruso et al., 2009). Peng et al. (2009) applied a proteomic approach to study the effect of drought and salinity stress on seedlings of the somatic hybrid wheat cv. Shanrong No. 3 and its parent line cv. Jinan 177. The proteomic study revealed similarities and differences with regard to differential expression of proteins in response to salinity and drought. Osmotic and ionic adjustment provided enhanced tolerance to Shanrong 3 cultivars in response to drought/salinity (Peng et al., 2009). Proteins were isolated from the leaves of three cultivars (Kukri, Excalibur, RAC 875) that differed in their ability to maintain grain yield during drought. Isobaric tags were used to follow changes in the relative abundance of 159 proteins. The three cultivars showed consistent changes in the increase of proteins involved in the oxidative stress metabolism and ROS-scavenging system and a decrease in proteins involved in photosynthesis and the Calvin cycle (Ford et al., 2011). The effect of high temperature events and water deficits on protein profiles was studied in wheat using grain albumin and gliadin protein fractions. The study identified the proteins involved in primary metabolism, storage, and stress response such as late embryogenesis abundant proteins, peroxiredoxins, and α-amylase/trypsin inhibitors (Yang et al., 2011). A proteomic approach was also applied to study the effect of salicylic acid on growth and tolerance to subsequent drought stress in wheat seedlings (Kang et al., 2012); it identified 76 proteins associated with signal transduction, stress defense, photosynthesis, carbohydrate metabolism, protein metabolism, and energy production. A comparative proteomic analysis of grain development was studied in two spring


31

wheat varieties (Ningchun 4 and Chinese Spring) in response to drought stress. The study identified 96 proteins with 6 different expression patterns associated with stress/defense/detoxification, carbohydrate metabolism, photosynthesis, nitrogen metabolism, and storage proteins (Ge et al., 2012). Comparative proteomic research was also performed to study drought responsive proteins at the time of grain development in two wheat varieties, Kauz (resistant) versus Janz (sensitive). The study revealed the changed abundance of 122 proteins mainly involved in carbohydrate metabolism, detoxification, and defense and storage proteins. The up-regulation of sucrose synthase and the triticin precursor (storage function) was greater in Kauz than Janz, implying the higher drought resistance of Kauz (Jiang et al., 2012). Alvarez et al. (2008) examined the changes in the xylem sap proteome of maize under extended drought; increased levels of cationic peroxidases and phenylpropanoids and reduced lignin biosynthesis were found. The study provided insights into the range of xylem sap compounds and how the changes in their composition may direct changes in development and signaling during adaption to drought. A study was carried out to see the differential expression of candidate genes for lignin biosynthesis under drought stress in maize leaves, which found that 58 proteins were responsive to drought stress. This showed a sequence similarity with cinnamyl alcohol dehydrogenase, cytochrome protein 96A8, and S-adenosyl L-methionine synthase. The results of a study done by Benesova et al. (2010) indicated that leaf lignin content is a useful index for evaluation of drought tolerance in maize. Drought resulted in the increased abundance of protective and stress-related proteins, mainly dehydrins and chaperons, in two genotypes of Zea mays. Barley adapts well to abiotic stresses including drought; therefore, it continues to be cultivated worldwide in marginal environments and in the driest rain-fed farming areas (Baum et al., 2007). Barley varieties, Golden promise (from the UK) and Basrah (from Iraq), subjected to drought were compared by proteomic analysis (Wendelboe-Nelson and Morris, 2012). This study identified 24 leaf and 45 root proteins in the two varieties. The Basrah variety exhibited an increased accumulation of proteins regulating the oxidative system and protein folding. In contrast, photosynthesisrelated proteins were down-regulated. The proteomic study revealed that the higher drought tolerance in the Basrah variety may be due to a greater regulation of ROS-homeostasis (Wendelboe-Nelson and Morris, 2012). A comparative proteomic approach was also applied to better understand the Piriformospora indica-mediated drought tolerance in the Golden promise cultivar of barley grown under different drought levels. Leaf proteomic analysis identified 45 differentially accumulated proteins associated with photosynthesis, ROS, signal transduction, and plant defense responses. This study revealed a locus on the impact of the endophyte on barley plants and also identified novel proteins (e.g., TCPP and PCNA) to use as potential candidates for raising drought tolerance in plants in the future (Ghabooli et al., 2013). Another comparative shoot proteomic study was also undertaken to investigate the response of three-day-old barley seedlings of genotype 004186 (sensitive) and genotype 004223 (tolerant) subjected to drought stress. The proteomic study exhibited the differential expression of proteins related to chloroplast metabolism, photosynthesis, amino acid synthesis, and energy metabolism (Kausar et al., 2013). Leaf proteome changes were studied in two barley cultivars, the Syrian Arta and the Australian Keel, in response to a combination of stresses (i.e., heat and drought). The proteome study identified 99 protein spots associated with photosynthesis, detoxification, energy metabolism, and protein biosynthesis (Rollins et al., 2013). Comparative proteomic analysis was performed to investigate

32


the effect of polyamines-mediated increased salt and drought responses in Bermuda grass (Shi et al., 2013) and hybrid Bermuda grass (Cyanodon dactylon (L.) X Cyanodon transvaalensis Burtt Davy cv. Tifway) (Zhao et al., 2011). Several studies were conducted to see the proteome responses of different Fabaceae members subjected to drought. A comparison was also made using leaf proteome of the control and droughtexposed cultivars. Tiber (tolerant) and Starzagorski cern (sensitive) of common bean resulted in the identification of 49 differentially expressed proteins mostly involved in energy metabolism, photosynthesis, adenosine triphosphate (ATP) interconversion, protein synthesis and proteolysis, stress, and defense-related proteins (Zadraznik et al., 2013). Pandey et al. (2008) investigated the effect of dehydration on the nuclear proteome of chickpea (Cicer arietinum), an economically valuable legume crop cultivated largely in hot and dry climates. The authors found that the increased accumulation of proteins was associated with cell signaling, the ROS-scavenging system, and defense and rescue proteins. A later study added proteins involved in cell wall modification to the list of potential targets for improvement of crops (Bhushan et al., 2011). A comparative proteomic study was conducted to characterize the nuclear proteome of two cultivars of chickpea, ICCV-2 (sensitive) and JG-62 (resistant), in response to dehydration (Subba et al., 2013a). The differential proteome and in silico analysis revealed cultivar-specific differential expression of several proteins associated with cellular functions and the ROS system (Subba et al., 2013a). A differential phosphoproteome study identified 91 putative phosphoproteins in chickpea associated with cell defense and rescue, photosynthesis and photorespiration, molecular chaperones, and ion transport (Subba et al., 2013b); this indicated the involvement of phosphorylation in drought reponses. The authors also noted the differential regulation of plasma membrane proteins, DREPP (developmentally regulated plasma membrane protein) and CaDREPP1. Wang et al. (2012) examined changes in embryo axis proteome of pea seeds during germination. They identified 139 proteins associated with desiccation tolerance and found a total of 7 proteins: tubulin α-1, seed biotin-containing protein SBP65, P54 protein, vicilin, vicilin-like antimicrobial peptides2-3, convicilin, and the TCP-1/cpn60 chaperonin family protein. The study also found that desiccation tolerance is linked with pathogen defense, protein conformation conservation, and cell structure stabilization. Kottapalli et al. (2009) studied alterations in the leaf proteome of peanut (Arachis hypogea) genotypes from the US mini-core collections during reproductive-stage growth under water deficit stress. Forty-nine nonredundant proteins were identified, largely representing the functions found in other organisms. Toorchi et al. (2009) carried out proteomic studies to identify drought stress-related proteins in soybean roots. Of the 415 proteins detected in PEG-treated soybean roots, the abundance of 37 proteins changed after the PEG treatment. Another proteomic study of drought-treated primary soybean roots detected 35 proteins that exhibited reproducible and significant changes in abundance in at least one region of water-stressed roots compared to the well-watered controls. The accumulation of ferritin proteins in the elongation zone of water-stressed roots, known to play an important role in protection against ROS, was found (Yamaguchi et al., 2010). Alterations in protein levels in organs (leaf, hypocotyl, and root) of drought-stressed soybean were analyzed (Mohammadi et al., 2012a). The root was found to be the most responsive organ to drought stress with the expression of 32 proteins. The comprehensive analysis of poplar proteome has been described based on the 2-DE reference maps for eight tissues and organs of the plant and the functional characterization of some proteins (Plomion et al., 2006). Bonhomme et al. (2009) conducted leaf proteomic analysis of eight genotypes


33

of Populus 3 euramericana plants in response to drought. Sixty-two proteins related to chloroplast, the Calvin cycle (i.e., Rubisco activase, sedoheptulose-1,7-bisphosphatase, and triose phosphate isomerase), and electron transport chains (ATP synthase subunit α) were detected. Proteins associated with oxidative stress and protein metabolism were also identified in response to drought stress. In another study, Bonhomme et al. (2009) studied the effect of water deficit on the leaf 2-DE protein profiles of two Populus deltoides 3 Populus nigra cv. Agathe F and Clima genotypes. The Clima genotype exhibited the highest abundance of antioxidant enzymes, whereas the Agathe F genotype showed an increase in the abundance of enzymes involved in photosynthesis, photorespiration, and oxidative stress. In P. cathahayana, leaf proteomic analyses resulted in the identification of 40 drought-responsive proteins involved in the regulation of transcription and translation, photosynthesis, cytoskeleton, secondary metabolism, HSP/chaperones, redox homeostasis, and defense response. The proteomic study provided insights about poplar’s tolerance to drought stress due to control of the reactive oxygen species and to its osmoprotective capacity (Xiao et al., 2009). A comparative proteomic study was conducted to determine sex-dependent responses to drought in P. cathayana (Zhang et al., 2010a). The authors identified 64 differentially abundant spots containing proteins related to drought and 44 spots that had a differential abundance, depending on the interaction between gender and drought. This study also provided insights about the relationship between sex and drought stress by the expression of photosynthesis-related proteins, homeostasisrelated proteins, and stress response proteins (Zhang et al., 2010b). A comparative proteomic investigation was conducted to assess drought responses using cuttings of P. kangdingensis and P. cathayana from high and low altitudes. The results indicated that physiological and proteomic responses to drought stress work cooperatively to establish a new cellular homeostasis, thus permitting poplar to gain a sort of drought tolerance. Changes in the protein profile of Quercus ilex leaves in response to drought stress and recovery were evaluated (Echevarria-Zomeno et al., 2009). This study led to the identification of 14 proteins related to photosynthesis, carbohydrate and nitrogen metabolism, and stress-related proteins (Echevarria-Zomeno et al., 2009). Another study was carried out to see the variation in the holm oak leaf proteome at different plant developmental stages, between provenances during drought. The study indicated the mobilization of storage proteins and carbohydrates, as well as photosynthetic inhibition under drought conditions (Jorge et al., 2006). Valero-Galvan et al. (2013) studied the effect of drought stress on the leaf proteomic profiles of one-year-old seedlings of holm oak (Quercus ilex subsp. ballota [Desf] Samp) collected from seven sites in Andalusia. The identified proteins were mainly related to chloroplast metabolism and defense mechanisms. The research also revealed the down-regulation of proteins related to ATP synthesis and photosynthesis. A leaf proteomic study also has been undertaken on the response of Quercus robur L. to drought exposure (Sergeant et al., 2011). A proteomic study on the shoot tips of two cultivars of grape (i.e., Chardonnay and Cabernet Sauvignon) revealed changes in the abundance of 191 unique proteins involved in photosynthesis, protein synthesis, and protein destination (Vincent et al., 2007). In another study, the shoot tips of Cabernet Sauvignon grape vines were subjected to progressive water deficit. A shotgun proteomics approach revealed changes in the abundance of proteins involved in translation, energy, antioxidant defense, and steroid metabolism (Cramer et al., 2013). Other species on which proteomic analyses have been performed to get a more profound insight into drought stress responses include sugar beet (Hajheidari et al, 2005), Elymus elongatum (Gazanchian et al., 2007), sunflower (Castillejo et al., 2008), wild watermelon (Yoshimura et al., 2008), Carissa

34


spinarum (Zhang et al., 2010a), potato (Zhang et al., 2010b), Eucalyptus (Bedon et al., 2012), seabuckthorn (Xu et al., 2012), and Arabidopsis (Horn et al., 2013). The set of data provided by these studies has resulted in an increased understanding of responses to drought. Use of genetic resources with dissimilar tolerances to drought in proteome research would be valuable for plant improvement.

2.3.1.2 Flooding stress Rainfall is required at key stages of crop development to guarantee good yield. However, intermittent downpours or continuous rain in an area with poorly drained soils can lead to flooding and soil waterlogging. It is suspected that about 16% of the world’s agricultural lands are affected by flooding (Boyer, 1982). As a result, the quantity of water present in the soil surpasses its absorption ability so that water remains on the surface. Although difficult to estimate, a soil saturated more than 20% above field capacity is said to be waterlogged (Aggarwal et al., 2006). Since the gas diffusion rate in water is four times slower than in air, waterlogged soils result in reduced (hypoxia) or lack of (anoxia) access to oxygen. Oxygen deprivation caused by flooding may be the main limiting factor for normal plant development and leads to modifications in both transcription and translation of the genes involved in various physiological and metabolic pathways. The most important groups of genes that show a differential expression under hypoxic conditions include transcription factors and components of signaling cascades but also genes involved in nitrogen metabolism and cell wall loosening (Liu et al., 2005). Oxygen deprivation also leads to anaerobic metabolism and directs sugars to the glycolysis, followed by pyruvate fermentation instead of oxidative decarboxylation and the Krebs cycle. In addition to an increase in the cellular energy charge, the other harmful effects connected with hypoxia and anoxia include a drop in cytoplasmic pH, accumulation of toxic metabolites, and ROS generation. Flooding/waterlogging is considered one of the most distressing environmental conditions. Floodingsensitive plant species are unable to induce acclimation mechanisms on exposure to such stress. Many crops cannot tolerate flooding, resulting in a retardation of growth and reduced yields. Maize, tomato, and some leguminous species (e.g., soybean) are flood-sensitive corps. Worldwide flooding stress results in a 25% decrease in yield of agricultural crops (Valliyodan and Nguyen, 2008). In contrast, flooding-tolerant species display both constitutive and inducible mechanisms for morphological and physiological adaptation to aqueous habitats. Rice is the best-known example of a flooding-tolerant crop. Proteomic approaches were applied to gain a better understanding of the mechanisms involved in tomato, wheat, and soybean in response to flooding/waterlogging stress. Recently, Komatsu et al. (2012a) discussed the contributions of proteomic studies toward increasing agriculturalists’ understanding of the well-organized cellular response to flooding in soybean and other crops. This review also discussed the biological significance of the proteins recognized using proteomic approaches in regard to crop stress tolerance (Komatsu et al., 2012b). In two follow-up studies, Ahsan et al. (2007a,b) investigated the response of tomato to waterlogging, which resulted in the increased abundance of proteins associated with the synthesis of hormones and secondary metabolites; however, proteins involved in the control of programmed cell death and stress defense mechanisms were also noted. The proteome level changes were accompanied by changes in physiological parameters, such as an increase in relative ion leakage, lipid peroxidation, and in vivo hydrogen peroxide (H2O2) content, in leaves. Similar observations were made in a study on soybean; continuous waterlogging resulted in a gradual increase of lipid


35

peroxidation and in vivo H2O2 level in the roots (Alam et al., 2010). One of the results also showed that waterlogging resulted in increased degradation of Rubisco, although it cannot be determined whether this degradation is enzymatic and/or due to ROS. This observation has important implications and cannot be made with nucleotide-level studies. A critical purification process was adopted for extracting and purifying cell wall proteins (CWP) from wheat seedling roots. The differential expression of CWPs under flooding stress was determined using gel-based and LC-MS/MS-based proteomic techniques. Eighteen proteins were found in increased abundance in response to flood stress by gel-based proteomics technique and 15 proteins were shown to accumulate in response to flooding by LC-MS/MS-based techniques. Proteins associated to the glycolysis pathway and cell wall structure and modification were down-regulated in response to flooding stress. In contrast, defense- and disease-responsive proteins were up-regulated. Among the identified proteins, only methionine synthase, β-1,3-glucanases, and β-glucosidase were constantly spotted by both approaches. The down-regulation of these three proteins suggested that wheat seedlings respond to flooding stress by limiting cell growth to escape energy consumption by organizing methionine assimilation and cell wall hydrolysis. CWPs contributed critically to flooding responsiveness (Kong et al., 2010). In another study, Haque et al. (2011) analyzed proteins in aerenchymatous seminal roots of seedlings of wheat grown in hypoxic soils under waterlogged conditions. A total of 29 proteins were differentially expressed. Of these, 10 exhibited a reproducible up- or down-regulated fluctuation. The up-regulated proteins were involved in alteration of energy and redox status, defense responses, and cell wall turnover. The study suggested that the effect of soil hypoxia on the up-regulation of proteins was connected with alternative respiration and cell degeneration in wheat in order to adjust its metabolism. Alternatively, ROS may be involved in signaling events related to the slowdown in growth observed in flooded plants (Shi et al., 2008). Gel-based proteomic analyses of soybean seedlings revealed that expression of glycolytic proteins is significantly impacted by flooding; however, proteins classified into the defense/disease-resistant category accounted for a major proportion of those induced in soybean undergoing flooding stress (Hashiguchi et al., 2009a,b). Komatsu et al. (2009a) conducted a comprehensive analysis of the soybean genes and proteins expressed under flooding stress using transcriptome and proteome techniques. A total of 39 proteins involved in alcohol fermentation, ethylene biosynthesis, pathogen defense, and cell wall loosening were more abundant in response to flooding stress. At the translational level, ROS scavengers and chaperons were changed. Young seedlings showed the response of adaptation under flooding stress by ensuring survival against hypoixa as well as to the direct damage of the cell by water. Komatsu et al. (2010a) studied the effect of nitrogen replacement with aeration during four days of flooding. The ROS scavenger 1-Cys peroxiredoxin (Prx) is up-regulated in soybean undergoing flooding stress and ascorbate peroxidase (Apx) is down-regulated. A gel-free proteomic analysis of young soybean seedlings identified 81 proteins that are responsive to flooding stress, while only 32 such proteins were identified using a gel-based approach (Nanjo et al., 2010). Based on the number and function of proteins identified by this study, it appears that glycolysis and fermentation enzymes, and inducers of heat shock proteins, play key roles in the early response of soybean seedlings to flooding stress. The alcohol dehydrogenase (ADH) abundance in the root tissue of soybean was also investigated using proteomics (Komatsu et al., 2011). A number of reports revealed the up-regulation of the molecular chaperone 70 kDa in flooded soybean, signifying that the protein is involved in temporary interactions to refold abnormal

36


proteins produced in response to flooding-caused injury (Komatsu et al., 2009a, 2010a; Nanjo et al., 2011b). A proteomics approach was used to investigate the organ-specific response mechanism in roots, hypocotyl, and leaves of seedlings of soybean under flooding stress. The study suggested that concurrence in expression of the isoflavone reductase protein level, along with disparity in other disease/defense and metabolism-related proteins, may lead to reduced growth of root, hypocotyl, and leaf of soybean seedlings under flooding stress (Khatoon et al., 2012a). In another study, Khatoon et al. (2012b) evaluated the effects of flooding stress on early symbiotic interactions between soybean roots and soil bacteria. The proteins associated with disease/defense, protein synthesis, energy, and metabolism were up-regulated in response to flooding stress. Nanjo et al. (2012) analyzed the phosphorylation/dephosphorylation of proteins in soybean in response to flooding stress using 2-DE in combination with ProQ Diamond staining. Their analyses revealed that flooding altered the phosphorylation state of 16 protein spots, mostly dephosphorylation in response to flooding, involved in energy generation, protein synthesis, and cell wall structure maintenance. A proteomic approach was applied for the identification of the proteins involved in postflooding recovery in roots of soybean. Comparative analysis revealed differential expression of 70 proteins; many were concerned with protein destination/storage and metabolic processes. It was also observed that the down-regulation of ion transport-related proteins and up-regulation of proteins involved in cytoskeletal reorganization, cell expansion, and programmed cell death suggested the effect of flooding on cell wall metabolism and cytoskeletal organization under the post-flooding recovery process (Salavati et al., 2012). A gel-based proteomic technique was used to analyze the flooding-tolerance mechanism in mutant soybean (Komatsu et al., 2013). Up-regulation of fermentation-related proteins was identified in the mutant under flooding stress. Alcohol dehydrogenase activity in the mutant was increased compared to that of the wild type at an early stage of flooding stress. These results suggested that activation of the fermentation system is necessary for the acquisition of flooding tolerance in soybean. Organelle proteomic approaches, increasing the focus of the study, have provided a more in-depth analysis of the mechanisms of flooding stress tolerance in plants. Komatsu et al. (2009b) investigated the effects of flooding stress on soybean plasma membrane proteins by applying an aqueous two-phase partitioning method in combination with gel-based and gel-free proteomic techniques. Results of their study indicated: (1) the proteins situated in the cell wall are upregulated in the plasma membrane, signifying the influence of the plasma membrane for alteration of the cell wall; (2) the proteins associated with the antioxidative system may play a vital role in guarding cells from oxidative injury; (3) heat shock cognate 70 kDa protein plays a role in protecting other proteins from denaturation and degradation; and (4) signaling proteins may maintain ion homeostasis. The cell wall of higher plants is the first compartment to be impacted by stress signals that are then communicated to the cell interior to modify cellular responses. Komatsu et al. (2010b) isolated CaCl2-extracted CWPs from roots and hypocotyls of soybeans subjected to flooding stress. Out of 204 CWPs, the abundance of 16 proteins was affected by flooding stress. Of these 2 lipoxygenases, 4 germin-like protein precursors, 3 stems, 28/31 kDa glycoprotein precursors, and 1 superoxide dismutase (Cu-Zn) were down-regulated. Lignin staining indicated that lignification is inhibited in the roots of flooding-stressed soybean. These results suggested the suppression of lignification in the soybean roots under flooding by down-regulation of ROS and jasmonate biosynthesis.


37

Proteomic and metabolomics techniques were applied to evaluate the function of mitochondria in roots and hypocotyls of soybean under flooding stress (Komatsu et al., 2011). The abundance of proteins related to the TCA cycle and α-aminobutyrate shunt increased. The contrary was observed for inner-membrane carrier proteins and proteins related to the electron transport chain, suggesting that flooding directly impairs these processes. Komatsu et al. (2012b) also studied the effect of flooding stress on endoplasmic reticulum fraction extracted from root tips of soybean using gelbased and gel-free proteomic approaches. A total of 111 functional proteins were identified. The study suggested that flooding mainly influenced the function of protein synthesis and glycosylation in the endoplasmic reticulum (ER) in soybean root tips. Ubiquitin (Ub)/proteasome-mediated proteolysis has been known to regulate the response to several environmental stresses in plants including soybean flooding. Shi et al. (2008) reported that levels of the 20 S proteasome α and Rpt2 subunits of the 26 S proteasome change in response to flooding stress of soybean roots. Under flooding stress, 26 S proteasome has an indirect impact on proteolysis and changes the activity of the proteasome itself as a result of conformational changes or other effects. The amounts of ubiquitinated proteins in soybean roots decreased after flooding treatment and increased to levels similar to controls after reversing submergence. Accumulation of both CSN4 and CSN5 proteins may improve the degradation of ubiquitinated proteins free from hypoxia by flooding (Yanagawa and Komatsu, 2012). The identification and analysis of floodresponsive proteins using different proteomics methods, such as differential proteomics, organ proteomics, organellar proteomics, phosphoproteomics, and Ub/proteasome-mediated proteolysis, may enhance our insight into how the cellular processes, metabolism, and Ub-related systems are influenced by flooding stress in soybean seedlings.

2.3.2 Imbalances in mineral nutrition Plants require at least 17 essential nutrients in order to successfully accomplish their life cycle. The essential elements are conventionally divided into two categories: (1) macronutrients that are involved in the structure of molecules and are required in large quantities and (2) the trace elements or micronutrients (Mengel et al., 2001). The latter are chlorine (Cl), boron (B), iron (Fe), manganese (Mn), copper (Cu), zinc (Zn), nickel (Ni), and molybdenum (Mo); they are required in comparatively small quantities and play catalytic and regulatory roles as enzyme activators and sometimes also have structural roles (Marschner, 1995). The uptake of mineral elements from the soil solution by plant roots and their subsequent distribution within the plant has been the subject of studies for many decades. Deficiency in any one of these mineral elements strictly restricts crop growth and yield. On the other hand, higher soil concentrations of mineral nutrients can have adverse effects on plant growth and development (White and Brown, 2010).

2.3.2.1 Deficient concentrations of mineral nutrients Physiological and molecular mechanisms underlying crop adaptation to mineral nutrient deficiency have been studied extensively (Xu et al., 2012), and proteomic techniques have been a crucial and complementary tool to acquire the knowledge thus far available, as was recently reviewed by Liang et al. (2013). The present chapter also updates a list of proteomic analyses of plant responses to mineral nutrient deficiency in Table 2.2.

38


Table 2.2 Summary of Proteomic Analysis of Plant Responses to Mineral Nutrient Deficiency Mineral Nutrient Deficiency

Plant

Tissue

UPs

IPs

Reference

Arabidopsis thaliana

Secreted proteins Roots

46

32

30

24

Leaves Nodules Roots

32 44 94

25 44 80

Roots

34

nd

Roots Roots

10 87

10 39

Roots

254

106

Tran and Plaxton, (2008) Chevalier et al. (2011) Yao et al. (2011) Yao et al. (2011) Fukuda et al. (2007) Torabi et al. (2009) Kim et al. (2011) Feng et al. (2012) Li et al. (2007)

Arabidopsis thaliana Agrostis tolonifera Hordeum vulgare Nicotiana tabacum Oryza sativa

Seedlings

170

170

Leaves

43

39

Leaves/roots

49

35

Leaves

5

5

Leaves Leaves

50 36

50 27

Triticum aestivum

Leaves

76

6

Roots

56

nd

Triticum (X Triticosecale wittmack)

Leaves

29

11


Leaves

45

45

Roots Leaves

101 75

101 34

Roots

61

22

Phosphorus

Brassica napus Glycine max Oryza sativa

Triticum aestivum Zea mays Nitrogen

Wang et al. (2012) Xu et al. (2011) Moller et al. (2011) Yang et al. (2012a) Kim et al. (2011) Song et al. (2011) Bahrman et al. (2004) Bahrman et al. (2005) Castillejo et al. (2008)

Iron

Beta vulgaris

Laganowsky et al. (2009) Lan et al. (2012) Andaluz et al. (2006) Rellan-Alvarez et al. (2010) (Continued)


39

Table 2.2 (Continued) Mineral Nutrient Deficiency

Plant

Tissue

UPs

IPs

Reference

Cucumis sativus Malus pumila

Roots

57

44

Roots

36

12

Medicago truncatula

Roots

69

51

Pisum sativum

Roots

89

15

Solanum lycoperscum

Roots

155

29

Roots

38

38

Donnini et al. (2010) Wang et al. (2010) RodriguezCelma et al. (2010) Meisrimler et al. (2011) Brumbarova et al. (2008) Li et al. (2008)


Seedlings

24

24

Kang et al. (2004)

Brassica napus

Roots

59

45

Lupinus alba

Roots

23

9

Wang et al. (2010) Alves et al. (2006)

Potassium

Boron

Plant roots acquire P as phosphate because it is present at extremely low concentrations in the soil solution, but they must search for this element. Strategies that improve P uptake include the exudation of protons, metabolites, and enzymes into the rhizosphere and structural changes in root morphology and/or associations with microorganisms (Hinsinger et al., 2009). Proteins responsible for these adaptive mechanisms have been identified in various tissues of different plant species, such as roots in Zea mays, Arabidopsis thaliana, and Oryza sativa, nodules in Glycine max, and leaves in Brassica napus (Fukuda et al., 2007; Li et al., 2007, 2008; Tran and Plaxton, 2008; Torabi et al., 2009; Chen et al., 2011; Chevalier and Rossignol, 2011; Kim et al., 2011; Yao et al., 2011; Feng et al., 2012; Lan et al., 2012). Several proteins with putative functions (e.g., GTPbinding nuclear protein, mini-chromosome maintenance protein, and glycogen synthase kinase-3 homolog MsK-3) to control root cell cycle and division were also found to be up-regulated by P deficiency (Li et al., 2007, 2008; Feng et al., 2012; Lan et al., 2012). Increased exudation of RNase1 was perceived for Arabidopsis suspension cells exposed to P deficiency, signifying that deficiency-boosted secretion of RNase1 may be imperative to mobilize Pi from extracellular nucleic acids (Tran and Plaxton, 2008). Differential proteomic analyses to identify P deficiency-responsive proteins resulted in the identification of the proteins involved in the synthesis and transport of plant phytohormones including ethylene, cytokinin, jasmonic acid, and auxin (Li et al., 2007; Torabi et al., 2009; Kim et al., 2011; Feng et al., 2012; Lan et al., 2012). Among the P deficiency-responsive proteins, several were

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involved in C metabolism, especially in glycolysis; the accumulation of some ubiquitin/26 S proteasome pathway proteins in maize and Arabidopsis were likewise influenced by P deficiency (Li et al., 2007, 2008; Chevalier and Rossignol, 2011; Yao et al., 2011; Lan et al., 2012). The same as other abiotic stresses, P deficiency causes the elevation of ROS in plants. Thus, a group of P deficiency-responsive proteins was found to be involved in oxidative stress defense through proteomic analysis including superoxide dismutase (SOD), 2-Cys peroxiredoxin, ascorbate peroxidase (APX), 1,4-benzoquinone reductase, and GST (Torabi et al., 2009; Chevalier and Rossignol, 2011; Kim et al., 2011). Most proteome studies were performed to identify N deficiency-responsive proteins in leaves and roots. It was found that the proteins in leaves were implicated in photosynthesis, Rubisco activase, Rubisco LS, and SS among others and were clearly down-regulated (Bahrman et al., 2004; Xu et al., 2011). In several studies, N deficiency also resulted in more complex responses of C metabolism in leaves, as revealed by the alterations of many C metabolism-related proteins in plants under N-deficient conditions (Bahrman et al., 2004; Kim et al., 2009; Song et al., 2010; Moller et al., 2011). Accelerated leaf senescence was observed, resulting in the breakdown of proteins (e.g., RuBisCO) under N-deficient conditions allowing the reuse and remobilization of N to other active tissues (Feller et al., 2008; Kim et al., 2009; Xu et al., 2011). N deficiency also may cause the elevation of ROS in leaves. Several proteins (e.g., 2-Cys peroxiredoxin in wheat, SOD in both rice and triticale, and APX in rice, triticale, and creeping bent grass) were drastically upregulated by N deficiency (Bahrman et al., 2004; Kim et al., 2009; Xu et al., 2011); also reported was monodehydro ascorbate reductase in barley (Moller et al., 2011). Augmented accumulation of these proteins may benefit plants so that they can evade the adverse effects caused by enhanced buildup of ROS as a result of N deficiency. Higher plants have developed two distinct mechanisms in response to Fe deficiency. Dicots and nongraminaceous monocots, classified as Strategy I plants, excrete protons resulting in soil acidification and Fe reduction. This means the Fe21 accessible grasses belong to the Strategy II group and secrete the mugineic acid (MA) family of phytosiderophores—natural Fe(III) chelators—to dissolve insoluble ferric Fe in the rhizosphere and to acquire it as Fe(III)MA complexes (Marschner, 1995). The mechanistic characteristics of these strategies have been studied using different proteome techniques on plants, especially roots, exposed to Fe-deficient conditions (Brumbarova et al., 2008; Li et al., 2008; Laganowsky et al., 2009; Donnini et al., 2010; Rellan-Alvarez et al., 2010; Wang et al., 2010; Meisrimler et al., 2011). Results have led to identifying one Fe deficiency up-regulated protein, SAMS, involved in ethylene synthesis in several plant species such as Arabidopsis, apple tree (Malus pumila), cucumber (Cucumis sativus), Medicago truncatula, and tomato (Solanum lycopersicum) (Li et al., 2008; Donnini et al., 2010; Rellan-Alvarez et al., 2010; Wang et al., 2010). Further, accumulations of several other proteins mediating root growth were found to be of higher abundance in Fe-deficient plants, including actin-depolymerizing factors, phytocystatin, and root hair-related V-ATPase (Wang et al., 2010). Another study found the increased accumulation of ferric chelate reductase in the roots of pea (Pisum sativum) (Meisrimler et al., 2011). Using proteomics analysis, proteins related to oxidative stress, ROS scavenging, and defense responses were also identified in plant roots subjected to Fe deficiency (Brumbarova et al., 2008; Li et al., 2008; Donnini et al., 2010; Rellan-Alvarez et al., 2010; Wang et al., 2010; Meisrimler et al., 2011). Up-regulation of these proteins indicated a significant enhanced defense system under Fe-deficient conditions in plants.


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Effects of a short-term (3 h) and a long-term (7 d) potassium deficiency have been examined in seedlings of A. thaliana (Kang et al., 2004). Both treatments resulted in increased accumulation of the proteins involved in signal transduction (14-3-3 proteins, a small G protein, ATH1 homeobox protein) and transcriptional regulation (TATA-binding protein Dr1 involved in repression of RNA polymerase II, bZIP transcription factor POSF21) as well as a 26 S proteasome subunit that is involved in ubiquitin-mediated protein degradation. Alves et al. (2006) observed the effects of boron deficiency on apoplastic leaf proteome in white lupine (Lupinus albus). They found a de novo accumulation of one PR-1 protein and an augmented buildup of several other PR proteins, namely β-1,3-glucanases, class III chitinases, thaumatin-like proteins, and expansin-like proteins. A number of proteins were also observed to be differentially expressed in B. napus by B deficiency. These proteins can be classified into several groups including signal transduction, antioxidative defenses, carbohydrate metabolism, and protein homeostasis (Wang et al., 2010). These results suggested that responses of plants to B deficiency are complex.

2.3.3 Heavy metal stress Anthropogenic activities that cause metal pollution in soils include metal mining and smelting, irregular agricultural and horticultural practices (i.e., excess application of fertilizers and pesticides), sewage sludge, fossil fuel combustion, metallurgical industries, and waste disposal. It has been estimated that metal contamination currently affects about 235 million ha of agricultural land. Metal-contaminated soils not only constrain crop yields, but also metals can be taken up into the edible parts of plants without showing any symptoms of phytotoxicity. This transfer of heavy metals into the food chain leads to a risk to human health and a threat to the entire ecosystem (Hart et al., 2006). Although some metals are essential micronutrients that are involved in the functional activities of a large number of proteins, an excess of them can cause problems. For other metals, little or no role in plant metabolism is known; these nonessential metals (e.g., Al, Cd, Cr, Pb, Hg, As) can have negative effects on plants, even from very low concentrations. The effect of metal on plants is complex and determined by the biological availability of a metal rather than by the absolute concentration in the soil (Marschner, 1995). Metal toxicity is exerted when ionic forms of the metals form complexes or ligands with biomolecules or when the presence of redox-active metal results in the production of ROS through Haber-Weiss and Fenton reactions. The interaction of metals with biomolecules, especially proteinscan, causes inactivation of important enzyme systems and/or affect protein structure. Further, many enzymes require some metal for their activity, and displacement of one metal by another may lead to inhibition or loss of enzyme activity. There are different ways in which plants respond to heavy metal toxicity such as immobilization, exclusion, chelation, and compartmentalization of ions (Ahsan et al., 2008). The formation of peptide metal-binding ligand phytochelatins (PCs) and metallothioneins (MTs), as well as the more general stress-response mechanisms, are among the ways plants combat stress (Ahsan et al., 2009; Hradilova et al., 2010). Several reviews of the application of proteomics in analyzing cellular mechanisms for heavy metal tolerance already have been published (Ahsan et al., 2009; Luque-Garcia et al., 2011; Villiers et al., 2011; Hossain and Komatsu, 2013). Proteomic analysis of plant responses to heavy metals (e.g., Al, Cd, Cu, Cr, Mn) and metalloids (e.g., As and B) is listed in Table 2.2.

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Aluminum (Al) is the third most abundant element in soil; it can inhibit root growth in many important crop species within a very short time (Kochian et al., 2004). The proteome of soybean subjected to toxic Al concentrations was analyzed by Zhen et al. (2007). Two signaling molecules, GTP-binding protein and phytochrome B protein, were differentially expressed in response to Al toxicity. In fact, the GTP-binding protein, as a molecular switch, enables transduction of signals across membranes, which controls cell proliferation, cytoskeletal assembly and organization, and intracellular membrane trafficking (Kang et al., 2004). Phytochrome B is a G-protein-coupled receptor that responds to incidental electromagnetic radiation. Low-molecular-weight HSP and three forms of DnaJ-like proteins were identified in Al-stressed soybean roots. Up-regulation of the ABC transporter and ATP-binding protein were also detected in soybean in response to Al toxicity (Zhen et al., 2007). Yang et al. (2007) carried out a comparative proteome analysis of Al-resistant and Al-sensitive rice cultivars in order to investigate Al tolerance and adaptation mechanisms in plants. This study revealed that cysteine synthase, a key enzyme in the glutathione (GSH) biosynthesis pathway, plays an important role in the mechanism of adaption of rice to Al toxicity. The proteome studies also showed the existence of antioxidation and detoxification mechanisms that led to up-regulation of SOD GST (SAMS2) in response to Al toxicity. Activation of the sulfur metabolism was also detected in rice (Yang et al., 2007). Duressa et al. (2011) identified two proteins—serine/theorine protein kinase and protein phosphatase 2A—both with a signaling function. No change in the expression level of G-protein and GTP-binding protein in Al-exposed rice roots was noted, implying that the activity of the G protein-coupled receptor is regulated by its phosphorylation state, which in turn is attenuated by protein kinase and phosphatase (Duressa et al., 2011). Cadmium (Cd) has deleterious effects on plants even at the lowest concentrations available in the substrate. Cd-induced elevated accumulation of protective proteins, enzymes involved in ROS scavenging, and biosynthesis of GSH have been observed in A. thaliana (Roth et al., 2006; Sarry et al., 2006; Semane et al., 2010). At a high Cd concentration, the cellular pool of GSH decreases dramatically with the increase in dipeptide γGlu-Cys, suggesting a high cellular demand of GSH for sustaining PC, (γGlu-Cys)n-Gly, synthesis. A proteomic study also highlighted the enhanced expression of NADP(H)-oxido-reductase, a vital component of plants that is a second line of defense and protects cells from heavy metal-induced oxidative damage (Sarry et al., 2006). Interestingly, Semane et al. (2010) reported an increase of photosynthetic protein abundance in leaves of Arabidopsis treated with mild Cd stress. Alvarez et al. (2009) employed two quantitative proteomic approaches, 2DE-DIGE and iTRAQ, to reveal the relationship between Cd21 sequestration and a thiol metabolism in roots of Brassica juncea. Both techniques identified an increased abundance of the proteins involved in sulfur metabolism. The enzymes sulfite reductase and O-acetylserine sulfhydrylase involved in reduction of sulfate to cysteine were found to be overexpressed in Cd-treated roots. The authors suggested that under Cd stress, sulfate availability for synthesis of PCs and GSH may limit Cd tolerance. The proteome of suspension-cultured cells of soybean subjected to various concentrations and time courses of Cd exposure has been analyzed (Sobkowiak and Deckert, 2006). Stress-induced protein SAM22, which is classified as a PR10 protein, was identified in an SDS-PAGE band that was enhanced by Cd treatment. Antioxidant enzymes, such as SOD [Cu- Zn], were also more abundant, providing a clue regarding the defense reaction of soybean to metal toxicity. Through comparative proteome analysis of high and low Cd-accumulating soybean cultivars, Hossain et al. (2012a)


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revealed the activation of SOD and CAT for cellular protection from ROS-mediated damage. This study also described the enhanced accumulation of glutamine synthetase (GS) that led to more GSH formation under Cd stress. It has also been reported that Cd-exposed soybean has an increased abundance of photosystem I and II proteins and of the proteins involved in the Calvin cycle; this indicates that increased photosynthesis may be an adaptive mechanism to withstand Cd injury. Alternatively, the increased abundance of these proteins may be a mechanism to replace inactivated proteins. Another study by Hossain et al. (2012b) noted an increased abundance of Hsp70 and Prx to maintain normal protein functions and activation of an antioxidant defense system, respectively, to combat Cd stress. Using iTRAQ to study the Cd-exposed barley leaf mesophyll tonoplast proteome, Schneider et al. (2009) revealed the up-regulation of B50 vacuolar transporters, including vacuolar ATPase subunits, MRP-like ABC transporter and two novel CAX transporters (CAX1a and CAX5), and one Al-activated malate transporter protein. In a Cd-treated flax cell culture, enhanced accumulation of proteins was observed; these included heavy metal-binding proteins (lipocalin-1, ferritin-2), fiber annexin, GS, isoflavone reductase-like protein, HSP70, formate dehydrogenase, chitinase, enzymes involved in SAM biosynthesis (SAMS, methionine synthetase), and enzymes involved in glycolysis (ALDO) (Hradilova et al., 2010). Low Cd treatment activated glycolysis and the TCA cycle in Lycopersicum esculentum (Rodriguez-Celma et al., 2010). Aina et al. (2007) reported significant inductions of GSH and PCPC3 in Cd-stressed rice roots, further confirming the role of thiol peptides in the heavy metal tolerance mechanism. This study also revealed the accumulation of cation/proton exchanger 1a and ABC transporters to ensure Cd21 sequestration to the vacuole (Aina et al., 2007). According to Lee et al. (2010), approximately half of the up-regulated proteins in rice roots are involved in oxidative stress response and GSH metabolism, illustrating the importance of the oxidative component in heavy metal stress. In poplar, a significant increase in various PR proteins—namely, β-1,3-glucanases, class I chitinases, and putative thaumatin-like proteins—in response to cadmium treatment was observed (Kieffer et al., 2008). Likewise, a Cd-induced decrease in some ROS scavenging enzymes (e.g., peroxidase, putative Trx peroxidase, Cu/Zn-SOD) was observed (Kieffer et al., 2008, 2009). Down-regulation of photosynthetic machinery is a known phenomenon of heavy metal stress; for instance, a low abundance of the proteins involved in the photosynthetic electron transport chain and Calvin cycle has been reported in Cd-exposed Populus (Kieffer et al., 2008, 2009; Durand et al., 2010). This data on poplar contradicts the observations of other plants. Why Cd exposure in poplar results in an apparent diminution of ROS-protective systems is unclear and further studies are required to explain this. Nonetheless, Bona et al. (2007) also observed a decreased abundance of Trx-POD in Cu-treated Cannabis sativa roots. It also has been noted that copper (Cu) stress induced aldo/keto reductase, which acts as a chaperone and reduces copper ions to Cu (I), and the up-regulation of PC-mediated vacuolar transport. In germinating seeds of rice, Ahsan et al. (2007c,d) observed that excess Cu induced oxidative stress, thus hampering metabolic processes. Up-regulation of antioxidant and stress-related regulatory proteins (e.g., glyoxalase I and peroxiredoxin) were detected to maintain cellular homeostasis. Li et al. (2009) evaluated the effects of elevated copper concentrations on Cu-accumulating Elsholtzia splendens plants. Several proteins with potential ion-binding functions (e.g., germin-like proteins GLPs with histidine motifs) were augmented in response to Cu. Components of the tonoplast protein pumps—that is, cation/H1 exchanger, thr proton-dependent oligopeptide transport

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(POT) family protein—which are involved in vacuolar metal sequestration were also increased. A large rearrangement of cytoskeletal proteins, such as protein F15H18.8 (similar to actin-related protein 4), tubulin α-6 chain, and actin-8, was found (Li et al., 2009). Cu-exposure was also studied in germinating rice embryos (Zhang et al., 2009a), indicating not only the importance of metallothioneins (MTs) as Cu-chelators but also as ROS scavengers (Wang et al., 2004). Toxicity of manganese (Mn) was studied in cowpea; early proteome-level observations indicated the increased abundance of a number of proteins in the “apoplastic washing fluid” including several isoforms of apoplastic PODs and PR proteins, especially glucanases, chitinases, and thaumatin-like proteins. A lower abundance of chloroplastic proteins involved in CO2 fixation and photosynthesis indicated that energy was channeled to withstand the Mn-stress (Fecht-Christoffers et al., 2003). At the symplast level, excess Mn resulted in a down-regulation of several enzymes involved in carbon assimilation (Rubisco-binding protein, Rubisco activase, PRK), and an increased abundance of OEC23 protein (a Mn-cluster containing protein), β6 subunit of proteasome, and several PR proteins (Fuhrs et al., 2008). These authors further observed greater activity of leaf apoplastic peroxidases in barley, a Mn-sensitive species, than in rice, a Mn-tolerant species; this demonstrated that, in rice, the greater the Mn tolerance of old leaves than young leaves is related to a higher capacity for binding Mn in the cell wall. Arsenic (As) is one of the most toxic metalloids for both plants and animals. A large number of physiological and biochemical analyses have been done in order to understand the As response in plants, and the proteome responses of crop plants; maize (Requejo and Tena, 2005), rice (Ahsan et al., 2008, 2010a), and Agrostis tenuis (Duquesnoy et al., 2009) have been investigated. These studies suggested that proteins related to energy metabolism, antioxidant defense, and signal transduction are of higher abundance under As stress. Requejo and Tena (2005) found an increased abundance of a group of seven enzymes involved in maintaining the cellular redox-homeostasis (i.e., three superoxide dismutases, two glutathione peroxidases, one peroxiredoxin, and one p-benzoquinone reductase) in addition to four other proteins (i.e., ATP synthase, succinyl-CoA synthetase, cytochrome P450, and guanine nucleotide-binding). These findings provided significant evidence that the induction of oxidative stress is the main process underlying heavy metal toxicity in plants. Research findings of Ahsan et al. (2008) revealed increased activity of GST-omega in rice roots following exposure to As(V), indicating the probable role of it in inorganic arsenic biotransformation and metabolism. Further, they suggested that GSH depletion may be associated with a high rate of PCs synthesis, detoxification through compartmentalization, or down-regulation of enzymes of GSH biosynthetic pathways such as GR and CS (Ahsan et al., 2008). In the leaf proteome of Agrostis tenuis, increased concentrations of As, especially As(III), led to degradation of several proteins (Rubisco LSU and SSU, components of OEC complex, components of ATP synthase) involved in photosynthetic reactions; this corresponded to the leaf chlorosis observed after As treatments (Duquesnoy et al., 2009). The proteomic work done by Ahsan et al. (2010b) on rice leaves subjected to As revealed suppression of energy and primary metabolic pathways and an increase in abundance of GSH content coupled with enhanced expressions of GR, SAMS, GSTs, and CS. The proteomic response of boron-tolerant (B) and B-intolerant barley cultivars under B stress was investigated by using iTRAQ (Patterson et al., 2007). This study revealed the higher abundance of three enzymes—iron deficiency sensitive 2 (IDS2), IDS3, and methylthio-ribose kinase in B-tolerant plants—involved in siderophore production; this suggests that under B stress there may


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be a potential link between iron, B, and the siderophore hydroxymugineis acid. Plants need to upregulate metabolic pathways (e.g., glycolysis, TCA cycle, and oxidation-reduction) in order to maintain growth and develop in a stressed environment. However, down-regulation of G3PDH and the suppression of cell division and protein metabolic processes were noted in roots of Lupinus albus under B deficiency (Alves et al., 2011). Although these recent proteomic studies provide many valuable clues for understanding some aspects of the heavy metal stress biology of plants, many questions remain. Little is known about the molecular actors of translocation, biotransformation and sequestration; the use of approaches destined for the analysis of any of these aspects may answer some of the open questions. Approaches, such as subcellular proteomics, characterization of PTM-modified proteins, and redox proteomics, remain to be studied. Likewise, other approaches, such as iTRAQ and interactomics (e.g., two yeast hybridization), may be helpful to further clarify the molecular mechanisms of plant responses to mineral nutrient deficiency and toxicity.

2.3.4 Salt stress Saline soil solutions contain as principal cations (Na1, Ca21, Mg21, and K1) and anions (Cl2, SO422, HCO32, CO3, 22, and NO32) but also other constituents (B, Sr21, SiO2, Mo, Ba21, and Al31) (Hu and Schmidhalter, 2002). The buildup of water-soluble salts in the soil solum (the upper part of a soil profile) or regolith (the layer or mantle of fragmental and unconsolidated rock material) contribute to salinization. Soils with a high salt content constitute nearly 10% of the land surface distributed over all climatic regions (Ruan et al., 2010). Salinization of soils devastatingly influences agricultural, environmental, and economic development (Rengasamy, 2006). It disturbs 50% of the irrigated lands on the globe, which accounts for only 15% of the total cultivated land while producing one-third of the world’s food (Munns and Tester, 2008). Salinity harmfully distresses plant growth and development in two principal ways: (1) osmotic or water-deficit effect and (2) ionic stress/toxicity (Wang et al., 2003). An osmotic or water-deficit effect involves a decrease of the osmotic potential of soil water that adjoins plant root cells due to dissolved salt ions. Osmotic stress constrains plants’ capacity to take up water leading to what is termed ‘‘physiological drought or cellular dehydration’’ (Munns, 2005). Salt (especially Na1 and Cl2, an intercellular buildup of which can injure cells and affect growth) enters plant cells with the transpiration stream and accumulates in cellular and extracellular compartments. Many plants under salt stress also suffer from secondary stresses, such as oxidative and mechanical, or poor health as a result of nutritional imbalances. The detrimental effects of salinity include slow/reduced growth, retarded development, reduced crop yields, low economic returns, soil erosion, ecological imbalance, and harm for human health due to the toxic effects of elements (e.g., B, F, and Se) entering into the food chain (Hu and Schmidhalter, 2002; Parida and Das, 2005). Production of salt stresstolerant crop plants is essentially required because of the growing threat of global warming on agricultural productivity, in addition to the predicted population explosion in the near future. Plants have already evolved developmental, morphological, physiological, biochemical, and molecular tactics to sense and cope with the detrimental effects of salt stress (Munns, 2005). Based on salt tolerance, plants are categorized as halophytes and nonhalophytes (glycophytes). Halophytes are salt-tolerant, which means they can accomplish their life cycle in environments where the salt concentration is around 200 mM NaCl or more. Nonhalophytes or glycophytes, on the contrary,

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show various degrees of damage and limited growth in the presence of sodium salts, effects that are usually at salt concentrations of 4 dS m21 40 mM NaCl or more (Chinnusamy et al., 2005). Several studies already have reported important findings of salinity-responsive genes, proteins, and metabolites involved in different cellular aspects important for salt stress response and tolerance. Various researchers have reported a species-specific proteome-response to salt stress (Hakeem et al., 2012b; Komatsu and Hossain, 2013; Kosova et al., 2013; Zhao et al., 2013). Currently, proteomics is regarded as an important research tool not only for the reconstruction of plants’ responses to salt stress but also to clarify its responsive pathways. Proteomics has developed as a central tool in the field of plant science, also permitting agriculturalists to better understand the salt tolerance mechanisms. Proteome researchers mainly utilize the 2-DE technique to separate the protein pool and both 2-DE/MALDI-TOF MS and gel-free LC-MS/ MS systems for identification of differentially expressed proteins while studying salt stress responses in plants. Comprehensive reviews have been published on the proteome level analysis of salinity-exposed plants (Sha Valli Khan et al., 2007; Afroz et al., 2011; Sobhanian et al., 2011; Zhang et al., 2012; Barkla et al., 2013; Kosova et al., 2013; Zhao et al., 2013). Moreover, further technical advances in protein analysis methods have made it possible to progress toward subcellular proteomics—the study of protein modifications and proteinprotein interactions. Significant results have recently been obtained through focused analyses of organelles or subcellular compartments of plant cells and the cell wall (Hossain et al., 2012c). Plant responses to salinity at the proteomic level have been investigated in various species covering both glyocophytes and halophytes. In glycophytes, the effects of salt stress have been studied in 17 dicotyledonous plants, with Arabidopsis thaliana (L.) Heynh being used the most frequently. Eight monocotyledonous plants have been studied with agriculturally important crops. Compared to glycophytes, the protein expression patterns in halophytes imply specific salt-responsive metabolisms. Proteomics results of salt stress responses have been published for 8 dicotyledonous and 3 monocotyledonous halophytes. Salt-responsive proteins were found in vegetative organs (e.g., seeds, seedlings, radicles, hypocotyls, roots, shoots, leaves), reproductive organs (e.g., panicles, anthers, grains), and other tissues (e.g., callus and cell suspension cultures). Focused proteome studies were also done on subcellular organelles and membrane systems: plasma membrane, microsome, apoplast, mitochondria, and chloroplast. Moreover, a few studies have been published on the comparison of salt-tolerant versus salt-sensitive varieties of soybean (Xu et al., 2011; Hakeem et al., 2012b; Ma et al., 2012), tomato (Chen et al., 2009), rice (Salekdeh et al., 2002a; Abbasi and Komatsu, 2004; Sarhadi et al., 2012), barley (Witzel et al., 2010; Rasoulnia et al., 2011), and wheat (Gu et al., 2013). In addition, studies were done with the mutant line versus the wild type of Arabidopsis (Shi et al., 2011) and rice (Nam et al., 2012). Comparative proteomic studies were also conducted with related plant species to contrast salt tolerance; for instance, between common wheat (Triticum aestivum) cv. Jinan 177 and Triticum aestivum/Thinopyrum ponticum introgression hybrid Shanrong 3 (Peng et al., 2009), salt-sensitive rice Oryza sativa versus salt-tolerant wild rice Porteresia coarctata (Yu et al., 2011), and Solanum chilense versus tomato (Zhou et al., 2011). Functional groups of proteins recognized as salt-stress responsive include those concerned with key processes such as stress signal transduction, transcription and protein metabolism, osmotic homeostasis, ion homeostasis, ROS homeostasis, photosynthesis, carbohydrate and energy metabolism, and cytoskeleton and cell wall dynamics. The insights gained in recent years provide crucial proteome-level


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information for understanding the molecular basis of the acquisition of stress tolerance; in addition, the studies are a source of information for testing new hypotheses on salt sensing and signal transduction and other related metabolic pathways (Kosovo et al., 2011; Zhao et al., 2013). Besides changes in the relative abundance of proteins, changes in the post-translational modification (PTM) pattern, as well as protein activity, have been detected under salinity. Comparative proteomics of sensitive versus salttolerant or glycophyte versus halophyte plants allowed the identification of differentially abundant proteins in genetically related plants, revealing differential stress tolerance. Proteomics has clearly added vital information for a much better understanding of the complex signaling and metabolic networks in plants under salt stress. Despite the significant progress, most of the current proteomic studies have focused on the expression of the abundant salt-responsive proteins. Large gaps still remain in agriculturalists’ knowledge with regard to profiling of low abundant proteins such as salt-responsive transcription factors, sensor/receptors in signaling transduction, membrane/vesicle channels, and transporters and metabolites in the energy supply. The extensive application of cutting-edge proteomic approaches and technologies promises to enhance the detection of low abundant proteins. Proteome characterization, including the description of PTM, proteinprotein interaction/dynamics, protein turnover/subcellular translocation, and the resulting molecular networks, may provide additional information but is far from being realized. Initiatives also need be started to identify and characterize organelle proteins, in particular, which may also open a new avenue for proteome-based salt-stress research.

2.3.5 Temperature stress The range of temperatures faced by organisms on the Earth’s surface is usually believed to be favorable for life. On the downside, biological processes are commonly restricted by the freezing point of water. The rate of most biochemical, enzymatic reactions rises two-fold for every 10 C increase between 2030 C. Temperatures outside this range reduce the reaction rate because enzymes become either inactivated gradually or denatured. Upsurges in temperature lead to the disruption of a protein’s tertiary/quaternary structure, which in turn decreases enzymatic activity. In other words, preserving enzymes in their active configurations is vital for cell survival. Therefore, individual organisms and species perform their growth and survival between two temperature extremes (Suzuki and Mittler, 2006). Plants exhibit a wide range of sensitivities to temperature extremes. There is an ideal temperature at which each plant grows and develops the most competently, and there are upper and lower limits. When the temperature varies outside these limits, there is no growth at all. Often a change of a few degrees substantially affects the plants’ growth and developmental processes, particularly reproduction. During the life cycle of flowering plants, reproductive development is considered a significant and delicate process and abiotic stresses, particularly heat and cold, have a detrimental effect on the early stage of male gametophyte in important crops such as rice, wheat, maize, barley, sorghum, and chickpea (Boyer and Westgate, 2004). Male sterility and abnormalities in the spikelets’ production were induced by heat stress in rice and wheat (Takeoka et al., 1991). The buildup of nonreducing sugars and the breakdown of starch in the pollen grains resulted in male sterility by cold in rice. It was observed that anthers become smaller and tapetal cells hypertrophic, resulting in the failure to supply nutrients to the developing pollen in the course of cold damage. In both wheat and rice, heat and cold stresses caused tapetum

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degradation, microspore callose wall and exine formation, and changes in carbohydrate metabolism, eventually resulting in male sterility (Mamun et al., 2006). In contrast, temperature stress has no negative effect on female gametophyte development (Saini and Aspinall, 1982). Fluctuations in global temperatures may prove to be a direct factor limiting crop yield in many parts of the world. Boyer and Westgate (2004) reported that cold stress caused an average annual yield decrease of 5 to 10% in rice in Australia, which sums to losses of up to $A44 million. Further yield losses of 2040% are projected due to arbitrary cold snaps happening on average every 3 to 4 years. Based on agricultural statistics, it has been found that rice grain yields were reduced by 10% for each 1 C rise above the optimum temperature during the growing season (Peng et al., 2004). Some estimates showed that elevated temperatures in the past two decades have resulted in a reduction in yield equal to $5 billion for the main food crops (e.g., rice, wheat, maize, barely, soybeans, and sorghum) (Lobell and Field, 2007). Plants have evolved a number of adaptive mechanisms that enable them to alleviate the negative effects of cold or heat stress; through reprogramming of their transcriptome, proteome, and metabolomes to reset physiological and molecular processes they can maintain steady-state homeostasis and reproductive developmental events under temperature stress. Understanding these mechanisms may have a profound impact on breeding or engineering of crops with thermotolerance. Of the various biological tools or systems available, a proteomic approach is very useful for deciphering molecular mechanisms (Neilson et al., 2010).

2.3.5.1 Heat stress Heat is one of the leading abiotic stresses that have a significant impact on growth and development of plants. Generally, high temperature stress causes irreversible denaturation of enzymes and problems with membrane fluidity. The synthesis of most proteins is suppressed and synthesis of HSPs is induced. Several reviews already have documented information about tissues and varieties used, the duration and degree of temperature applied, and the proteomic method adopted for the analysis of heat stress (Neilson et al., 2010; Kosova et al., 2011; Hakeem et al., 2012b). Proteomic responses to heat stress have been studied in a number of plant species (Table 2.3), including tomato (Iwahashi and Hosoda, 2000), wheat (Majoul et al., 2004), barley (Sule et al., 2004), rice (Lee et al., 2007), Populus euphratica (Ferreira et al., 2006), Brassica (Kosakivska et al., 2008), Picea abies (Valcu et al., 2008), Arabidopsis (Koussevitzky et al., 2008; Viridi et al., 2009), Prunus (Lara et al., 2009), soybean (Ahsan et al., 2010c), Carrissa spinarum (Zhang et al., 2010b), Agrostis (Xu et al., 2010), Suaeda (Li et al., 2011), potato (Savic et al., 2012), and Portulaca (Yang et al., 2012a). A proteomic approach was applied to study the effect of high temperature on rice quality during caryopsis development using two rice cultivars: indica type, heat-tolerant Taichung Native 1 (TN 1), and japonica type heat-sensitive Tainung 67 (TNG 67) (Lin et al., 2005). The results of the study revealed that the high-temperature treatment enhanced the abundance of low-molecularweight sHSPs but had a limited effect on the expression of high-molecular-weight HSPs. Further, the expression level of glyceraldehyde-3-phosphate dehydrogenase, an enzyme involved in the glycolytic pathway, increased in TNG 67; while the accumulation of prolamine, a storage protein, increased, especially in TN 1 (Lin et al., 2005). Proteomic analysis has also been performed on rice (japonica rice, cv. Dongjin) leaves (Lee et al., 2007). During at least one time point, 73 protein spots were differentially expressed. Of

Table 2.3 Summary of Proteomic Analysis of Plant Responses to Temperature Stress Plant Material Low temperature Arabidopsis thaliana

Oryza sativa

Variety and Tissue

Treatment

Approach

UPs

IDs

Reference

Col-0 Nuclear proteome Col-0 Leaf plasma membrane Col-0 leaf

4 C/6 h 2 C/1, 2, 7 d

2-DE MALDI-TOF 2-DE MALDI-TOF

500 42

184 38

2-DE MALDI-TOF

22

14 18 41

Imin et al. (2004) Cui et al. (2005)

96 39

85 34

Dongin seedling root

10 C/1 d, 2 d

37

27

Yan et al. (2006) Hashimoto and Komatsu 2007) Lee et al. (2009)

Leaves

5,10 C/12 h, 1 d, 1.5 d, 3 d 5/4 C/0,6 h, 2, 5, 24 d 5 C/several d 4/2 C/0, 2, 8, 26 h, 3, 5, 7, 14, 21 d 4 C/1 d 4 C/1.5 d

2-DE MALDI-TOF 2-DE MALDI-TOF-ESIMS/MS 2-DE MALDI-TOF/TOF 2-DE MALDI-TOF-ESIMS/MS 2-DE MALDI-TOF-ESIMS/MS 2-DE MALDI-TOF-ESIMS/MS 2-DE MALDI-TOF/TOFLC-MS/MS 2-DE MALDI-TOF/TOF 2-DE-ESI-MS/MS

70 60

Nipponbore seedling leaf Nipponbore seedling

6 or 10 C /7 d and recovery 12 C /4 d 5, 10, and 15 C/1 d 6 C/6 h, 1 d 5 C/2 d

Bae et al. (2003) Kawamura and Uemura (2003) Amme et al. (2006)

30

14

Lee et al. (2007)

66

50

Gao et al. (2009)

21 41

21 41

Degand et al. (2009) Kosmala et al. (2009)

2-DE MALDI-TOF 2-DE-LC-MS/MS

40 33

37 32

Cheng et al. (2010) Taylor et al. (2005)

6/ 2 8 C/4 d 10/2 C/11 d

2-DE-HPLC-ESI-MS/MS

260

68

Dumonta et al. (2011)

4 C/14 d

2-DE MALDI-TOF

60

26

Renaut et al. (2004)

5 C/0, 21, 35 d

2-DE MALDI-TOF/TOF

114

67

Renaut et al. (2008)

Doongara anther Japonica seedling leaf

Thellungiella halophila Chicory Festuca pratensis

Shandong leaf

Glycine max Pisum sativum

Gen, 222 seed Green fest leaf mitochondria Terese Champagne root stem, leaf Leaf

Populus tremula x P. tremuloids Prunus persica

Root

Canadian harmony bark

(Continued)

Table 2.3 (Continued) Plant Material

Variety and Tissue

Treatment

Approach

UPs

IDs

Reference

Triticum aestivum

Mironovskaya 808 leaf

2 C/21 d

2-DEnanoLC-LC-MS/MS (Q-TOF)

40 (C) 33 (T)

40 (C) 33 (T)

Vitamvas et al. (2007a)

Fang, Wyuna Grain Thesee-grain

40 C/3 d

2-DE MALDI-TOF

48

7

Skylas et al. (2002)

34 C/several days 42 C/3 d 42 C/12 h, 1 d

2-DE MALDI-TOF, LC-MS/MS 2-DE MALDI-TOF/TOF 2-DE MALDI-TOF 2-DE MALDI-TOF/TOF 2-DE MALDI-TOF/TOF, Q-TRAP LC-MS/MS

43

42

Majoul et al. (2004)

62 73 49 14

51 48 30 14

Ferreira et al. (2006) Lee et al. (2007) Zhang et al. (2010b) Sule et al. (2004)

Heat Triticum aestivum

Populus euphratica Oryza sativa Carissa spinaram Hordeum vulgare

Leaf Leaf Shoot

40 C/2 h


51

these, 47 were up-regulated, 18 were down-regulated, and 8 were newly produced after heat treatment. The majority of the proteins are HSPs connected with improving protein stability and folding, suggesting that protein denaturation and regulation are critically disturbed by high-temperature stress. Other differentially expressed proteins relate to energy production, photosynthesis, cell wall biosynthesis, and stress (Lee et al., 2007). Another characteristic feature of heat stress is oxidative damage. The up-regulation of several enzymes involved in redox homeostasis, such as GST, dehydroascorbate reductase (DHAR), thioredoxin h-type (Trx h), and chloroplast precursors of SOD, was reported (Lee et al., 2007). Concerning energy metabolism, an increased accumulation of enzymes involved in the biosynthesis of UDP-glucose (UDP glucose pyrophosphorylase UGPase), thiamine and dehydrogenation of pyruvate (pyruvate dehydrogenase), and transketolase was detected after addition of heat (Lee et al., 2007). This study showed that heat stress affects proteins, namely sHSPs. The heat stress response of the grains of two cultivars of wheat, susceptible Wyuna and tolerant Fang, during the filling period has been studied using proteomics (Skylas et al., 2002). The results indicated that Fang expressed more diverse and more abundant HSPs in comparison to Wyuna. The majority of these proteins were identified as sHSPs. Further, some isoforms of sHSPs showed differences in expression levels between the two cultivars. Two more studies examined the effect of heat stress on the protein composition of hexaploid wheat during grain filling; one characterized the heat-responsive proteins from total endosperm (Majoul et al., 2003), while the other characterized heat-responsive proteins from a nonprolamin fraction (Majoul et al., 2004). The study of the proteome response from total endosperm identified 36 protein spots to be up-regulated and 1 spot to be down-regulated (Majoul et al., 2003). Among the heat-induced proteins were several HSPs belonging to the HSP90, HSP70, and sHSP families; other stress-related proteins and enzymes were involved in cellular metabolism. The down-regulated protein was glucose-1-phosphate adenyltransferase, which is known to play a role in starch synthesis. In the study of the nonprolamin, or water-soluble, fraction 24 protein spots were up-regulated, while 19 were down-regulated (Majoul et al., 2004). Proteomic analyses of heat-stress response have been performed on barley (Hordeum vulgare) shoots of two cultivars, Jubilant (abiotic stress-susceptible, spring type) and Mandolina (abiotic stress-tolerant, spring type) (Sule et al., 2004). The study revealed the up-regulated expression of distinct isoforms of several sHSPs and S-adenosylmethionine synthetase (SAM-S) in cv. Mandolina compared to cv. Jubilant. Expressions of two sHSPs were found exclusive to cv. Jubilant (Sule et al., 2004). Zhang et al. (2009b) reported that a calmodulin knockout reduced thermotolerance in Arabidopsis, and a search for calmodulin-binding proteins by a proteomic approach revealed a 85 kDa HSP protein as an interacting protein in sorghum (Viridi et al., 2009). A proteomic approach has been carried out to study the effect of a combination of drought and heat stress on Arabidopsis (Koussevitzky et al., 2008). The authors identified 45 proteins that were distinctive to combined drought and heat stress. Of these proteins, 16 are chloroplastic, indicating the significant role of the chloroplast in plant stress responses. The other proteins are related to ROS detoxification, malate metabolism, and the Calvin cycle (Koussevitzky et al., 2008). Proteomic studies were applied to the analysis of changes in tomato pericarp proteins under heat stress (Iwahashi and Hosoda, 2000). This study detected a total of 12,000 proteins in control conditions, and an abundance of the expression level of 27% of the proteins was induced by heat stress. Fourteen novel proteins were up-regulated only under heat stress conditions (Iwahashi and Hosoda, 2000).

52


Proteins of the HSP family and their upstream transcription factors have also been proven to play a role in the thermotolerance of tomato (Yang et al., 2006). Ahsan et al. (2010c) reported enhanced accumulation of several other proteins with chaperone functions (chaperonin 60b subunit CPN60-b, HS90, chaperonin CPN10, and chloroplast chaperonin) in soybean seedlings under heat stress. Another proteomic study revealed the expression of the HSP-interacting proteins for the improvement of heat stress tolerance in soybean (Zhu et al., 2006). Proteomic approaches were used to understand the mechanisms concerned with heat stress tolerance in Populus euphratica, considered as a model plant for analyzing abiotic stresses including extreme temperatures, drought, and salt (Ferreira et al., 2006). Based on the protein accumulation pattern, heat-responsive proteins were grouped into proteins that have short-term up-regulation, long-term up-regulation, short-term down-regulation, and long-term down-regulation. The results showed that short-term up-regulated proteins were involved in membrane destabilization, cytoskeleton restructuring, sulfur assimilation, thiamine and hydrophobic amino acid biosynthesis, and protein stability. Proteins with increased accumulation for longer periods were associated with redox homeostasis and photosynthesis. The results also indicated that protein synthesis was disturbed at the early stages of heat stress but improved afterward (Ferreira et al., 2006). Protein expression has been examined in two ecotypes, low elevation and high elevation, of Picea abies (Norway spruce) in response to high-temperature stress (Valcu et al., 2008). The analysis of needles showed an increased abundance of sHSPs during recovery from heat stress, precisely in the low elevation ecotype. The expression of glyceraldehyde-3-phosphate dehydrogenase was enhanced in the high elevation ecotype during recovery and was reduced later (Valcu et al., 2008). A proteomic study was conducted with the roots of two C3 grasses: Agrostis scabra (a geothermal species capable of surviving in soils heated at 4550 C) and Agrostis stolonifera (heat-sensitive) (Xu and Huang, 2008). The study revealed differential expression of 70 protein spots. Of these, 66 were identified as being related to energy production. A. scabra exhibited more upregulated protein spots than A. stolonifera under heat stress. The proteins exclusively regulated by heat in A. scabra were sucrose synthase, superoxide dismutase, glutathione S-transferase, and stress-inducible HSP. A study was carried out on differential proteome analysis of peach (Prunus) fruits subjected to heat stress. It revealed expression of several heat-responsive proteins (Lara et al., 2009). Heat-stress response at the proteome level has also been studied, predominantly with a heat- and drought-tolerant Populus euphratica (Ferreira et al., 2006) and with the wild plant, Carissa spinarum, that inhabits hot and dry valleys in central China (Zhang et al., 2010b). These authors reported that heat stress induced profound changes in cytoskeleton composition, indicating its reorganization. In addition, an increased accumulation of some eukaryotic translation initiation factors (eIF4F and eIF5A-3) was observed, indicating profound cellular organization leading to programmed cell death (PCD) under heat stress. Studies by Li et al. (2009) on Suaeda salsa and Yang et al. (2012b) on Portulaca showed the differential expression of 440 and 51 proteins, respectively, under heat-stress conditions. The functional analysis and categorization of differentially expressed heat stress-related proteins revealed that they are HSP, energy and metabolism, redox homeostasis, protein biosynthesis and degradation, signal transduction, lignin biosynthesis, antioxidant enzymes, and regulatory and storage proteins. However, information on the systemic response of plants to heat stress is still limited because plant perception and response to a single environmental stress is not specific to the stress but often uses factors common to the response to other stresses.


53

2.3.5.2 Cold stress Chilling or cold is a key environmental stress and a serious limitation on crop growth and productivity in many parts of the world (Renaut et al., 2004). Commonly, plants deriving from temperate regions display a variable degree of chilling tolerance and can enhance their tolerance ability during exposure to chilling, and temperatures above freezing—cold acclimation. On the other hand, plants from tropical and subtropical regions are sensitive to chilling and generally lack the cold acclimation mechanism (Renaut et al., 2004). Similar to high/elevated temperatures, chilling temperatures directly result in the slowdown of metabolic processes, loss of membrane functions, and thus to cold stress. Based on their ability to survive chilling temperatures, plants are classified into three types: (1) chilling sensitive, (2) chillingtolerant/resistant, and (3) freezing-tolerant (Hallgren and Oquist, 1990). Thakur et al. (2010) defined chilling-sensitive plants as those exhibiting metabolic dysfunction when subjected to temperatures marginally below the optimum; while chilling-tolerant plants endure lower than optimum, nonfreezing temperatures. Freezing-tolerant plants have the capacity to survive in below freezing conditions. Cold induces significant changes in many metabolic pathways, particularly energy metabolism, oxidative processes, gene regulation, and cell compartmentation (Apel and Hirt, 2004). During cold acclimation, plants initiate numerous molecular events, all of which enhance tolerance to freezing temperatures (Kjellsen et al., 2010). The proteomic approach has been applied successfully to analyze the cold-responsive proteins in Arabidopsis thaliana (Bae et al., 2003; Kawamura and Uemura, 2003; Amme et al., 2006), Thellungiella halophila (Gao et al., 2009), Oryza sativa (Imin et al., 2004, Cui et al., 2005, Yan et al., 2006; Hashimoto and Komatsu, 2007; Lee et al., 2007, 2009), chicory (Degand et al., 2009), Festuca pratensis (Kosmala et al., 2009), Glycine max (Cheng et al., 2010), Pisum sativum (Taylor et al., 2005; Dumonta et al., 2011), Triticum aestivum (Vitamvas et al., 2007b), as well as in woody species such as poplar (Renaut et al., 2004) and Prunus persica (Renaut et al., 2008). Organs (e.g., leaf, root, stem, anther, and embryo) have been studied. Proteomic studies have also been carried out at the organellar level using plasma membrane, nucleus, and mitochondria for analyzing cold stress (see Table 2.3). Imin et al. (2004) studied the effects of mild cold stress on the proteome of anthers of cultivar (cv.) Doongara of rice. The study gave insights primarily into the effect of cold damage at the early microspore development stage and the resulting cold-induced male sterility due to incomplete ripening of pollen grains. UDP-glucose pyrophosporylase or sucrose synthase, a protein associated with the formation of UDP-glucose, has been found to up-regulate in response to short-term cold treatment in the leaf blade of Japonica rice seedlings (Cui et al., 2005). Yan et al. (2006) carried out a similar study on cold-inducible changes at the protein and transcript level in a Dongin variety of rice seedlings. A connection between the dynamics of proteins and mRNA was perceived for most down-regulated proteins, except for two: ferredoxin-nitrite reductase and an unknown protein. For the up-regulated proteins, the relationship between protein and transcript dynamics was observed only for five proteins: myosin-like, putative PGM, putative phosphatase, 2 C-like, putative glycerol-3-phosphate dehydrogenase (NAD1), and a hypothetical protein. This study revealed that photosynthetic proteins are largely affected under cold stress, which may explain the decrease of net photosynthetic rate and ultimately the reduction in crop yield associated with cold temperatures (Yan et al., 2006). S-adenosylmethionine (SAM) is a donor of the methyl group in methylation reactions and a precursor of ethylene and polyamines with levels that increase considerably when exposed to cold (Cui et al., 2005; Amme et al., 2006; Yan et al., 2006).

54


Lee et al. (2007) analyzed the stress-responsive proteome of leaves’ moderate and extreme cold stress. Fourteen spots were found to be up-regulated by cold stress and seven cold-responsive proteins were newly identified. Four antioxidant enzymes (i.e., APX, glutathionine S-transferase, thioredoxin h, and thioredoxin peroxidase) are known to be induced by oxidative stress caused by ROS. In another study, one of the new cold-induced proteins, a RING zinc finger protein-like one, was found to be markedly responsive only to extreme cold stress (Lee et al., 2009). After lowtemperature exposure, 37 protein spots exhibited differential expression and 27 proteins were identified by MS. The majority of the proteins affected by cold stress were associated with energy production (Lee et al., 2009). Komatsu et al. (2009c) identified 12 N-glycosylated proteins that were differentially expressed in rice leaf sheaths following exposure to cold. Among the proteins detected, a calreticulin displayed both glycosylation and phosphorylation in leaf sheaths in response to cold stress. Calreticulin is an important protein that may control the expression levels of other proteins (Komatsu et al., 2009c). Several studies have been conducted to reveal the proteomic responses of Arabidopsis to cold temperature stress. The nuclear proteome of Arabidopsis was characterized and its response to cold temperature stress was examined by Bae et al. (2003). A total of 184 proteins were detected from the nuclear proteome and 54 displayed at least a two-fold alteration in accumulation. Of the 54 proteins, 40 were up-regulated, while 14 were down-regulated. These proteins were associated with RNA metabolism, protein synthesis, protein folding, and transcriptional regulation (Bae et al., 2003). Cold stress also increased the accumulation of proteins with chaperone functions (e.g., different HSPs), as well as cytosolic, chloroplastic, and mitochondrial chaperonins (Kawamura and Uemura, 2003). Enhanced levels of RNA-binding protein cp29 and Rieske protein have been reported frequently (Amme et al., 2006). An up-regulation of stroma-located components of the Calvin cycle, especially Rubisco and Rubisco activase, has also been observed (Amme et al., 2006). The proteomes of the chloroplast lumen and stroma of Arabidopsis have also been examined under cold stress (Goulas et al., 2006). The stromal proteome shows an increased abundance of 52 spots in response to cold treatment. Of these, 8 novel proteins were induced and 31 proteins were up-regulated while 13 were down-regulated. The functions found include proteins involved in stress-sensing, signal transduction, photosynthesis, other plastid metabolic functions, and hormone biosynthesis (Goulas et al., 2006). An enhanced level of Rieske protein and plastocyanin was also observed in coldtreated Thellungiella halophila (Gao et al., 2009). Most studies also have noted changes in the abundance of enzymes associated with carbohydrate metabolism. Overall, up-regulation of catabolic pathways and down-regulation of anabolic pathways also may be perceived. The Pisum sativum leaf mitochondrial proteome has been examined to study the effect of cold stress in combination with drought and herbicide application (Taylor et al., 2005). Thirty-three proteins were found to be differentially abundant: glycine decarboxylase, serine hydroxyl methyl transferase, TCA cycle, oxidative phosphorylation complexes, and HSPs. Proteomic studies were conducted to determine cold stress response (2 C) in two genotypes of meadow fescue (Festuca pratensis) differing in their frost tolerance (Kosmala et al., 2009). This study revealed the increased abundance of several components of thylakoid-membrane-connected photosynthetic apparatus containing oxygen-evolving enhancer protein 1 OEE1 (OEC), light-harvesting complexes, cytochrome b6/f complex ironsulfur subunit, or Rieske FeS protein (Kosmala et al., 2009). Enhanced levels of Cu/Zn-SOD have also been reported in roots of chicory (Degand et al., 2009).

2.4 Conclusion and future prospects

55

In wheat, cold-induced up-regulation of some HSP proteins with chaperone functions, namely HSP70, and down-regulation of some other HSP proteins, namely HSP90, have been observed (Vitamvas et al., 2007b). Renaut et al. (2004) applied proteomic technologies to examine the nature of molecular changes in leaves of poplar during cold acclimation. More than 800 leaf protein spots were reproducibly detected on 2-DE gels, with 60 spots displaying changes in abundance in response to cold stress. Using PMF, 26 proteins were associated with ROS defense—for example, the detoxifying enzymes ascorbate peroxidase, thioredoxin, and peroxiredoxin. The increased abundance of molecular chaperone-like proteins involved in protein folding and stabilization was also observed. Proteomic analysis of the bark proteome of Prunus persica was conducted in response to cold stress. Proteins that increased in abundance were functionally categorized as being connected with stress response, lignin metabolism, glycolysis, amino acid metabolism, protein catabolism, or acting as chaperones. Proteins down-regulated under cold stress were associated with plant hormone response, cytoskeletal organization, defense mechanisms, and photosynthesis. The elucidation of other cold-stress proteomes from monocot and dicot crop species is needed; together they can provide the insights required to understand the cold stress biology of plants and may be useful for producing cold-tolerant plants in the future.

2.4 Conclusion and future prospects The present chapter summarizes studies on the influence of various abiotic stress factors on the proteome of plants. The majority of them in the existing literature are based on comparative proteomics using either stressed versus nonstressed plants (control) or sensitive verus tolerant plants. Most studies on this topic use 2-DE, but recently the 2-DE/MALDI-TOF MS/MS approach is about equal in importance, compared to gel-free LC-MS/MS, for analyzing plants’ responses to abiotic stresses. The most remarkable recent change is the switch from studying the total proteome to a more focused method (e.g., subcellular proteomics of the nuclear, mitochondrial, plastid proteomes). As more results become available, it is gradually evident that abiotic stresses cause distinct molecular responses in plant tissues. A lot of information is also accessible on changes in cellular metabolism as well as stress-protective proteins in plant proteome under stress. Insights are scanty, however, about the less abundant regulatory proteins associated with stress signaling and regulation of gene expression. Overall, proteomic approaches have proved to be useful not only for unraveling reprogramming of plants’ responses to various abiotic stresses as a whole but also to dissect stress-responsive pathways. Advances in approaches and techniques may change the manner in which plant stress proteomics studies are performed. Improved protein extraction protocols and innovations in technology, such as multidimensional protein fractionation, isobaric tags for comparative and absolute quantitation, label-free quantification mass spectrometry, and phosphoprotein, and glycoprotein enrichment and tagging, may permit the discovery of proteins and novel regulatory mechanisms that occur during abiotic stress signaling and related metabolic pathways. The integration of proteomics with transcriptomics, metabolomics, and bioinformatics is expected to enable more insights into the molecular networks underlying salt stress response and tolerance.

56


By summarizing important contributions related to abiotic stresses and plant proteomes, efforts have been made to define the molecular basis of the acquisition of the stress-tolerance mechanism. The information here may further assist with finding protein biomarkers linked to plants’ abiotic stress tolerance. Future initiatives should be taken to identify and characterize those proteins that may open a new avenue for proteome-based abiotic stress research. Finally, we hope that this chapter has not only provided new insights into plants’ stress response mechanisms, which are necessary for continued development of genetically engineered stress-tolerant crop plants, but also has highlighted the significance of studying changes in protein abundance in response to abiotic stress factors.

References Abbasi, F.M., Komatsu, S.A., 2004. Proteomic approach to analyze salt-responsive proteins in rice leaf sheath. Proteomics 4, 20722081. Afroz, A., Ali, G.M., Mir, A., Komatsu, S., 2011. Application of proteomics to investigate stress-induced proteins for improvement in crop protection. Plant Cell Rep. 30, 745763. Aggarwal, K., Choe, L.H., Lee, K.H., 2006. Shotgun proteomics using the iTRAQ isobaric tags. Brief. Funct. Genomics Proteomics 5, 112120. Ahsan, N., Lee, D.G., Lee, S.H., Kang, K.Y., Bahk, J.D., Choi, M.S., et al., 2007a. A comparative proteomic analysis of tomato leaves in response to waterlogging stress. Physiol. Plant 131, 555570. Ahsan, N., Lee, D.G., Lee, S.H., Kang, K.Y., Lee, J.J., Kim, P.J., et al., 2007b. Excess copper induced physiological and proteomic changes in germinating rice seeds. Chemosphere 67, 11821193. Ahsan, N., Lee, D.G., Lee, S.H., Lee, K.W., Bahk, J.D., Lee, B.H., 2007c. A proteomic screen and identification of water logging regulated proteins in tomato roots. Plant Soil 295, 3751. Ahsan, N., Lee, S.H., Lee, D.G., Lee, H., Lee, S.W., Bahk, J.D., et al., 2007d. Physiological and protein profiles alternation of germinating rice seedlings exposed to acute cadmium toxicity. C. R. Biol. 330, 735746. Ahsan, N., Lee, D.G., Alam, I., Kim, P.J., Lee, J.J., Ahn, Y.O., et al., 2008. Comparative proteomic study of arsenic-induced differentially expressed proteins in rice roots reveals glutathione plays a central role during as stress. Proteomics 8, 35613576. Ahsan, N., Renaut, J., Komatsu, S., 2009. Recent developments in the application of proteomics to the analysis of plant responses to heavy metals. Proteomics 9, 26022621. Ahsan, N., Donnart, T., Nouri, M.Z., Komatsu, S., 2010a. Tissue specific defense and thermo-adaptive mechanisms of soybean seedlings under heat stress revealed by proteomic approach. J. Proteome Res. 9, 41894204. Ahsan, N., Lee, D.G., Kim, K.H., Alam, I., Lee, S.H., Lee, K.W., et al., 2010b. Analysis of arsenic stressinduced differentially expressed proteins in rice leaves by two-dimensional gel electrophoresis coupled with mass spectrometry. Chemosphere 78, 224231. Ahsan, N., Nanjo, Y., Sawada, H., Kohno, Y., Komatsu, S., 2010c. Ozone stress-induced proteomic changes in leaf total soluble and chloroplast proteins of soybean reveal that carbon allocation is involved in adaptation in the early developmental stage. Proteomics 10, 26052619. Aina, R., Labra, M., Fumagalli, P., Vannini, C., Marsoni, M., Cucchi, U., et al., 2007. Thiol-peptide level and proteomic changes in response to cadmium toxicity in Oryza sativa L. roots. Environ. Exp. Bot. 59, 381392. Alam, I., Lee, D.G., Kim, K.H., Park, C.H., Sharmin, S.A., Lee, H., et al., 2010. Proteome analysis of soybean roots under water logging stress at an early vegetative stage. J. Biosci. 35, 4962.

References

57

Ali, G.M., Komatsu, S., 2006. Proteomic analysis of rice leaf sheath during drought stress. J. Proteome Res. 5, 396403. Alvarez, S., Marsh, E.L., Schroeder, S.G., Schachtman, D.P., 2008. Metabolomic and proteomic changes in the xylem sap of maize under drought. Plant Cell Environ. 31, 325340. Alvarez, S., Berla, B.M., Sheffield, J., Cahoon, R.E., Jez, J.M., Hicks, L.M., 2009. Comprehensive analysis of the Brassica juncea root proteome in response to cadmium exposure by complementary proteomic approaches. Proteomics 9, 24192431. Alves, M., Francisco, R., Martins, I., Ricardo, C.P.P., 2006. Analysis of Lupinus albus leaf apoplastic proteins in response to boron deficiency. Plant Soil 279, 111. Alves, M., Moes, S., Jeno, P., Pinheiro, C., Passarinho, J., Ricardo, C.P., 2011. The analysis of Lupinus albus root proteome revealed cytoskeleton altered features due to long-term boron deficiency. J. Proteomics 74, 13511363. Amme, S., Matros, A., Schlesier, B., Mock, H.P., 2006. Proteome analysis of cold stress response in Arabidopsis thaliana using DIGE-technology. J. Exp. Bot. 57, 15371546. Andaluz, S., Lopez-Millan, A.F., De Las, R.J., Aro, E.M., 2006. Proteomic profiles of thylakoid membranes and changes in response to iron deficiency. Photosynth. Res. 89, 141155. Apel, K., Hirt, H., 2004. Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu. Rev. Plant Biol. 55, 373399. Bae, M.S., Cho, E.J., Choi, E.Y., Park, O.K., 2003. Analysis of the Arabidopsis nuclear proteome and its response to cold stress. Plant J. 36, 652663. Bahrman, N., Le Gouis, J., Negroni, L., Amilhat, L., 2004. Differential protein expression assessed by twodimensional gel electrophoresis for two wheat varieties grown at four nitrogen levels. Proteomics 4, 709719. Bahrman, N., Gouy, A., Devienne-Barret, F., Hirel, B., 2005. Differential change in root protein patterns of two wheat varieties under high and low nitrogen nutrition levels. Plant Sci. 168, 8187. Barkla, B.J., Castellanos-Cervantes, T., Diaz de leon, J.L., Matros, A., Mock, H.P., Perez-Alfocea, F., et al., 2013. Elucidation of salt stress defense and tolerance mechanisms of crop plants using proteomics—current achievements and perspectives. Proteomics 13, 18852000. Baum, M., von Korff, M., Guo, P., Lakew, B., Udupa, S.M., Sayed, H., et al., 2007. Molecular approaches and breeding strategies for drought tolerance in barley. In: Varshney, R., Tuberosa, R. (Eds.), Genomic Assisted Crop Improvement. Springer, Amsterdam, pp. 5179. Bazargani, M.M., Sarhadi, E., Bushehri, A.A.S., Matros, A., Mock, H.P., Naghavi, M.R., et al., 2011. A proteomics view on the role of drought-induced senescence and oxidative stress defense in enhanced stem reserves remobilization in wheat. J. Prot. 74, 19591973. Bedon, F., Villar, E., Vincent, D., Dupuy, J.W., Lomenech, A.M., Mabialangoma, A., et al., 2012. Proteomic plasticity of two Eucalyptus genotypes under contrasted water regimes in the field. Plant Cell Environ. 35, 790805. Benesova, M., Hola, D., Fischer, L., Jedelsky, P.L., Hnilicka, F., Wilhelmova, N., et al., 2012. The physiology and proteomics of drought tolerance in maize: early stomata closure as a cause of lower tolerance to shortterm dehydration? PloS One 7, e38017. Bhushan, D., Jaiswal, D.K., Ray, D., Basu, D., Datta, A., Chakraborty, S., et al., 2011. Dehydration-responsive reversible and irreversible changes in the extracellular matrix: comparative proteomics of chickpea genotypes with contrasting tolerance. J. Proteome Res 10, 20272046. Bona, E., Marsano, F., Cavaletto, M., Berta, G., 2007. Proteomic characterization of copper stress response in Cannabis sativa roots. Proteomics 7, 11211130. Bonhomme, L., Monclus, R., Vincent, D., Carpin, S., Claverol, S., Lomenech, A.M., et al., 2009. Genetic variation and drought response in two Populus x Euramericana genotypes through, 2-DE proteomic analysis of leaves from field and glasshouse cultivated plants. Phytochemistry 70, 9881002.

58


Boyer, J.S., 1982. Plant productivity and environment. Science 218, 443448. Boyer, J.S., Westgate, M.E., 2004. Grain yields with limited water. J. Exp. Bot. 55, 23852394. Brumbarova, T., Matros, A., Mock, H.P., Bauer, P., 2008. A proteomic study showing differential regulation of stress, redox regulation and peroxidase proteins by iron supply and the transcription factor FER. Plant J. 54, 321334. Caruso, G., Cavaliere, C., Foglia, P., Gubbiotti, R., Samperi, R., Lagana, A., 2009. Analysis of drought responsive proteins in wheat (Triticum durum) by 2D-PAGE and MALDI-TOF mass spectrometry. Plant Sci. 177, 570576. Castillejo, M.A., Maldonado, A.M., Ogueta, S., Jorrin, J.V., 2008. Proteomic analysis of responses to drought stress in sunflower (Helianthus annuus) leaves by 2DE gel electrophoresis and mass spectrometry. Open Proteomics J. 1, 5971. Chen, F.G., Zhang, S., Jiang, H., Ma, W.J., Korpelainen, H., Li, C., 2011. Comparative proteomics analysis of salt response reveals sex-related photosynthetic inhibition by salinity in Populus cathayana cuttings. J. Proteom. Res. 10, 39443958. Chen, S.B., Gollop, N., Heuer, B., 2009. Proteomic analysis of salt stressed tomato (Solanum lycopersicum) seedlings: effect of genotype and exogenous application of glycine betaine. J. Exp. Bot. 60, 20052019. Cheng, L., Gao, X., Li, S., Shi, M., Javeed, H., Jing, X., et al., 2010. Proteomic analysis of soybean (Glycine max (L.) Meer.) seeds during inhibition at chilling temperature. Mol. Breed. 26, 117. Chevalier, F., Rossignol, M., 2011. Proteomic analysis of (Arabidopsis thaliana) ecotypes with contrasted root architecture in response to phosphate deficiency. J. Plant Physiol. 168, 18851890. Chinnusamy, V., Jagendorf, A., Zhu, J.K., 2005. Understanding and improving salt tolerance in plants. Crop Sci. 45, 437448. Choudhary, M.K., Basu, D., Datta, A., Chakraborty, N., Chakraborty, S., 2009. Dehydration-responsive nuclear proteome of rice (Oryza sativa L.) illustrates protein network, novel regulators of cellular adaptation, and evolutionary perspective. Mol. Cell Proteomics 8, 15791598. Cramer, G.R., Urano, K., Delrot, S., Pezzotti, M., Shinozaki, K., 2011. Effects of abiotic stress on plants: a systems biology perspective. BMC Plant Biol. 11, 163176. Cramer, G.R., Van Sluyter, S.C., Hopper, D.W., Pascovici, D., Keighley, T., Haynes, P.A., 2013. Proteomic analysis indicates massive changes in metabolism prior to the inhibition of growth and photosynthesis of grape vine (Vitis vinifera L.) in response to water deficit. BMC Plant Biol. 13, 4971. Cui, S., Huang, F., Wang, J., Ma, X., Cheng, Y., Liu, J., 2005. A proteomic analysis of cold stress responses in rice seedlings. Proteomics 5, 31623172. Degand, H., Faber, A.M., Dauchot, N., Mingeot, D., Watillon, B., Cutsem, P.V., et al., 2009. Proteomic analysis of chicory root identifies proteins typically involved in cold acclimation. Proteomics 9, 29032907. Donnini, S., Prinsi, B., Negri, A.S., Vigani, G., 2010. Proteomic characterization of iron deficiency responses in (Cucumis sativus L.) roots. BMC Plant Biol 10, 268282. Dumonta, E., Bahrmana, N., Goulasa, E., Valotc, B., Sellier, H., Hilberta, J.L., et al., 2011. A proteomic approach to decipher chilling response from cold acclimation in pea (Pisum sativum L.). Plant Sci. 180, 8698. Duquesnoy, I., Goupil, P., Nadaud, I., Branlard, G., Piquet-Pissaloux, A., Ledoigt, G., 2009. Identification of Agrostis tenuis leaf proteins in response to As (V) and As (III) induced stress using a proteomics approach. Plant Sci. 176, 206213. Durand, T.C., Sergeant, K., Planchon, S., Carpin, S., Label, P., Morabito, D., et al., 2010. Acute metal stress in Populus tremula x P. alba (717-1B4 genotype): leaf and cambial proteome changes induced by cadmium (21). Proteomics 10, 349368. Duressa, D., Soliman, K., Robert, T., Senwo, Z., 2011. Proteomic analysis of soybean roots under aluminum stress. Int. J. Plant Genomics 112.

References

59

Echevarria-Zomeno, S., Ariza, D., Jorge, I., Lenz, C., Del Campo, A., Jorrin, J.V., et al., 2009. Changes in the protein profile of Quercus ilex leaves in response to drought stress and recovery. J. Plant Physiol. 166, 233245. Fecht-Christoffers, M.M., Braun, H.P., Lemaitre-Guillier, C., Van Dorsselaer, A., Horst, W.J., 2003. Effect of manganese toxicity on the proteome of the leaf apoplast in cowpea. Plant Physiol. 133, 19351946. Feller, U., Anders, I., Mae, T., 2008. Rubisco lytics: fate of Rubisco after its enzymatic function in a cell is terminated. J. Exp. Bot. 59, 16151624. Feng, W., Li, Z., Guo, B., Peng, H., 2012. Identification of differential expressed proteins responding to phosphorus starvation based on proteomic analysis in roots of wheat (Triticum aestivum L.). Acta Agron. Sin. 38, 780790. Ferreira, S., Hjerno, K., Larsen, M., Wingsle, G., et al., 2006. Proteome profiling of Populus euphratica Oliv. upon heat stress. Ann. Bot. 98, 361377. Food and Agriculture Organization (FAO) 2007. Mapping biophysical factors that influence agricultural production and rural vulnerability. Available at:,http://faostat.fao.org/.. Ford, K.L., Cassin, A., Baci, C., 2011. Quantitative proteomic analysis of wheat cultivars with differing drought stress tolerance. Front. Plant Sci. 2, 111. Fuhrs, H., Hartwig, M., Molina, L.E., Heintz, D., Van Dorsselaer, A., Braun, H.P., et al., 2008. Early manganese-toxicity response in Vigna unguiculata L.—a proteomic and transcriptomic study. Proteomics 8, 149159. Fukuda, T., Saito, A., Wasaki, J., Shinano, T., Osaki, M., 2007. Metabolic alterations proposed by proteome in rice roots grown under low P and high Al concentration under low pH. Plant Sci. 172, 11571165. Gao, F., Zhou, Y., Zhu, W., Li, X., Fan, L., Zhang, G., 2009. Proteomic analysis of cold stress-responsive proteins in Thellungiella rosette leaves. Planta 230, 10331046. Gazanchian, A., Hajheidari, M., Sima, N.K., et al., 2007. Proteome response of Elymus elongatum to severe water stress and recovery: integrated approaches to sustain and improve plant production under drought stress. J. Exp. Bot. 58, 291300. Ge, P., Ma, C., Wang, S., Gao, L., Li, X., Guo, G., et al., 2012. Comparitive proteomic analysis of grain development in two spring wheat varieties under drought stress. Anal. Bioanal. Chem. 402, 12971313. Ghabooli, M., Khatabi, B., Ahmadi, F.S., Sepehri, M., Mirzaei, M., Amirkhani, A., et al., 2013. Proteomics study reveals the molecular mechanisms underlying water stress tolerance induced by Piriformospora indica in barley. J. Proteomics 94, 289301. Goulas, E., Schubert, M., Kieselbach, T., Kleczkowski, L.A., Gardestrom, P., Schroder, W., et al., 2006. The chloroplast lumen and stromal proteomes of Arabidopsis thaliana show differential sensitivity to short- and long-term exposure to low temperature. Plant J. 47, 720734. Grimplet, J., Wheatley, M.D., Jouria, H.B., Deluc, L.G., Cramer, G.R., Cushman, J.C., 2009. Proteomic and selected metabolite analysis of grape berry tissues under well-watered and water-deficit stress conditions. Proteomics 9, 25032528. Gu, X., Gao, Z., Zhuang, W., Qiao, Y., Wang, X., Mi, L., et al., 2013. Comparative proteomic analysis of rd29A: RdreB1BI transgenic and non-transgenic strawberries exposed to low temperature. J. Plant Physiol. 170, 696706. Hadiarto, T., Tran, L.P., 2011. Progress studies of drought responsive genes in rice. Plant Cell Rep. 30, 297310. Hajheidari, M., Abdollahian-Noghabi, M., Askari, H., Heidari, M., Sadeghian, S.Y., Ober, E.S., et al., 2005. Proteome analysis of sugar beet leaves under drought stress. Proteomics 5, 950960. Hajheidari, M., Eivazi, A., Buchanan, B.B., Wong, J.H., Majidi, I., Salekdeh, G.H., 2007. Proteomics uncovers a role for redox in drought tolerance in wheat. J. Proteome Res. 6, 14511460. Hakeem, K.R., Chandaana, R., Ahemad, R.P., Iqbal, M., Ozaturk, M., 2012a. Relevance of proteomic investigations in plant abiotic stress physiology. OMICS: J. Integ. Biol. 16, 621635.

60


Hakeem, R., Khan, F., Chandana, R., Siddiqui, T.O., Iqbal, M., 2012b. Genotypic variability among soybean genotypes under NaCl stress and proteome analysis of salt-tolerant genotype. Appl. Biochem. Biotech. 168, 23092329. Hallgren, J.-E., Oquist, G., 1990. Adaptations to low temperature. In: Alscher, R.G., Cummings, G.R. (Eds.), Stress Responses in Plants: Adaptation and Acclimation Mechanisms. Wiley-Liss Inc, New York, pp. 265293. Haque, M.E., Kawaguchi, K., Komatsu, S., 2011. Analysis of proteins in aerenchymatous seminal roots of wheat grown in hypoxic soil under waterlogged conditions. Protein Peptide Lett. 18, 912924. Hart, J.J., Welch, R.M., Norvell, W.A., Kochian, L.V., 2006. Characterization of cadmium uptake, translocation and storage in near-isogenic lines of durum wheat that differ in grain cadmium concentration. New Phytol. 172, 261271. Hashiguchi, A., Ahasan, N., Komatsu, S., 2009a. Proteomics application of crops in the context of climate changes. Food Res. Inter. 43, 18031813. Hashiguchi, A., Sakata, K., Komatsu, S., 2009b. Proteome analysis of early-stage soybean seedlings under flooding stress. J. Proteome Res. 8, 20582069. Hashimoto, M., Komatsu, S., 2007. Proteomic analysis of rice seedlings during cold stress. Proteomics 7, 12931302. Hinsinger, P., Bengough, A.G., Vetterien, D., Young, I.M., 2009. Rhizospheric biophysics, biogeochemistry and ecological relevance. Plant Soil 321, 117152. Horn, R., Chudobova, I., Hansel, U., Herwartz, D., Koskull-Doring, P.V., Schillberg, S., 2013. Simultaneous treatment with tebuconazole and abscisic acid induces drought and salinity stress tolerance in Arabidopsis thaliana by maintaining key plastid protein levels. J. Proteome Res. 12, 12661281. Hossain, Z., Komatsu, S., 2013. Contribution of proteomic studies towards understanding plant heavy metal stress response. Front. Plant Sci. 3, 112. Hossain, Z., Hajika, M., Komatsu, S., 2012a. Comparative proteome analysis of high and low cadmium accumulating soybeans under cadmium stress. Amino Acids 43, 23932416. Hossain, Z., Makino, T., Komatsu, S., 2012b. Proteomic study of β-aminobutyric acid-mediated cadmium stress alleviation in soybean. J. Proteomics 75, 41514164. Hossain, Z., Nouri, M.Z., Komatsu, S., 2012c. Plant cell organelle proteomics in response to abiotic stress. J. Proteome Res. 11, 3748. Hradilova, J., Rehulka, P., Rehulkova, H., Vrbova, M., Griga, M., Brzobohaty, B., 2010. Comparative analysis of proteomic changes in contrasting flax cultivars upon cadmium exposure. Electrophoresis 31, 421431. Hu, Y., Schmidhalter, U., 2002. Limitation of salt stress to plant growth. In: Hock, B., Elstner, C.F. (Eds.), Plant Toxicology. Marcel Dekker, New York, pp. 91224. Hu, Y., Li, W.C., Xu, Y.Q., Li, G.J., Liao, Y., Fu, F.L., 2009. Differential expression of candidate genes for lignin biosynthesis under drought stress in maize leaves. J. Appl. Genet. 50, 213223. Imin, N., Kerim, T., Rolfe, B.G., Weinman, J.J., 2004. Effect of early cold stress on the maturation of rice anthers. Proteomics 4, 18731882. International Panel on Climate Change 2007. Climate Change: synthesis report. Pachauri, R.K. and Reisinger, A. (Eds.) IPCC, Geneva, Switzerland. Available at: ,www.ipcc.ch.. Iwahashi, Y., Hosoda, H., 2000. Effect of heat stress on tomato fruit protein capression. Electrophoresis 21, 17661771. Jaiswal, D.K., Ray, D., Choudhary, M.K., Subba, P., Kumar, A., Verma, J., et al., 2013. Comparative proteomics of dehydration response in the rice nucleus: new insights into the molecular basis of genotypespecific adaptation. Proteomics 2324, 34783497. Jiang, S.-S., Liang, X.-N., Li, X., Wang, S.-L., Lv, D.-W., Ma, C.-Y., et al., 2012. Wheat drought responsive grain proteome analysis by linear and non-linear, 2-DE and MALDi-TOF mass spectrometry. Int. J. Mol. Sci. 13, 1606516083.

References

61

Jogaiah, S., Govind, S.R., Tran, L.S.P., 2013. Systems biology-based approaches toward understanding drought tolerance in food crops. Crit. Rev. Biotech. 33, 2329. Jorge, I., Navarro, R.M., Lenz, C., Ariza, D., Jorrin, J., 2006. Variation in the holm oak leaf proteome at different plant developmental stages, between provenances and in response to drought stress. Proteomics 6, 207214. Kamal, A.H.M., Kim, K.H., Shin, K.H., Choi, J.S., Baik, B.K., Tsujimoto, H., et al., 2010. Abiotic stress responsive proteins of wheat grain determined using proteomics technique. Aust. J. Crop. Sci. 4, 196208. Kang, G., Li, G., Xu, W., Peng, X., Han, Q., Zhu, Y., et al., 2012. Proteomics reveals the effects of salicylic acid on growth and tolerance to subsequent drought stress in wheat. J. Proteome Res. 11, 60666079. Kang, J., Lin, C., Chen, J., Liu, Q., 2004. Copper induces histone hypoacetylation through directly inhibiting histone acetyltransferase activity. Chem. Biol. Interact. 148, 115123. Kausar, R., Arshad, M., Shahzad, A., Komatsu, S., 2013. Proteomics analysis of sensitive and tolerant barley genotypes under drought stress. Amino Acids 44, 345359. Kawamura, Y., Uemura, M., 2003. Mass spectrometric approach for identifying putative plasma membrane proteins of Arabidopsis leaves associated with cold acclimation. Plant J. 36, 141154. Ke, Y., Han, G., He, H., Li, J., 2009. Differential regulation of proteins and phosphor proteins in rice under drought stress. Biochem. Biophys. Res. Commun. 379, 133138. Khatoon, A., Rehman, S., Hiraga, S., Makino, T., Komatsu, S., 2012a. Organ-specific proteomics analysis for identification of response mechanism in soybean seedlings under flooding stress. J. Proteomics 75, 57065723. Khatoon, A., Rehman, S., Oh, M.W., Woo, S.H., Komatsu, S., 2012b. Analysis of response mechanism in soybean under low oxygen and flooding stresses using gel-base proteomics technique. Mol. Biol. Rep. 39, 1058110594. Kieffer, P., Dommes, J., Hoffmann, L., Hausman, J.F., Renaut, J., 2008. Quantitative changes in protein expression of cadmium-exposed poplar plants. Proteomics 8, 25142530. Kieffer, P., Sebastien, P., Oufir, M., Ziebel, J., Dommes, J., Hoffmann, L., et al., 2009. Combining proteomics and metabolite analyses to unravel cadmium stress-response in poplar leaves. J. Proteome Res. 8, 400417. Kim, S.G., Wang, Y., Lee, C.H., Mun, B.G., 2011. A comparative proteomics survey of proteins responsive to phosphorous starvation in roots of hydroponically-grown rice seedlings. J. Korean Soc. Appl. Biol. Chem. 54, 667677. Kjellsen, T.D., Shiryaeva, L., Schro¨der, W.P., Strimbeck, G.R., 2010. Proteomics of extreme freezing tolerance in Siberian Spruce (Picea obovata). J. Proteomics 73, 965975. Kochian, L.V., Hoeckenga, O.A., Pineros, M.A., 2004. How do crop plants tolerate acid soils? Mechanisms of aluminium to lerance and phosphorus efficiency. Annu. Rev. Plant Biol. 55, 459493. Komatsu, S., Hossain, Z., 2013. Organ-specific proteome analysis for identification of abiotic stress response mechanism in crop. Front. Plant Sci. 4, 19. Komatsu, S., Wada, T., Abelea, Y., Nouri, M.Z., Nanjo, Y., Nakayama, N., et al., 2009a. Analysis of plasma membrane proteome in soybean and application to flooding stress response. J. Proteome Res. 8, 44874499. Komatsu, S., Yamada, E., Furukawa, K., 2009b. Cold stress changes the concanavalin A-positive glycosylation pattern of proteins expressed in the basal parts of rice leaf sheaths. Amino Acids 36, 115123. Komatsu, S., Yamamoto, R., Nanjo, Y., Mikami, Y., Yunokawa, H., Sakata, K.A., 2009c. Comprehensive analysis of the soybean genes and proteins expressed under flooding stress using transcriptome and proteome techniques. J. Proteome Res. 8, 47664778. Komatsu, S., Sugimoto, T., Hoshino, T., Nanjo, Y., Furukawa, K., 2010a. Identification of flooding stress responsible cascades in root and hypocotyls of soybean using proteome analysis. Amino Acids 38, 729738. Komatsu, S., Kobayashi, Y., Nishizawa, K., Nanjo, Y., Furukawa, K., 2010b. Comparative proteomics analysis of differentially expressed proteins in soybean cell wall during flooding stress. Amino Acids 39, 14351449.

62


Komatsu, S., Yamamoto, A., Nakamura, T., Mohammad-Zaman, N., Nanjo, Y., Nishizawa, K., et al., 2011. Comprehensive analysis of mitochondria of roots and hypocotyls of soybean under flooding stress using proteomics and metabolomics techniques. J. Proteome Res. 10, 39934004. Komatsu, S., Kuji, R., Nanjo, Y., Hiraga, S., Furukawa, K., 2012a. Comprehensive analysis of endoplasmic reticulum enriched fraction in root tips of soybean under flooding stress using proteomics techniques. J. Proteomics 77, 531560. Komatsu, S., Hiraga, S., Yanagawa, Y., 2012b. Proteomics techniques for the development of flood tolerant crops. J. Proteome Res. 11, 6878. Komatsu, S., Nanjo, Y., Nishimura, M., 2013. Proteomic analysis of the flooding tolerance mechanism in mutant soybean. J. Proteomics 79, 231250. Kong, F.J., Oyanagi, A., Komatsu, S., 2010. Cell wall proteome of wheat roots under flooding stress using gelbased and LC MS/MS-based proteomics approaches. BBA-Protein Proteomics 1804, 124136. Kosakivska, I., Klymchuk, D., Negretzky, V., Bluma, D., Ustinova, A., 2008. Stress proteins and ultrastructural characteristics of leaf cells of plants with different types of ecological strategies. Genetic. Appl. Plant. Physiol. 34, 405418. Kosmala, A., Bocian, A., Rapacz, M., Jurczyk, B., Zwierzykowski, Z., 2009. Identification of leaf proteins differentially accumulated during cold acclimation between Festuca pratensis plants with distinct levels of frost tolerance. J. Exp. Bot. 60, 35953609. Kosova, K., Vitamvas, P., Prasil, I.T., Renaut, J., 2011. Plant proteome changes under abiotic stress—contribution of proteomics studies to understanding plant stress response. J. Proteomics 74, 13011322. Kosova, K., Prasil, I.T., Vitamvas, P., 2013. Protein contribution to plant salinity response and tolerance acquisition. Int. J. Mol. Sci. 14, 67576789. Kottapalli, K.R., Rakwal, R., Shibato, J., Burow, G., Tissue, D., Burke, J., et al., 2009. Physiology and proteomics of the water-deficit stress response in three contrasting peanut genotypes. Plant Cell Environ. 32, 380407. Koussevitzky, S., Suzuki, N., Huntington, S., Armijo, L., 2008. Ascorbate peroxidase 1 plays a key role in the response of Arabidopsis thaliana to stress combination. J. Biol. Chem. 283, 3419734203. Kundzewicz, Z., Ulbrich, U., Brucher, T., Graczyk, D., Kruger, A., Leckebusch, G.C., et al., 2005. Summer floods in central Europe—climate change track? Nat. Hazar. 36, 165189. Laganowsky, A., Gomez, S.M., Whitelegge, J.P., Nishio, J.N., 2009. Hydroponics on a chip: analysis of the Fe deficient Arabidopsis thylakoid membrane proteome. J. Proteomics 72, 397415. Lan, P., Li, W., Schmidt, W., 2012. Complementary proteome and transcriptome profiling in phosphate-deficient Arabidopsis roots reveals multiple levels of gene regulation. Mol. Cell Proteomics 11, 11561166. Lara, E., Moreira, D., Vereschaka, A., Lopez-Garcia, 2009. Panoceamic distribution of new diverse clades of deep sea diplonemids. Enviro. Microbiol. 11, 4755. Lee, D.G., Ahsan, N., Lee, S.H., Kang, K.Y., Lee, J.J., Lee, B.H., 2007. An approach to identify cold-induced low-abundant proteins in rice leaf. C R Biol. 330, 215225. Lee, D.G., Ahsan, N., Lee, S.H., Lee, J.J., Bahka, J.D., Kanga, K.Y., et al., 2009. Chilling stress-induced proteomic changes in rice roots. J. Plant Physiol. 166, 111. Lee, K., Bae, D.W., Kim, S.H., Han, H.J., Liu, X., Park, H.C., et al., 2010. Comparative proteomic analysis of the short-term responses of rice roots and leaves to cadmium. J. Plant Physiol. 167, 161168. Levitt, J., 1980. Responses of Plants to Environmental Stress. Chilling, Freezing and High Temperature Stresses. second ed. Academic Press, New York. Li, K., Xu, C., Zhang, K., Yang, A., Zhang, J., 2007. Proteomic analysis of roots growth and metabolic changes under phosphorus deficit in maize (Zea mays L.) plants. Proteomics 7, 15011512. Li, K., Xu, C., Li, Z., Zhang, K., 2008. Comparative proteome analyses of phosphorus responses in maize (Zea mays L.) roots of wild-type and a low-P-tolerant mutant reveal root characteristics associated with phosphorus efficiency. Plant J. 55, 927939.

References

63

Li, W., Zhang, C.Y., Lu, Q.T., Wen, X.G., Lu, C.M., 2011. The combined effect of salt stress and heat shock on proteome profiling in Suaeda salsa. J. Plant Physiol. 168, 17431752. Li, Y., Song, Y., Shi, G., Wang, J., Hou, X., 2009. Response of antioxidant activity to excess copper in two cultivars of Brassica campestris ssp. chinensis Makino. Acta. Physiol. Plant. 31, 155162. Liang, C., Tian, J., Liao, H., 2013. Proteomics dissection of plant responses to mineral nutrient deficiency. Proteomics 13, 624663. Lin, S.-K., Chang, M.-C., Tsai, Y.-G., Lur, H.-S., 2005. Proteomic analysis of the expression of proteins related to rice quality during caryopsis development and the effect of high temperature on expression. Proteomics 5, 21402156. Liu, F., Van Toai, T., Moy, L., Bock, G., Linford, L.D., Quackenbush, J., 2005. Global transcription profiling reveals novel insights into hypoxic response in Arabidopsis. Plant Physiol. 137, 11151129. Lobell, D.B., Field, C.B., 2007. Global scale climatecrop yield relationships and the impacts of recent warming. Env. Res. Lett. 2, 014002. Luque-Garcia, J.L., Cabezas-Sanchez, P., Camara, C., 2011. Proteomics as a tool for examining the toxicity of heavy metals. Trends Anal. Chem. 30, 703716. Ma, H., Song, L., Shu, Y., Wang, S., Niu, J., Wang, Z., et al., 2012. Comparative proteomic analysis of seedling leaves of different salt tolerant soybean genotypes. J. Proteomics. 75, 15291546. Majoul, T., Bancel, E., Triboi, E., Ben Hamida, J., Branlard, G., 2003. Proteomic analysis of the effect of heat stress on hexaploid wheat grain: characterization of heat-responsive proteins from total endosperm. Proteomics 3, 175183. Majoul, T., Bancel, E., Triboi, E., Ben Hamida, J., Branlard, G., 2004. Proteomic analysis of the effect of heat stress on hexaploid wheat grain: characterization of heat-responsive proteinsfrom non-prolamins fraction. Proteomics 4, 505513. Mamun, E.A., Alfred, S., Cantrill, L.C., Overall, R.L., Sutton, B.G., 2006. Effects of chilling on male gametophyte development in rice. Cell Biol. Int. 30, 583591. Marschner, H., 1995. Mineral Nutrition of Higher Plants. second ed. Academic Press, London. Meisrimler, C.N., Planchon, S., Renaut, J., Sergeant, K., Luthje, S., 2011. Alteration of plasma membranebound redox systems of iron deficient pea roots by chitosan. J. Proteomics 74, 14371449. Mengel, K., Kirkby, E.V., Kosegarten, H., Appel, I., 2001. Principles of Plant Nutrition. Kluwer Academic, Dordchet. Mirzaei, M., Soltani, N., Sarhadi, E., Pascovici, D., Keighley, T., Salekdeh, G.H., et al., 2012. Shotgun proteomic analysis of longdistance drought signaling in rice roots. J. Proteome. Res 1, 348358. Mohammadi, P.P., Moieni, A., Hiraga, S., Komatsu, S., 2012a. Proteomic analysis of drought-stressed soybean seedlings. J. Proteomics 16, 19061923. Mohammadi, P.P., Moieni, A., Komatsu, S., 2012b. Comparative proteome analysis of drought-sensitive and drought-tolerant rapeseed roots and their hybrid F1 line under drought stress. Amino Acids 43, 21372152. Moller, A.L., Pedas, P., Andersen, B., Svensson, B., 2011. Responses of barley root and shoot proteomes to long-term nitrogen deficiency, short-term nitrogen starvation and ammonium. Plant Cell Environ. 34, 20242037. Munns, R.A., 2005. Gene and salt tolerance: bringing them together. New Phytol. 167, 645663. Munns, R., Tester, M., 2008. Mechanisms of salinity tolerance. Ann. Rev. Plant Biol. 59, 651681. Muthurajan, R., Shobbar, Z.S., Jagadish, S.V., Bruskiewich, R., Ismail, A., Leung, H., et al., 2011. Physiological and proteomic responses of rice peduncles to drought stress. Mol. Biotechnol. 48, 173182. Nam, M.H., Huh, S.M., Kim, K.M., Park, W.J., Seo, J.B., Cho, K., et al., 2012. Comparative proteomic analysis of early salt stress-responsive proteins in roots of SnRK2 transgenic rice. Proteomic Sci. 10, 2544. Nanjo, Y., Skultety, L., Ashraf, Y., Komatsu, S., 2010. Comparative proteomic analysis of early-stage soybean seedlings responses to flooding by using gel and gel-free techniques. J. Prot. Res. 9, 39894002.

64


Nanjo, Y., Maruyama, K., Yasue, H., Yamaguchi-Shinozaki, K., Shinozaki, K., Komatsu, S., 2011a. Transcriptional responses to flooding stress in roots including hypocotyl of soybean seedlings. Plant Mol. Biol. 77, 129144. Nanjo, Y., Nouri, M.Z., Komatsu, S., 2011b. Quantitative proteomic analysis of crop seedlings subjected to stress conditions; a commentary. Phytochemistry 72, 12631272. Nanjo, Y., Skultety, L., Uvackova, L., Klubicova, K., Haiduch, M., Komatsu, S., 2012. Mass spectrometry-based analysis of proteomic changes in the root tips of flooded soybean seedlings. J. Proteome Res. 11, 372385. Neilson, K.A., Gamulla, C.G., Mirzaei, M., Imin, N., Haynes, P.A., 2010. Proteomic analysis of temperature stress in plants. Proteomics 10, 828845. Pandey, A., Chakraborty, S., Datta, A., Chakraborty, N., 2008. Proteomics approach to identify dehydration responsive nuclear proteins from chickpea (Cicer arietinum L.). Mol. Cell Proteomics 7, 88107. Pandey, A., Rajamani, U., Verma, J., Subba, P., Chakraborty, N., Datta, A., et al., 2010. Identification of extracellular matrix proteins of rice (Oryza sativa L.) involved in dehydration responsive network: a proteomic approach. J. Proteome Res. 9, 34433464. Parida, A.K., Das, A.B., 2005. Salt tolerance and salinity effects on plants: a review. Ecotoxicol. Environ. Saf. 60, 324349. Patterson, J., Ford, K., Cassin Natera, S., Bacic, A., 2007. Increased abundance of proteins involved in phytosiderophore production in boron-tolerant barley. Plant Physiol. 144, 16121631. Peng, S., Huang, J., Sheehy, J.E., Laza, R.C., Visperas, R.M., Zhong, X., 2004. Rice yields decline with higher night temperature from global warming. Proc. Natl. Acad. Sci. U.S.A. 101, 99719975. Peng, Z.Y., Wang, M.C., Li, F., Lv, H.J., Li, C.L., Xia, G.M., 2009. A proteomic study of the response to salinity and drought stress in an introgression strain of bread wheat. Mol. Cell Proteomics 8, 26762686. Plomion, C., Lalanne, C., Claverol, S., Meddour, H., Kohler, A., Bogeat-Triboulot, M.B., et al., 2006. Mapping the proteome of popular and application to the discovery of drought-stress responsive proteins. Proteomics 6, 65096527. Raman, S.V., Iniyan, S., Goic, R., 2012. A review of climate change, mitigation and adaptation. Renew. Sust. Energ. Rev. 16, 878897. Rasoulnia, A., Bihamta, M., Peyghambari, S., Alizadeh, H., Rahnama, A., 2011. Proteomic response of barley leaves to salinity. Mol. Biol. Rep. 38, 50555063. Rellan-Alvarez, R., Andaluz, S., Rodriguez-Celma, J., Wohlgemuth, G., 2010. Changes in the proteomic and metabolic profiles of Beta vulgaris root tips in response to iron deficiency and resupply. BMC Plant Biol. 10, 120134. Renaut, J., Lutts, S., Hoffmann, L., Hausman, J.F., 2004. Responses of poplar to chilling temperatures: proteomic and physiological aspects. Plant Biol. 6, 8190. Renaut, J., Hausman, J.F., Bassett, C., Artlip, T., Cauchie, H.M., Witters, E., et al., 2008. Quantitative proteomic analysis of short photoperiod and low-temperature responses in bark tissues of peach (Prunus persica L. Batsch). Tree Genet. Genom. 4, 589600. Rengasamy, P., 2006. World salinization with emphasis on Australia. J. Exp. Bot. 57, 10171023. Requejo, R., Tena, M., 2005. Proteome analysis of maize roots reveals that oxidative stress is a main contributing factor to plant arsenic toxicity. Phytochemistry 66, 15191528. Rodriguez-Celma, J., Rellan-Alvarez, R., Abadia, A., Abadia, J., Lopez-Millan, A.F., 2010. Changes induced by two levels of cadmium toxicity in the 2-DE protein profile of tomato roots. J. Proteomics 73, 16941706. Rollins, J.A., Habte, E., Templer, S.E., Colby, T., Schmidt, J., von Korff, M., 2013. Leaf proteome alternations in the context of physiological and morphological responses to drought and heat stress in barley (Hordeum vulgare L.). J. Exp. Bot. 64, 32013212. Roth, U., von Roepenack-Lahaye, E., Clemens, S., 2006. Proteome changes in Arabidopsis thaliana roots upon exposure to Cd21. J. Exp. Bot. 57, 40034013.

References

65

Ruan, C.J., Teixeira da Silva, J.A., Mopper, S., Qin, P., Lutts, S., 2010. Halophyte improvement for salinized world. CRC Crit. Rev. Plant Sci. 29, 329359. Saini, H.S., Aspinall, D., 1982. Abnormal sporogenesis in wheat (Triticum aestivum L.) induced by short periods of high temperature. Ann. Bot. 49, 835846. Salavati, A., Khatoon, A., Nanjo, Y., Komatsu, S., 2012. Analysis of proteomic changes in roots of soybean seedlings during recovery after flooding. J. Proteomics 75, 878893. Salekdeh, G.H., Siopongco, J., Wade, L.J., Ghareyazie, B., Bennett, J.A., 2002a. Proteomic approach to analyzing drought and salt responsiveness in rice. Field Crop Res. 76, 199219. Salekdeh, G.H., Siopongco, J., Wade, L.J., Ghareyazie, B., Bennett, J., 2002b. Proteomic analysis of rice leaves during drought stress and recovery. Proteomics 2, 11311145. Sarhadi, E., Bazargani, M.M., Sajise, A.G., Abdolahi, S., Vispo, N.A., Arceta, M., et al., 2012. Proteomic analysis of rice anthers under salt stress. Plant Physiol. Biochem. 58, 280287. Sarry, J.-E., Lauriane, K., Cée´ ine, D., Alexandra, L., Christophe, J., Véronique, H., et al., 2006. The early responses of Arabidopsis thaliana cells to cadmium exposure explored by protein and metabolite profiling analyses. Proteomics 6, 21802198. Savic, J., Dragicevic, I., Pantelic, D., Olsaca, J., Momeilovi, I., 2012. Expression of small heat shock proteins and heat tolerance in potato (Solanum tuberosum). Ann. Biol. Sci. 64, 135144. Schneider, T., Schellenberg, M., Meyer, S., Kelle, F., Gehrig, P., Riedel, K., et al., 2009. Quantitative detection of changes in the leaf-mesophyll tonoplast proteome independency of a cadmium exposure of barley (Hordeum vulgare L.) plants. Proteomics 9, 26682677. Semane, B., Dupae, J., Cuypers, A., Noben, J.P., Tuomainen, M., Tervahauta, A., et al., 2010. Leaf proteome responses of Arabidopsis thaliana exposed to mild cadmium stress. J. Plant Physiol. 167, 247254. Sergeant, K., Spiess, N., Renaut, J., Wilhelm, E., Hausman, J.F., 2011. One dry summer: a leaf proteome study on the response of oak to drought exposure. J. Proteomics 12, 13851395. Sha Valli Khan, P.S., Hoffman, L., Renaut, J., Housman, J.F., 2007. Current initiatives in proteomics for analysis of plant salt tolerance. Curr. Sci. 93, 807817. Shi, F., Yamamoto, R., Shimamura, S., Hiraga, S., Nakamura, T., Yukawa, M., et al., 2008. Ascorbate peroxidase, 2 (Apx, 2) involves in the response to submergence in soybean. Phytochemistry 69, 12951303. Shi, H., Ye, T., Chan, Z., 2013. Comparative proteomic and physiological analyses reveal the protective effect of exogenous polyamines in the Bermuda grass (Cynodon dactylon) response to salt and drought stresses. J. Proteome Res. 12, 49514964. Shi, S., Chen, W., Sun, W., 2011. Comparative proteomic analysis of the Arabidopsis cbl1mutant in response to salt stress. Proteomics 11, 47124725. Shu, L., Lou, Q., Ma, C., Ding, W., Zhou, J., Feng, F., et al., 2011. Genetic, proteomic and metabolic analysis of the regulation of energy storage in rice seedlings in response to drought. Proteomics 11, 41224138. Skylas, D.J., Cordwell, S.J., Hains, P.G., Larsen, M.R., et al., 2002. Heat shock of wheat during grain filling: proteins associated with heat tolerance. J. Cereal Sci. 35, 175188. Sobhanian, H., Aghaei, K., Komatsu, S., 2011. Changes in the plant proteome resulting from salt-stress: toward the creation of salt-tolerant crops? J. Proteomics 74, 13221327. Sobkowiak, R., Deckert, J., 2006. Proteins induced by cadmium in soybean cells. J. Plant Physiol. 163, 12031206. Song, C., Zeng, F., Feibo, W., Ma, W., Zhang, G., 2010. Proteomic analysis of nitrogen stress-responsive proteins in two rice cultivars differing in N utilization efficiency. J. Integr. Omics 1, 7887. Song, Y., Zhang, C., Ge, W., Zhang, Y., Burlingame, A.L., Guo, Y., 2011. Identification of NaCl stressresponsive apoplastic proteins in rice shoot stems by 2D-DIGE. J. Proteomics 74, 10451106. Subba, P., Barua, P., Kumar, R., Datta, A., Soni, K.K., Chakraborty, S., et al., 2013a. Phosphoproteomic dynamics of chickpea (Cicer arietinum L.) reveals shared and distinct components of dehydration response. J. Proteome Res. 12, 50255047.

66


Subba, P., Kumar, R., Gayali, S., Parveen, S., Pandey, A., Datta, A., et al., 2013b. Characterisation of the nuclear proteome of a dehydration-sensitive cultivar of chickpea and comparative proteomic analysis with a tolerant cultivar. Proteomics 13, 19731992. Sule, A., Vanrobaeys, F., Hajos, G., Van Beeumen, J., Devreese, B., 2004. Proteomic analysis of small heat shock protein isoforms in barley shoots. Phytochemistry 65, 18531863. Suzuki, N., Mittler, R., 2006. Reactive oxygen species and temperature stresses: a delicate balance between signalling and destruction. Physiol. Plant 126, 4551. Takeoka, Y., Hiroi, K., Kitano, H., Wada, T., 1991. Pistil hyper plasiain rice spikelets as affected by heat stress. Sex. Plant Reprod. 4, 3943. Taylor, N.L., Heazlewood, J.L., Day, D.A., Millar, A.H., 2005. Differential impact of environmental stresses on the pea mitochondrial proteome. Mol. Cell Proteom. 4, 122133. Tester, M., Langridge, P., 2010. Breeding technologies to increase crop production in a changing world. Science 327, 818822. Thakur, P., Kumara, S., Malika, J.A., Bergerb, J.D., Nayyar, H., 2010. Cold stress effects on reproductive development in grain crops: an overview. Environ. Exp. Bot. 67, 429443. Timperio, A.M., Egidi, M.G., Zolla, L., 2008. Proteomics applied on plant abiotic stresses: role of heat shock proteins (HSP). J. Proteomics 71, 391411. Toorchi, M., Yukawa, K., Nouri, M.Z., Komatsu, S., 2009. Proteomics approach for identifying osmotic-stressrelated proteins in soybean roots. Peptides 30, 21082117. Torabi, S., Wissuwa, M., Heidari, M., Naghavi, M.R., 2009. A comparative proteome approach to decipher the mechanism of rice adaptation to phosphorous deficiency. Proteomics 9, 159170. Tran, H.T., Plaxton, W.C., 2008. Proteomic analysis of alterations in the secretome of Arabidopsis thaliana suspension cells subjected to nutritional phosphate deficiency. Proteomics 8, 43174326. Valcu, C.M., Lalanne, C., Plomion, C., Schlink, K., 2008. Heat induced changes in protein expression profiles of Norway spruce (Picea abies) ecotypes from different elevations. Proteomics 8, 42874302. Valero-Galvan, J., Gonzalez-Fernandez, R., Navarro-Cerrillo, R.M., Gil-Pelegrin, E., Jorrin-Novo, J.V., 2013. Physiological and proteomic analyses of drought stress response in holm oak provenances. J. Proteome Res. 1, 51105123. Valliyodan, B., Nguyen, H.T., 2008. Genomics of abiotic stress in soybean. Plant Genet. Geno. Crops Models 2, 342373. Vanhove, A.C., Vermaelen, W., Panis, B., Swennen, R., Carpentier, S.C., 2012. Screening the banana biodiversity for drought tolerance: can an in vitro growth model and proteomics be used as a tool to discover tplerant varieties and understand homeostasis. Front. Plant Sci. 2, 176184. Villiers, F., Ducruix, C., Hugouvieux, V., Jarno, N., Ezan, E., Garin, J., et al., 2011. Investigating the plant response to cadmium exposure by proteomic and metabolomic approaches. Proteomics 11, 16501663. Vincent, D., Ergul, A., Bohlman, M.C., Tattersall, E.A., Tillett, R.L., Wheatley, M.D., et al., 2007. Proteomic analysis reveals differences between Vitis vinifera L. cv. Chardonnay and cv. Cabernet Sauvignon and their responses to water deficit and salinity. J. Exp. Bot. 58, 18731892. Viridi, A.S., Thakur, A., Dutt, S., Kumar, S., Singh, P., 2009. A sorghum 85 kDa heat stress modulated protein shows calmodulin-binding properties and cross reach to anti-Neurospora crassa Hrp 80 antibodies. FEBS Lett. 583, 767770. Vitamvas, P., Kosova, K., Prasil, I.T., 2007a. Proteome analysis in plant stress research. Czech. J. Genet. Plant Breed. 43, 16. Vitamvas, P., Saalbach, G., Prasil, I.T., Capkovs, V., Opatrna, J., Ahmed, J., 2007b. WCS120 protein family and proteins soluble upon boiling in cold-acclimated winter wheat. J. Plant Physiol. 164, 11971207. Wang, C., Zhang, L., Yuan, M., Ge, Y., Liu, Y., Fan, J., et al., 2010. The microfilament cytoskeleton plays a vital role in salt and osmotic stress tolerance in Arabidopsis. Plant Biol. 12, 7078.

References

67

Wang, W., Vinocur, B., Shoseyov, O., Altman, A., 2004. Role of plant heat-shock proteins and molecular chaperones in the abiotic stress response. Trends. Plant Sci 9, 244252. Wang, W.Q., Moller, I.M., Song, S.Q., 2012. Proteomic analysis of embryonic axis of Pisum sativum seeds during germination and identification of proteins associated with loss of desiccation tolerance. J. Proteomics 21, 6886. Wang, X.W., Vinocur, B., Altman, A., 2003. Plant responses to drought, salinity and extreme temperatures: towards genetic engineering for stress tolerance. Planta 21, 114. Wendelboe-Nelson, C., Morris, P.C., 2012. Proteins linked to drought tolerance revealed by DIGE analysis of drought resistant and susceptible barley varieties. Proteomics 12, 33743385. White, P.J., Brown, P.H., 2010. Plant nutrition for sustainable development and global health. Ann. Bot. 105, 10731080. Wilkins, M.R., Sanchez, J.C., Gooley, A.A., Appel, R.D., Humphery-Smith, I., Hochstrasser, D.F., et al., 1996. Progress with proteome projects: why all proteins expressed by a genome should be identified and how to do it. Biotech. Genet. Eng. Rev. 13, 1950. Witzel, K., Weidner, A., Surabhi, G.K., Varshney, R.K., Kunze, G., Buck-Sorlin, G.H., et al., 2010. Comparative analysis of the grain proteome fraction in barley genotypes with contrasting salinity tolerance during germination. Plant Cell Environ. 33, 211222. World Wide Fund for Nature. (WWF) 2008 Living Planet Report. World Wide Fund for Nature, Gland, Vaud, Switzerland. Xiao, X., Yang, F., Zhang, S., Korpelainen, H., Li, C., 2009. Physiological and proteomic responses of two contrasting Populus cathayana populations to drought stress. Physiol. Plant 136, 150168. Xu, C., Huang, B., 2008. Root proteomic responses to heat stress in two agrostis grass species contrasting in heat tolerance. J. Exp. Bot. 59, 41834194. Xu, C.P., Sibicky, T., Huang, B.R.I., 2010. Protein profile analysis of salt responsive proteins in leaves and roots in two cultivars of creeping bent grass differing in salinity tolerance. Plant Cell Rep. 29, 595615. Xu, G., Fan, X., Miller, A.J., 2012. Plant nitrogen assimilation and use efficiency. Ann. Rev. Plant Biol. 63, 153182. Xu, X.Y., Fan, R., Zheng, R., Li, C.H., Yu, D.Y., 2011. Proteomic analysis of seed germination under saltstress in soybeans. J. Zhejiang Univ. Sci. B 12, 507517. Yamaguchi, M., Valliyodan, B., Zhang, J., Lenoble, M.E., Yu, O., Rogers, E.E., et al., 2010. Regulation of growth response to water stress in the soybean primary root. I. Proteomic analysis reveals region-specific regulation of phenyl propanoid metabolism and control of free iron in the elongation zone. Plant Cell Environ. 33, 223243. Yan, S.P., Zhang, Q.Y., Tang, Z.C., Su, W.A., Sun, W.N., 2006. Comparative proteomic analysis provides new insights into chilling stress responses in rice. Mol. Cell Proteom. 5, 484496. Yanagawa, Y., Komatsu, S., 2012. Ubiquitin/proteasome-mediated proteolysis is involved in the response to flooding stress in soybean roots, independent of oxygen limitation. Plant Sci. 185186, 250258. Yang, F., Wang, Y., Miao, L.F., 2010. Comparative physiological and proteomic responses to drought stress in two poplar species originating from different altitudes. Physiol. Plant 139, 388400. Yang, F., Jorgensen, A.D., Li, H., Sondergaard, I., Finnie, C., Svensson, B., et al., 2011. Implications of hightemperature events and water deficits on protein profiles in wheat (Triticum aestivum L. cv. Vinjett) grain. Proteomics 11, 16841695. Yang, J.Y., Sun, Y., Sun, A.Q., Yi, S.Y., Qin, J., Li, M.H., et al., 2006. The involvement of chloroplast HSP100/ClpB in the acquired thermotolerance in tomato. Plant Mol. Biol. 62, 385395. Yang, Q., Wang, Y., Zhang, J., Shi, W., Qian, C., Peng, X., 2007. Identification of aluminum-responsive proteins in rice roots by a proteomic approach: cysteine synthase as a key player in Al response. Proteomics 7, 737749.

68


Yang, Q.S., Wu, J.H., Li, C.Y., Wei, Y.R., Sheng, O., Hu, C.H., et al., 2012a. Quantitative proteomic analysis reveals that antioxidation mechanisms contribute to cold tolerance in plantain (Musa paradisiaca L.; ABB Group) seedlings. Mol. Cell Proteom. 11, 18531869. Yang, Y., Wang, L., Tian, J., Sun, J., He, L., Gio, S., et al., 2012b. Proteomic study participating the enhancement of growth and salt tolerance of bottle gourd root stock-grafted watermelon seedlings. Plant Physiol. Biochem. 58, 5465. Yao, Y., Sun, H., Xu, F., Zhang, X., Liu, S., 2011. Comparative proteome analysis of metabolic changes by low phosphorus stress in two (Brassica napus) genotypes. Planta 233, 523537. Yoshimura, K., Masuda, A., Kuwano, M., Yokota, A., Akashi, K., 2008. Programmed proteome response for drought avoidance/tolerance in the root of ac3 xerophyte (wild watermelon) under water deficits. Plant Cell Physiol. 49, 226241. Yu, J.J., Chen, S.X., Zhao, Q., Wang, T., Yang, C.P., Diaz, C., et al., 2011. Physiological and proteomic analysis of salinity tolerance in Puccinellia tenuiflora. J. Proteome Res. 10, 38523870. Zadraznik, T., Hollung, K., Egge-Jacobsen, W., Meglic, V., Sustar-Vozlic, J., 2013. Differential proteomic analysis of drought stress response in leaves of common bean (Phaseolus vulgaris L.). J. Proteomics 14, 254272. Zhang, H., Lian, C., Shen, Z., 2009a. Proteomic identification of small, copper-responsive proteins in germinating embryos of Oryza sativa. Ann. Bot. 103, 923930. Zhang, L., Tian, L.H., Zhao, J.F., Song, Y., Zhang, C.J., Guo, Y., 2009b. Identification of an apoplastic protein involved in the initial phase of salt stress response in rice root by two-dimensional electrophoresis. Plant Physiol. 149, 916928. Zhang, M., Li, G., Huang, W., Bi, T., Chen, G., Tang, Z., et al., 2010a. Proteomic study of Carissa spinarum in response to combined heat and drought stress. Proteomics 10, 31173129. Zhang, S., Chen, F., Peng, S., Ma, W., Korpelainen, H., Li, C., 2010b. Comparative physiological, ultrastructural and proteomic analyses reveal sexual differences in the responses of Populus cathayana under drought stress. Proteomics 10, 661677. Zhang, S., Feng, L., Jiang, H., Ma, W., Korpelainen, H., Li, C., 2012. Biochemical and proteomic analyses reveal that (Populus cathayana) males and females have different metabolic activities under chilling stress. J. Proteome Res. 11, 58155826. Zhang, Y.T., Zhou, D.Q., Su, Y., Yu, P., Zhou, X.G., Yao, C.X., 2013. Proteome analysis of potato drought resistance variety in Ninglang leaves under drought stress. Yi. Chuan. 35, 666672. Zhao, Q., Zhang, H., Wang, T., Chen, S., Dai, S., 2013. Proteomics based investigation of salt responsive mechanisms in plant roots. J. Proteomics 82, 230253. Zhao, Y., Du, H., Wang, Z., Huang, B., 2011. Identification of proteins associated with waterdeficit tolerance in C4 perennial grass species, Cynodon dactylon x Cynodon transvaalensis and Cynodon dactylon. Physiol. Plant 141, 4055. Zhen, Y., Qi, J.L., Wang, S.S., Su, J., Xu, G.H., Zhang, M.S., et al., 2007. Comparative proteome analysis of differentially expressed proteins induced by Al toxicity in soybean. Physiol. Plant 131, 542554. Zhou, S.P., Sauvé, R.J., Liu, Z., Reddy, S.K., Bhatti, S., Hucko, S.D., et al., 2011. Identification of saltinduced changes in leaf and root proteomes of the wild tomato, Solanum chilense. J. Am. Soc. Hortic. Sci. 136, 288302. Zhu, L., Chen, S., Alvarez, S., Asirvatham, V.S., Schachtman, D.P., Wu, Y., et al., 2006. Cell wall proteome in the maize primary root elongation zone. I. Extraction and identification of water soluble and lightly ionically bound proteins. Plant Physiol. 140, 311325.

CHAPTER

Arbuscular Mycorrhiza in Crop Improvement under Environmental Stress

3

Mohammad Abass Ahanger, Abeer Hashem, Elsayed Fathi Abd-Allah and Parvaiz Ahmad

3.1 Introduction Physiological performance of plants depends on the rhizosphere characteristics. Plants continuously interact with the microorganisms present in the rhizosphere and can establish mutually beneficial associations with them (Raaijmakers et al., 2009; Lopez-Raez et al., 2011; Wu et al., 2011; Dickie et al., 2013). One of the important beneficial associations that is gaining much attention of researchers all over the world is the AMF association. AMF association involves plants and some soil fungi known as arbuscular mycorrhizal fungi (AMF). Interestingly, the majority of land plants, including most agricultural crop species, are able to establish arbuscular mycorrhizal (AM) symbiosis (Finlay, 2008; Parniske, 2008; Smith and Read, 2008; Brundrett, 2009; Helgason and Fitter, 2009). Besides benefiting the host plant in maintaining healthy growth under normal environmental conditions, the role of AMF in enhancing tolerance against various biotic and abiotic stresses has now been well established (Song, 2005; Ruiz-Lozano et al., 2008). Nevertheless, the negative impact of AM on the growth of host plants has also been reported, which has been reflected to an imbalance in nutrient (carbon) supplied by host plant and phosphorous benefit supplied by the associated fungi (Pozo and Azcoń-Aguilar, 2007). At least 1020% carbon of net primary productivity is allocated to associated mycorrhizal fungi (Leake et al., 2004; Hogberg and Read, 2006; Parniske, 2008; Helgason and Fitter, 2009) and in turn a majority of the nutrients are obtained via AMF (Leake et al., 2004). Nearly 80% of the plant families have been reported to form arbuscular mycorrhizal associations with fungi (Sieverding, 1990; Hamel et al., 1994; Daniell et al., 2001; Opik et al., 2006; Giovannetti, 2008). Fungi involved in such associations belong to the order Glomales, which includes five families—Glomaceae (single genus Glomus), Acaulosporaceae (includes genus Acaulospora and Entrophospora) and Gigasporaceae (includes genus Gigaspora and Scutellospora), and recently described Archaeosporaceae and Paraglomaceae (Smith and Read, 1997; Morton and Redecker, 2001; Smith and Read, 2008; Mohammadi, 2011). Broadly categorizing, there are two main types of mycorrhizal associations: (1) ectomycorrhiza and (2) endomycorrhiza; both have different structural as well as physiological bearings with the host plant (Brundrett, 2004). Mycorrhizal fungi colonize root hair cells and enhance root proliferation and their penetration in soil pores that are too small for root hairs to enter, thereby resulting in enhanced nutrient uptake (Lin et al., 1991; Mohammadi et al., 2011). P. Ahmad (Ed): Emerging Technologies and Management of Crop Stress Tolerance, Volume 2. DOI: http://dx.doi.org/10.1016/B978-0-12-800875-1.00003-X © 2014 Elsevier Inc. All rights reserved.

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CHAPTER 3 Arbuscular Mycorrhiza in Crop Improvement

Reports from fossil and molecular studies reveal that the occurrence of AMF in plants dates back almost 400 million years (Remy et al., 1994). During the course of evolution, the potential of host plants to discriminate between beneficial and harmful microorganisms remained preserved in the plants that evolved. The selective recognition and selection of fungal species for the establishment of associations is directed through molecular signaling pathways (Requena et al., 2007). Extensive hyphal production by AM colonization helps in resource exchange between host plant and associated fungi, thereby helping host plants to grow under relatively harsh conditions. AMF form special structures known as arbuscules within the root cortical cells (Smith and Read, 2008). Because of the formation of such intraradical structures, AM are sometimes called endomycorrhizas. Arbuscules are modified fungal hyphae that provide a large surface area for exchange of resources. Arbuscules and the associated storage vesicles located within or between the cells have long been accepted as the diagnostic for AM symbiosis. However, extraradical hyphae of AM fungi lack regular cross walls allowing materials, including nuclei, to flow relatively freely within the mycelium. Ectomycorrhizas are found in families of gymnosperms (e.g., Pinaceae) and angiosperms (e.g., Dipterocarpaceae, Betulaceae) and have a very important role in growth maintenance of many temperate and boreal forest trees. Ectomycorrhizal fungi form a sheath around the root called the mantle from which hyphae radiate outward into the substrate. Hyphae may also penetrate between the cells of the root to form a complex intercellular network system called the Hartig net. Ectomycorrhizal fungi do not penetrate intracellularly. Mycorrhizal symbioses alter both the physical and chemical characteristics of the rhizosphere (Cardon and Whitbeck, 2007). AMF association is involved in nutrient cycling, especially phosphorus and carbon. Glomalin, a proteinaceous compound, accumulation triggers nutrient cycling (Pirozynski and Malloch, 1975; Wright and Upadhyaya, 1998; Zhu and Miller, 2003; Lovelock et al., 2004) and also mediates the aggregation and stability of soil particles (Rillig, 2004). These mutual associations in rhizosphere determine plant health as well as soil fertility (Jeffries et al., 2003). Other related characteristics influenced by AMF include development of the plant community, plant yield (Wright et al., 2007), nutrient uptake (Finlay, 2008), and the relationship of water (Ruiz-Lozano et al., 2008). Moreover, AM fungi act as bioprotectants against pathogen attack and various stresses (van der Heijden et al., 1998; Barea et al., 2005; Ruiz-Lozano et al., 2008). For establishment of AM symbiosis, a very well directed and high degree of coordination between the two partners (plant and associated fungi) regulated through molecular dialogue is ubiquitous (Hause et al., 2007; Hause and Schaarschmidt, 2009). Mostly under nutrient-deficient conditions this communication leads to the establishment of association that starts in the rhizosphere with the production and exudation of signaling molecules by the host plants, which are recognized by AMF, thereby stimulating hyphal growth. Among these signals, the strigolactones have been considered as important cues for the initiation and establishment of the association (Bouwmeester et al., 2007; Parker, 2009; Lopez-Raez et al., 2011; Kohlen et al., 2012). For initiation of association, plants produce a signal earlier than the fungal associate. Fungal responses involve a diffuse signal allowing a plant to detect aspresorium and induction of gene expression (Gianinazzi-Pearson et al., 1996). Among various signaling molecules favoring the formation of association, flavonoids have been proposed as the active molecule (Phillips and Tsai, 1992); however, it must be noted here that they are not ubiquitous for such interactions (Becard et al., 1995). At the plant level, strigolactones have been recently identified as the initial signal to

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initiate formation of such associations. Strigolactones are a group of sesquiterpenes lactones (Steinkellner et al., 2007). Honiges and colleagues (2012), while studying the root exudates of Carduus, which infects Orobanche reticulata, found that strigolactones are active even if present in very low concentrations and the root exudates’ concentration has a direct influence on the different types of strigolactones.

3.2 Diversity of arbuscular mycorrhizal fungi Ecosystem functioning and stability is determined by existing plant biodiversity and species composition. Nevertheless, the precise ecological mechanisms contributing to regulation and maintainence of plant biodiversity and species composition are not well understood, but research is being carried out to unravel such mechanisms. Complete identification/understanding of these mechanisms would lead to, perhaps ensure, successful management for conservation and restoration of diverse natural ecosystems. Belowground arbuscular mycorrhizal fungi diversity is one of the major factors contributing to the maintenance of plant biodiversity and ecosystem functioning. Low AMF diversity and/or any change in AMF considerably affect the plant species composition, nutrient capture, productivity, and overall structure of microcosms and vice versa (Heijden et al., 1998). For the efficient utilization of AMF in conservation of environment and sustainable plant production, thorough knowledge about the conservation strategies of symbiotic arbuscular mycorrhizal fungi is of immense importance. Poor responses of AMF to pure culture, or insufficient information about their reproductive biology, clearly indicate that the understanding about the variations in population biology, ecological specificity, and symbiotic activity is still incomplete at the gene level. In short, a multidisciplinary approach is needed so that any significant difference between populations and species can be located (Giovannetti and Gianinazzi-Pearson, 1994). It is plant productivity rather than plant species richness that is believed to determine the abundance of microbes in the soil; however, plant species richness has a direct bearing on AMF abundance. Improvement in plant nutrition and health due to AMF varies markedly with the species of arbuscular mycorrhizal fungi involved; for example, in the Glomus species a large diversity has been reported for mycelium growth and phosphorus uptake, indicating that a large functional heterogeneity exists among various AMF communities (Munkvold et al., 2004). However, due to a lack of proper knowledge about the functional diversity, it is impossible to correlate the diversity of an AMF community to its functional properties. Several biotic as well as abiotic factors have a key role in controlling the diversity of AMF, the aboveground plant community itself being the one prominent factor. Plant community has an obvious affect through the specificity/preference exhibited by either partner in the mycorrhizal symbiosis. Richer plant communities have been reported to support production, richness, and germination of AMF spores (Burrows and Pfleger, 2002). Moreover, plant assemblage has a highly significant impact on the genetic diversity of AMF, as has been revealed by Johnson et al. (2003) while studying the DNA of AMF. The impact of the host specificity of AMF and plant species richness on AMF diversity in natural ecosystems, using both spore-related characteristics (production, richness, and germination) (Eom et al., 2000) and fungal DNA (Husband et al., 2002; Vandenkoornhuyse et al., 2002), is well documented.

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Plant productivity also has an influence on the diversity of AMF. Fungal colonization increases with an increase in host productivity (Zak et al., 2003). However, increased plant productivity is intrinsically linked with plant diversity (Tilman et al., 1996). This discrimination between the influences of host plant diversity and productivity on mycorrhizal fungi is a challenge to modern plant scientists. Moreover, the effect of various edaphic factors in the control of mycorrhizal fungal communities is also well documented (Hansen, 1988; Bruns, 1995; Colpaert and van Tichelen, 1996; Kernaghan and Harper, 2001; Erland and Taylor, 2002). AMF utilize the organic forms of available soil nutrients more efficiently (Read et al., 2004). The quality, quantity, as well as the heterogeneity of soil organic matter, significantly influence the growth and diversity of the AMF community as has been reported in studies of pine and oak (Ruhling and Tyler, 1990; Conn and Dighton, 2000). In addition to this, leaf litter extracts also influence AM fungal growth (Baar et al., 1994; Conn and Dighton, 2000). Johnson et al. (1992), while making an assessment on the impact of various edaphic factors on AMF colonization using different combinations of soil types and host species, have found that distribution of some AMF species is dependent on particular soil type, on particular host, or on particular plantsoil combinations. Thus, soil characteristics, such as organic matter content, pH, nutrient status, and phenolic content, have their contribution in controlling the diversity of AMF (Hobbie, 1992; Wardle, 2002). In addition to the preceding factors, interaction with soil organisms other than AMF also influence AM fungal diversity. Several bacteria improve root colonization by AMF (Garbaye, 1994), while saprophytic fungi try to weaken the association because of the competitive nature (Shaw et al., 1995), and attack to host plant from herbivores (Gehring and Whitham, 2002) usually leads to reduction in colonization. Many anthropogenic threats (e.g., forest fire, according to Dahlberg, 2002) also tend to decrease diversity and/or change the species composition of AM fungi (Erland and Taylor, 2002). Other factors influencing AMF indirectly through their impact on the plant community’s structure include microclimate, topography, acid rain (Roth and Fahey, 1998), and tillage (Jansa et al., 2003). Several plant root exudates including carbohydrates, amino acids, and secondary metabolites (e.g., phenols, terpenoids, flavonoids) are accumulated in the rhizospheric area and are used as a source of energy by the microorganisms living in the close vicinity of the root (Koske and Gemma, 1992). However, some of the low-molecular-weight compounds influence microbe growth (Curl and Truelove, 1986). Root exudates of compatible host plants have been reported to influence both spore germination and hyphal growth in some species of AMF (Gianinazzi-Pearson et al., 1989). Nevertheless, the exact mechanisms involved in controlling host specificity still are not fully known. It is believed, however, that communication occurs through secondary metabolites (Anderson, 1988; Horan and Chilvers, 1990), which may include plant flavonoids (Vierheilig and Piche, 2002), fungal auxins (Podila, 2002), or oxylipins of fungi and the host plant as well (Christensen and Kolomiets, 2011). These are implicated in the complex signaling that exists between AMF and the host roots during the initiation of association.

3.3 Effect of arbuscular mycorrhizal fungi on soil fertility Because of the increasing cost of fertilizers and their subsequent negative environmental impacts, the search for microorganisms that can improve soil fertility and enhance plant nutrition is gaining pace and the attention of researchers. Symbiotic association with arbuscular mycorrhizal fungi is considered

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to be the primary determinant of plant health and soil fertility (Jeffries et al., 2003). Fungal hyphae that extend into the soil help plants to exploit soil minerals more efficiently and, further, to reduce the growth of other harmful fungi and nematode on roots to some extent (Smith and Read, 2007). Arbuscular mycorrhizal fungi are very crucial for ecosystem functioning and contribute to the formation of soil aggregates through the exudations (e.g., glomalin) by their extraradical hyphae. Exogenous application of phosphorous fertilizer enhances population size, species richness, diversity of AMF, as well as the contents of glomalin-related soil protein (GRSP) and soil organic carbon. This suggests the key role of phosphorus in the maintainence of soil fertility as well as the diversity of AMF (Curaqueo et al., 2011; Dai et al., 2013). However, various factors (e.g., community structure, population size, external mycelium length, and GRSP content) directly or indirectly contribute to the soil AMF properties, thereby providing help in gaining information immediately and accurately about any kind of change in soil fertility status (Bedini et al., 2007; Alguacil et al., 2010; Ngosong et al., 2010). Sustainable growth and development of plants depends on soil health to a great extent. Agricultural malpractices and increasing degradation of soils through various anthropogenic threats has resulted in progressive loss of soil fertility in arable/agricultural areas. Besides the physical and chemical properties of soil, diversity as well as biological activities of its existing biota has a direct bearing on soil quality (Doran and Linn, 1994). AMF is the essential representative of soil biota that exists in almost all ecological conditions, including the natural ecosystem and normal crop systems, that have species diversity. However, the contribution of AMF to soil fertility depends heavily on the understanding of the functional processes that are carried out by them and strategies that can contribute to enhance their activity in soil. AMF-infected plants use most of the available nutrients and moisture present in the soil. In exchange of the phosphorus the carbon obtained from the plants is delivered back to the soil via the extraradical hyphae, thereby contributing to the soil carbon pool. As a result of this, the activities of other soil biota having antagonistic activity against soil-borne pathogens are stimulated (Linderman, 2000), which therefore contributes to the maintenance of soil fertility/health. One of the well-documented roles of the AMF mycelium is the formation of soil aggregates (Andrade et al., 1998; Miller and Jastrow, 2000) in which glomalin deposition on the outer walls of extraradical mycelium and the adjacent soil particles acts as a strong adhesive/binding agent (Wright and Upadhyaya, 1999), resulting in the formation of a bag-like structure (usually meshlike) by the fungal hyphae together with the fibrous roots of the host plant. Smaller soil particles are entangled and enmeshed within this sticky bag resulting in the formation of macro soil aggregates that form the basic building blocks of soil structure (Miller and Jastrow, 2000). So, from this it can be suggested that AMF have a crucial role in restoration of spoiled/waste land and also in maintainence of agricultural soil structure—a more beneficial role. In addition to this, many biotic and abiotic interactions within the rhizosphere are mediated by AMF. Thus, from an agricultural point of view, AMF may be very useful for the soil where use of fertilizers, pesticides, or other chemical inputs can be reduced to levels that are sufficiently economical and do not pose any threat to soil fertility, the environment, and health as well (Bethlenfalvay and Linderman, 1992).

3.4 Arbuscular mycorrhizal fungi and environmental stresses in plants Stress tolerance of plants is a complex phenomenon involving changes at physiological, biochemical, and molecular levels. Reduction in growth and yield are undoubtedly the most important

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physiological responses of plants to adverse environmental conditions. AMF can be of immense use to overcome the deleterious effects of various environmental stresses (water and salinity) by increasing water and nutrient uptake from the soil. Completely understanding the mechanisms that enable a plant to withstand and grow under changing/unfavorable environmental conditions is important. Presently, most strategies being used to cope with stress induce changes so as to minimize crop losses. Such strategies include traditional breeding for developing stress-tolerant crop varieties and the use of genetic engineering for developing tolerant cultivars through the use of a definite set of markers (Sanan-Mishra et al., 2005; Cuartero et al., 2006). However, implementing the preceding approaches needs thorough knowledge and high financial investments. Therefore, to overcome losses in crop production due to environmental stresses, we need to find alternatives that are less expensive and more environmentally friendly. Thus, employing/exploiting biological methods for alleviating the negative impact of stresses is receiving the attention of researchers (Al-Karaki and Hammad, 2001; Giri and Mukerji, 2004; Miransari et al., 2007, 2008; Miransari and Smith, 2008). AM symbiosis has been reported to alter the physiology and metabolism of plants (Toussaint, 2007). AMF colonization induces early flowering and an increased number of flowers (Nowak, 2004; Gaur and Adholeya, 2005; Usha et al., 2005). Symbiotic relationships formed in association with arbuscular mycorrhizal fungi can improve plant growth and tolerance against various environmental stresses (Tang and Chen, 1999; Turnau and Haselwandter, 2002; Cho et al., 2006; Miransari, 2010; Smith et al., 2010). Greater tolerance of drought, salinity, heavy metals, and pests has been attributed to AMF symbiosis. Moreover, they have been reported to play a key role in improving nutrient uptake and the soilwater relationship as well (Smith and Read, 1997). A mechanism that induces enhanced stress tolerance for plants because of AMF association is possibly attributed to the following attributes: 1. Improvement in the rhizospheric soil properties 2. Enhanced/profuse development of a root system, resulting in increased root area and root plasticity, therefore improved water absorption (Echeverria et al., 2008) 3. Enhanced absorption of nutritional elements mostly phosphorus resulting in improved nutritional status of the host plant (Al-Karaki et al., 2001; Asghari et al., 2005; Asghari, 2008) 4. Quick activation of a defense system 5. Mitigation of oxidative damage by enhancing antioxidant enzyme activities (He et al., 2007) 6. Effects on the expression of genes (Song, 2005).

3.4.1 Arbuscular mycorrhizal fungi and water stress Arbuscular mycorrhizal fungi can help plants mitigate water stress-induced deleterious changes (Newsham et al., 1995; Ruiz-Lozano, 2003). Under water-stress conditions, the positive impact of AMF association has been studied, mostly at physiological levels such as regulation of water absorption, transpiration, and photosynthesis (Marschner and Dell, 1994; Auge, 2004). Under water-stress conditions, AMF association helps plants to maintain leaf water potential so that any drop in turgor is prevented (Dixon et al., 1994; Subramanian and Charest, 1995, 1997). Moreover, after stress release, AMF-infected plants recover quickly to normal conditions as compared to nonAMF plants (Subramanian and Charest, 1997). Stress recovery potential is similar to stress


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tolerance (Grzesiak et al., 2006; Oukarroum et al., 2007). AMF-associated plants show different transpiration rates and stomatal conductance compared to non-AMF plants (Marschner and Dell, 1994). Altered stomatal conductance and transpiration as a result of AMF has been reported in blue gram, cowpea, lettuce, soybean, and wheat. AMF enhances plant stomatal opening (Auge, 2001). Nevertheless, it should be noted here that the positive impact of AMF colonization on stomatal characteristics is genus dependent—for example, stomatal conductance of Citrus taxa and sorghum is not affected by AMF colonization. AMF association induces increased expression levels of certain genes directly contributing to increased drought tolerance (Ruiz-Lozano et al., 2006). These genes include P5CS and genes encoding for late embryogenesis abundant (LEA) proteins (Porcel et al., 2004, 2005). P5CS enzyme is involved in the biosynthesis of proline, having an important role in osmoregulation, while LEA proteins are involved in ion association, the antioxidative system, maintaining membrane integrity, protein stabilization, and folding (Tunnacliffe and Wise, 2007). In addition to this, the differential expression of gene coding for NCED has been reported in AM-infected plants (Schwartz et al., 2003; Maurel, 2007). Changes in expression levels have been postulated to be caused by the interaction of AMF with ABA (Ruiz-Lozano et al., 2006) and indeed all previously described genes are regulated by ABA (Strizhov et al., 1997; Aroca et al., 2006). Moreover, under drought conditions the abscisic acid (ABA) content of plants has been found to be regulated by the associated AMF (Goicoechea et al., 1997; Estrada-Luna and Davies, 2003). However, the effect of the exogenous application of ABA on the expression levels of these genes, and the physiology of AMF, has not been studied yet. In addition, studies pertaining to the differential expression of these genes by AMF have been worked out only at the root level, while it is widely accepted that AMF colonization alters both physiology and metabolism of aboveground plant parts (Toussaint, 2007).

3.4.2 Arbuscular mycorrhizal fungi and salinity stress Salinity is one of the common agricultural and biological problems. Most studies have shown that AM colonization increases plants’ tolerance to salinity (Evelin et al., 2009; Porcel et al., 2012) through alteration in hormonal profiles (Shekoofeh et al., 2012; Aroca et al., 2013). It has been reported that inoculation of Glomus mosseae and Glomus intraradices enhanced salt tolerance of green basil (Ocimum basilicum L.). Mycorrhizal inoculation caused decreased lipid peroxidation, sodium content while reduced sugars, free proline, protein, and potassium contents in aerial organs and roots were increased (Shekoofeh et al., 2012). Salinity hampers growth of plants as well as associated AMF and the colonizing capacity of AMF; it interferes with spore germination and fungal hyphal growth as well. Salinity-induced reduction in viability and AM-colonization capacity have been reported in Jatropha curcas L. (Kumar et al., 2010), tomato (Abdel-latef and Chaoxing, 2011), and Ocimum basilicum L. (Shekoofeh et al., 2012). Better growth performance of plants treated with AMF under salinity stress, in terms of stomatal conductance and efficiency of photosystem II, has been reported for lettuce (Aroca et al., 2013). Under various stress conditions, AMF colonizing of plants is having many beneficial effects on their growth (Smith and Read, 1997). In connection with NaCl stress, any alleviation of negative impacts on crop plants through AMF is of due interest because of the enormous potential and attributes of AMF (Aggarwal et al., 2012). As far as the existing literature pertaining to the interactions

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of higher salt concentrations and arbuscular mycorrhizal fungi colonization of plants, most reports are somewhat controversial. It has been noted that higher salt concentrations inhibit germination of spores/fungal propagules, prevent colonization of the plant roots, and therefore sporulation of AMF (Juniper and Abbott 1993; Smith and Read, 1997; Juniper and Abbott, 2006; Jahromi et al., 2008). However, on the other hand, plants (e.g., Aster tripolium) that grow well in salt marshes have been reported to have an intense colonization of AMF (Mason, 1928; Carvalho et al., 2001; Hildebrandt et al., 2001; Landwehr et al., 2002; Neto et al., 2006; Wilde et al., 2009). Amelioration of salinityinduced reduction in plant growth and yield, thus imparting increased salt tolerance through AMF in saline soils, is well documented (Hatimi, 1999; Tsang and Maun, 1999; Cantrell and Linderman, 2001; Al-Karaki et al., 2001). However, at molecular levels, the actual mechanisms leading to enhanced salt tolerance conferred by AMF remain to be unraveled (Aroca et al., 2013). Plants adopt different tolerance mechanisms that make direct or indirect contributions to salinity tolerance (Ahmad and Sharma, 2008; Rasool et al., 2013). These mechanisms include generation and accumulation of osmoprotectants (e.g., proline, glycine betaine, free sugars, polyols), meeting the increasing energy demands of ATPases for the quick export of Na1 and Cl2 ions from cytoplasm, specific transport proteins that can efficiently transfer exported ions into the vacuole or apoplastic spaces, and highly efficient aquaporins to maintain the osmobalance through sufficient water supply (Hasegawa et al., 2000). Among the few Na1/H1 antiporters that have been fully sequenced, most have been found to be homologs in the plasma membrane intrinsic protein (PIP) subgroup (Xia et al., 2002; Jang et al., 2004). Wu et al. (2010) reported that inoculation of arbuscular mycorrhizal fungi (Glomus mosseae and Paraglomus occultum) in Citrus tangerine under salinity stress significantly increased plant height, stem diameter, shoot, root and total plant biomass, photosynthetic rate, transpiration rate, stomatal conductance, and maintained ionic balance. However, the effect was more pronounced in Paraglomus occultum inoculated plants. Under normal conditions, AM also decreased leaf Na1 content with a concomitant increase in K1 and Mg21 content and the K1/Na1 ratio. Under both normal as well as salt-stress conditions, Qun et al. (2007) reported that inoculation of AMF (Glomus mosseae) to tomato plants reduced cell membrane osmosis and malonaldehyde content with a significant increase in activities of antioxidant enzymes, leading to better growth through efficient scavenging of reactive oxygen species (ROS) generated. In pigeon pea, AMF inoculation increased general morphological attributes, antioxidant enzyme activity, K uptake, Ca, and proline accumulation while decreasing Na uptake and accumulation, resulting in an increased K/Na and Ca/Na ratio (Garg and Manchanda, 2009). Increased plant growth, synthesis of osmolytes (e.g., proline), and increased resistance to salt stress through AMF symbiosis may be the result of increased phosphate and decreased Na uptake (Pfeiffer and Bloss, 1987; Giri and Mukerji, 2004). Amelioration of salt stress by AMF inoculation has been reported in cucumber (Rosendahl and Rosendahl, 1991), mung bean (Jindal et al., 1993), alfalfa (Azcoń and El-Atrash, 1997), tomato (Al-Karaki, 2000; Al-Karaki et al., 2001), maize (Feng et al., 2002), clover (Ben Khaled et al., 2003), and pigeon pea (Garg and Manchanda, 2009). Nevertheless, the exact mechanisms involved are yet to be fully unraveled (Ruiz-Lozano et al., 2012). Arbuscular mycorrhizal fungi are an important integral component of the natural ecosystem. As already noted, AMF have the potential to grow in saline environmental conditions where they improve plant tolerance to salinity (Juniper and Abbott, 1993, Aliasgharzadeh et al., 2001; Giri et al., 2003; Smith et al., 2009). Under saline environmental conditions, besides improving


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nutrition, AMF improves the water absorption capacity of plants by increasing root hydraulic conductivity and maintaining osmolarity (Auge, 2001), thus, help in ameliorating the adverse effects of excess salt accumulation in roots (Dixon et al., 1993).

3.4.3 Arbuscular mycorrhizal fungi and pathogen attack Plants are continuously attacked by a wide number of pathogens that cause a wide range of diseases resulting in plant growth retardation and, under serious infection, can lead to plant death. Infection by pathogens also reduces crop yield and therefore has a close and, of course, direct link to increasing the threat to the world’s food supply. Most commonly developed symptoms of pathogen attack include wilting of leaf and fruit, root and stem rot (Rekah et al., 1999), chlorosis, and necrosis, which have a direct bearing on the rate of photosynthesis (Kocal et al., 2008; Kim et al., 2010), resulting in yield loss; under severe infection this more often than not can lead to plant death (Berger et al., 2007). During pathogen attack, several plantpathogen interactions indigenous to the host plant are triggered. Changes induced usually include: development of physical barriers, modifications in cell wall, and de novo synthesis of metabolites (Ishihara et al., 2008). Biotrophic fungi are effective in preventing fungal penetration because of their ability to terminate the development and functioning of the parasitic fungal intracellular hypha (haustorium), thereby restricting it from extracting nutrition from plant cells (Wen et al., 2011). Control of plant pathogens through biological means to increase plant yield by suppressing or destroying them, thus enhancing plant resistance, is an important strategy attracting the interest of researchers worldwide. Microorganisms that are antagonistic to plant pathogens may be from the residing community or foreign to the existing community; nevertheless, there are threats from using microorganisms of foreign origin. Still, it is accepted that biological control has numerous benefits—for example, being a component of the environment, development of pesticide resistance is relatively safe, has a minor chance of being of any risk, and may have a role in enhancing sustainable agriculture. Arbuscular mycorrhizal fungi form one such group of organisms that can act as bioprotectors of plants (Newsham et al., 1995). Incompatible AMF association can lead to poor plant growth and reduction in yield, while compatible association enhances plant productivity (Ravnskov and Jakobsen, 1995), prevents pathogen growth (Caron, 1986), and up-regulates activity of plant hormones (Frankenberger and Arshad, 1995). AMF are credited with enhancing plant growth and yield; inducing local and systemic resistance against pathogens using a variety of mechanisms, including increased mineral nutrition; and the expression of plant genes resulting in enhanced resistance due to their antifungal effects (Graham et al., 1990; Al-Karaki et al., 2004). AMF help plants combate pathogen-induced attack by enhancing genetic, biochemical, and signaling factors responsible for their defense purpose (Khan et al., 2010). In connection with disease control, the specificity of AMF can never be neglected. There are many studies pertaining to this; for example, those that have been reported in eggplant, cucumber (Li et al., 1997), and banana (Jaizme-Vega et al., 1998). AMF-induced protection against various pathogenic fungi is well documented (Krishna and Bagyaraj, 1983; Boyetchko and Tewari, 1988; Duchesne et al., 1989; Garcia-Garrido and Ocampo, 1989; Guillemin et al., 1993; Azcoń-Aguilar and Barea, 1996; Pinochet et al., 1996; Kapoor et al., 1998; Kegler and Gottwald, 1998; Becker et al., 1999; Filion et al., 1999; Bodker et al., 2002; Kasiamdari et al., 2002). Some, however, have reported that AMF make no contribution to pathogen

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resistance (Wyss et al., 1991; Larsen and Bodker, 2001; Guillon et al., 2002). To reach a solid conclusion, extensive, practical, and regular use of AMF against plant pathogenic fungi is needed. More often, different AMF species or combinations of microorganisms are used to inhibit pathogen infection/growth. For example, inoculation of groundnut with Gigaspora margarita, Acaulospora laevis, and Sclerocystis dussii suppressed the deleterious effects of Sclerotium rolfsii (Kulkarni et al., 1997) and inoculating tobacco with a mixture of Glomus fasciculatum and Trichoderma harzianum controlled damping-off and black shank disease caused by Pythium aphanidermatum and Pythium parasitica, respectively (Sreeramulu et al., 1998). Sometimes microbial mixtures act synergistically with pesticides for effective control of plant diseases—that is, carbendazim and Glomus fasciculatum protected safflower from Macrophomina phaseolina, a root rot pathogen (Prashanthi et al., 1997). Moreover, there are a number of reports related to AMF-induced reduction of root rot disease in cereal crops (Grey et al., 1989; Thompson and Wildermuth, 1989; Rempel and Bernier, 1990). For elucidating the AMF-mediated disease control Phytophthora spp. and their interaction with crop plants have been considered as a model system by several researchers (Gullemin et al., 1994; Cordier et al., 1996; Pozo et al., 1996; Mark and Cassells, 1999; Norman and Hooker, 2000); AMF inoculation reduces the severity of the disease (Caron et al., 1985, 1986). Control of diseases by AMF under field conditions has not been thoroughly studied (Newsham et al., 1995; Bodker et al., 2002). Inoculation of grass (Vulpia ciliate var. ambigua) with Glomus sp. reduced Fusarium oxysporum growth (Newsham et al., 1995) and pretreatment of onion with Glomus sp. resulted in an increase in yield through control over white rot disease (Torres-Barragan et al., 1996). In fact, as per the reports, it seems that AMF has a tremendous potential to control and protect plants from any possible pathogenic attack and proper planning, as well as execution, is of course needed to properly address the problems of inconsistency.

3.4.4 AMF and herbicides and pesticides Disease control agriculturalists largely depend on the use of fungicides and insecticides and other chemical compounds that are toxic to plant invaders, causative, or carrier agents. However, it is obvious that the hazardous affects of these chemicals, or their degradation products, on the environment and human health strongly necessitates the search for new, harmless disease control alternatives. Therefore, indeed a natural/biological phenomenon/means that can enhance inherent as well acquired resistance to protect plants from disease is required. Depending on the chemical used for control of pests and herbs, several biosynthetic pathways are triggered. Elicitors are compounds that activate chemical defense in plants. Often tested chemical elicitors are salicylic acid, methyl salicylate, benzoic acid, chitosan, and others, which affect the activation of enzymes involved in secondary metabolite synthetic pathways, especially in phenolic compound production. Introduction of biological approaches into agricultural practices for control of pests and herbs could minimize the scope of chemical control, thus contributing to the development of sustainable agriculture (Thakur and Sohal, 2013). A variety of biotic stresses (e.g., fungal, bacterial, or pest infections) can lead to a great loss of yield. There are a number of options available to the farmers to protect their crops from diseases. Development of resistant cultivars, biological control, crop rotation, tillage, and chemical pesticides are the most important and open up options for an agriculturalist. Nearly all chemical pesticides or fungicides have a direct antibiotic principle; however, their use at a commercial level is not

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economical and excessive application is having a direct impact on the food chain—some are carcinogenic as well. Efforts are being made to frame environmentally friendly strategies so as to check plant diseases and save humankind from health hazards (El-Gamal et al., 2007). In connection with this, AMF can be of immense use as pointed out earlier while discussing the use of AMF against pathogen attack. However, it must be noted here that there are hardly any research reports pertaining to the use of AMF as a biological controller of pests and herbs; this is certainly an area of great concern and should be given due attention.

3.5 Ion transport in plants under stress and the role of arbuscular mycorrhizal fungi Among the proteins in salt-tolerant plants, Na1/H1 transporters and aquaporins are of immense importance. The Na1/H1 ion transporter helps plants maintain adequate ion concentration while aquaporins are involved in the movement of water. Stress tolerance is a complex trait and many factors may contribute to enhanced tolerance; for example, overproduction and accumulation of osmoprotectants (e.g., proline, glycine betaine, polyols) in the cytoplasm, specific transport proteins for the transfer/compartmentation of deleterious ions into the vacuole or into the apoplastic spaces, and sufficient water supply mediated by aquaporins (Hasegawa et al., 2000). Under salt stress, Northern analyses and in situ hybridization studies carried out on tomato showed that AMF does not significantly affect expression of Na1/H1 transporter genes. But transcript levels of the aquaporin gene (tonoplast as well as plasmalema) are reduced by salt stress and were enhanced by AMF both in leaves and roots, thereby maintaining well-regulated water flow (Ouziad et al., 2006). The Na1/H1 antiporter transfers Na1 out of the cytoplasm either into the vacuole or the apoplasm. Enhancement in compartmentation of Na1 into the vacuole through tonoplast Na1/H1 antiporters, and active extrusion of Na1 to the apoplast through Na1/H1 antiporters present at the plasma membrane level, are the two main strategies adapted by plants to avoid/ameliorate any possible toxicity of Na1 in the cytoplasm. Transgenic Arabidopsis overexpressing Na1/H1 antiporter have been reported to be more salt tolerant (Gaxiola et al., 1999; Sottosanto et al., 2004) than rice (Fukuda et al., 1999). Under stress conditions (water and salinity) due to the negative water potential, plants must maintain their osmotic balance, which otherwise leads to wilting, in the cytoplasm. The role of aquaporins in plants needs full and thorough study. However, a large content of water passes through the plasmalema or the tonoplast channels formed by aquaporins (Zeuthen, 2001; Hill et al., 2004). Expression/activity of aquaporins is definitely related to salt-stress tolerance (Johansson et al., 2000). Plants always prefer K1 over Na1. Salt-tolerant plants usually maintain a higher K1/Na1 ratio. Several types of transporters located at the plasma membrane include Na1/H1 antiporter, H1/Cl2 symporter and H1/K1 symporter, which are actively involved in maintenance of suitable and selective ion fluxes.

3.6 Arbuscular mycorrhizal fungi and mineral nutrition Balanced supplementation/application of fertilizers of macroelements (e.g., nitrogen, phosphorus and potassium) is important for better plant growth (Chu et al., 2007). Earlier it was believed that

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arbuscular mycorrhizal fungi lack the ability to use the soils’ organic nutrients, but recent studies suggest that AMF has the ability to access as well as enhance the uptake of organic forms of mineral nutrients. The role of AMF in increasing efficient utilization of available mineral nutrients under normal as well as stress conditions (e.g., drought, low temperature, salt stress) is well documented (Azcoń-Aguilar and Barea, 1997; Al-Karaki and Clark, 1998; Mena-Violante et al., 2006; Miransari, 2010). Moreover, AMF is believed to mediate selective uptake (Giri and Mukerji, 2004) and enhance transport of nutrients (Al-Karaki, 2000; Sharifi et al., 2007). AMF help plants take in nutrients (George, 2000; Hawkins et al., 2000; Hodge et al., 2001; Neumann and George, 2005; Wu et al., 2011; Hart and Forsythe, 2012). Most plants depend on mycorrhizal fungal symbionts for their nutrient uptake (Lambers et al., 2008). Nearly 10 to 20% carbon of net primary productivity is allocated to associated mycorrhizal fungi (Hobbie, 1992; Genre and Bonfante, 2010; Nasim, 2010) and plants in turn absorb a majority of their mineral nutrients (Leake et al., 2004; Khan et al., 2010).

3.6.1 Phosphorus Phosphorus is one of the important macronutrients required for plants’ vital functions including photosynthesis; protein synthesis; nitrogen fixation; formation of oil, sugars, starch; and so on (Awasthi et al., 2011). Extreme stress conditions (especially drought and salinity) lead to precipitation of important ions (e.g., phosphates) so that they are unavailable to plants, resulting in considerable reduction in absorption and transport of mineral nutrients (Azcoń-Aguilar et al., 1979). Therefore, solubilization of phosphates is essential so that they are available to plants, which may also contribute to mitigating stress (Cantrell and Linderman, 2001). Nearly 80% of plants’ required phosphorus is delivered by AMF hyphae. Extensive hyphal growth of the associated fungus allows plants to explore more soil volume, thereby mediating increased phosphorus uptake (Ruiz-Lozano and Azcoń, 2000). Under salt stress, AMF-inoculated Pistacia versa L. (Abbaspour et al., 2005), Acacia nilotica (Giri et al., 2007), and Trifolium alexandrium (Shokri and Maadi, 2009) showed more phosphorous content. An AMF-induced increase in phosphorous content has also been reported in tomato (Gamalero et al., 2004), Vicia faba (Jia et al., 2004), Cucumis sativus L. (Ortas, 2010), Plantago lanceolata L., and Allium porrum L. (Hart and Forsythe, 2012). This increased phosphorous nutrition in AMF-inoculated plants has a direct bearing on growth, antioxidant production, and nitrogen metabolism (Feng et al., 2002; Alguacil et al., 2003; Garg and Manchanda, 2008; Aziz et al., 2011). Improved uptake of phosphorus in AMF-inoculated plants helps them maintain vacuolar membrane integrity, which facilitates compartmentalization within the vacuole as well as selective ion uptake (Rinaldelli and Mancuso, 1996); this thereby prevents toxic ion-induced interference in metabolic pathways (Cantrell and Linderman, 2001).

3.6.2 Nitrogen Environmental stress adversely affects acquisition as well as efficient utilization of nitrogen by its affect on various nitrogen metabolism stages including nitrate uptake and reduction and protein synthesis (Aslam et al., 1984; Frechill et al., 2001). Inoculation of AMF can improve nitrogen metabolism in host plants under normal as well as stress conditions. An increase in nitrogen assimilation as a result of AMF has been reported in Sesbania grandiflora and Sesbania aegyptiaca (Giri and Mukerji, 2004), Vicia faba (Jia et al., 2004), Plantago lanceolata L., and Allium porrum L. (Hart and Forsythe, 2012).

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Enhanced uptake and accumulation of nitrogen in AMF-colonized plants is attributed to the increased uptake of inorganic nitrogen through the extraradical mycelia and its subsequent reduction via arbuscule localized nitrate reductase and the GS-GOGAT cycle, thereby resulting in the formation of various nitrogenous compounds (Kaldorf et al., 1998); these are then transported to the intraradical mycelia for further catabolism. The whole process is accompanied by enhanced expression of enzymes involved in nitrogen fixation and metabolism in the extraradical mycelia. However, the mode of transport of nitrogen from associated fungus to a host plant is still to be unraveled, but certain researchers have hypothesized the involvement of ammonium transporters (Govindarajulu et al., 2005). Enhanced uptake and metabolism of nitrogen in AMFinfected plants is attributed to the increased activity of nitrogen-metabolizing enzymes (Cliquet and Stewart, 1993). It is well documented that improved nitrogen metabolism reduces the ill effects of Na ions by reducing its uptake, which further protects chlorophyll degradation. However, it should be noted here that the actual mechanisms employed by AMF to improve nitrogen uptake under stress conditions remain unclear. Reynolds et al. (2005) reported that AMF do not enhance nitrogen uptake under nitrogen-deficient conditions in Salvia lyrata L., Plantago lanceolata L., Rumex acetosella L., Panicum sphaerocarpon, and Anthoxanthum odoratum L.

3.6.3 Potassium and K1/Na1 ratio Under salt-stress conditions, excessive uptake of Na1 results in a drastic decline in potassium uptake. This is because Na1 ions compete with K1 for binding sites essential for various cellular functions (Rus et al., 2001). Potassium has an important role in plant metabolism; it is involved in activation of enzymes, stomatal movements, and protein synthesis (Amtmann et al., 2008; Wang et al., 2013; Ahmad et al., 2014). These important functions cannot be met by Na1 ions. Higher salinity reduces the K/Na ratio, disturbs ionic balance of the cytoplasm, and ultimately affects physiological and biochemical processes (Giri et al., 2007; Luan et al., 2009). However, colonization of plants with AMF can reduce such a deleterious impact of the higher salt concentration. Under saline conditions, AMF can improve uptake of potassium and prevent Na uptake so as to maintain the K/Na ratio, thus leading to better stress adaptation (Grattan and Grieve, 1998; Alguacil et al., 2003; Rabie and Almadini, 2005; Giri et al., 2007; Sharifi et al., 2007; Zuccarini and Okurowska, 2008). AMF (Glomus estunicatum)-induced increase in potassium uptake under salinity stress has been reported in Pistacia versa L. (Abbaspour et al., 2005). In addition to this, potassium ion has a direct bearing with Na uptake; that is, it can prevent excessive uptake of Na to a considerable extent so that ionic balance can be maintained in the cytoplasm (Allen and Cunningham, 1983; Founoune et al., 2002; Giri et al., 2003; Colla et al., 2008; Umar et al., 2011). Maintainence of a high K/Na ratio prevents interference in various enzymatic processes regulated by potassium. A higher K/Na ratio is usually maintained through proper expression and regulation of the activities of potassium (K1) and sodium (Na1) ion transporters and hydrogen (H1) pumps (Parida and Das, 2005). Sodium ions are removed from cytoplasm and put into vacuoles by the Na1/H1 antiporter (Ouziad et al., 2006). High concentrations of K1 are required in protein synthesis because K1 is used in the binding of tRNA to the ribosomes (Blaha et al., 2000). AMF increased potassium uptake in Prunus persica L. (Wu et al., 2011), Plantago lanceolata L., and Allium porrum L. (Hart and Forsythe, 2012).

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3.6.4 Calcium Calcium acts as a second messenger and on exposure of plants to stress, Ca21 concentration is increased in order to mediate transduction of the stress signal. Mycorrhiza has been reported to alter calcium content in plants. An increase in uptake and accumulation of calcium due to AMF has been reported in lettuce (Cantrell and Linderman, 2001), banana (Yano-Melo et al., 2003), Prunus persica L. (Wu et al., 2011), Plantago lanceolata L., and Allium porrum L. (Hart and Forsythe, 2012). In addition to this, higher calcium favors colonization and sporulation of AMF (Jarstfer et al., 1998). Nevertheless, some reports point to the fact that mycorrhizal inoculation does not have any positive association with calcium uptake as has been in Acacia auriculiformis (Giri et al., 2003).

3.6.5 Magnesium Magnesium is another important mineral nutrient, which is the key component of photosynthetic compounds—the chlorophyll. Environmental stresses considerably affect the light-harvesting process and thus reduce photosynthesis. A mycorrhiza-induced increase in magnesium enhances chlorophyll content, suggesting the role of mycorrhizal fungi in increasing photosynthesis (Giri et al., 2003). Salinity-induced reduction in chlorophyll was less in mycorrhizal inoculated compared to nonmycorrhizal (Giri and Mukerji, 2004). Wu et al. (2011) reported an increase in magnesium content in Prunus persica L. inoculated with AMF (i.e., Glomus mosseae, Glomus versiforme, and Paraglomus occultum).

3.7 Conclusion and future prospects Environmental stresses (biotic as well as abiotic) result in great yield losses. Stress alters the physiological and biochemical processes resulting in altered metabolism and thus retards growth. Plants employ different strategies to cope with stress, including excess production and accumulation of compatible organic osmolytes, selective uptake of ions, increased expression and activity of antioxidant enzymes, and so on. Arbuscular mycorrhizal fungi form symbiotic associations with a majority of plants and such beneficial associations between plant roots and microbes are the sole interactions in determining both plant health and soil fertility. The associations help plants maintain growth and development processes such as nutrient uptake and protection against pathogens and stresses (van der Heijden et al., 1998). However, in order to exploit the potential of AMF to their maximum limit, it is important to adopt proper management practices and use less chemical fertilizer and pesticides. An agriculturalist needs to protect AMF to ensure smooth/normal ecosystem functioning such as maintaining plant biodiversity as well as productivity. Here questions arise about how to exploit the benefits of AMF for plant health. This depends heavily on the knowledge and understandings about the functional processes carried out by AMF, as well as the management practices to be implemented. Arbuscular mycorrhizal fungi can be very handy if we have to achieve a state where use/application of higher amounts of chemical fertilizers can be reduced to levels that do not pose any threat (environmental pollution and/or health risks). When making a transition from chemical to biological methods, such as utilization of AMF, agriculturalists really need to have a good knowledge about the interaction between crop plants and AMF.

References

83

References Abbaspour, H., Fallahyan, F., Fahimi, H., 2005. Effects of endomycorrhizal fungi and salt stress on nutrient acquisition and growth of Pistacia vera L. Pak. J. Bio. Sci. 8 (7), 10061010. Abdel Latef, A.A.H., Chaoxing, H., 2011. Effect of arbuscular mycorrhizal fungi on growth, mineral nutrition, antioxidant enzymes activity and fruit yield of tomato grown under salinity stress. Sci. Hortic. 127 (3), 228233. Aggarwal, A., Kadian, N., Karishma, N., Tanwar, A., Gupta, K.K., 2012. Arbuscular mycorrhizal symbiosis and alleviation of salinity stress. J. Appl. Nat. Sci. 4 (1), 144155. Ahmad, P., Sharma, S., 2008. Salt stress and phyto-biochemical responses of plants. Plant Soil Environ. 54 (3), 8999. Ahmad, P., Ashraf, M., Azooz, M.M., Rasool, S., Akram, N.A., 2014. Potassium starvation-induced oxidative stress and antioxidant defense responses in Brassica juncea. J. Plant Interact. 9 (1), 460467. Al-Karaki, G.N., 2000. Growth of mycorrhizal tomato and mineral acquisition under salt stress. Mycorrhiza 10, 5154. Al-Karaki, G.N., Clark, R.B., 1998. Growth, mineral acquisition and water use by mycorrhizal wheat grown under water stress. J. Plant Nutr. 21, 263276. Al-Karaki, G.N., Hammad, R., 2001. Mycorrhizal influence on fruit yield and mineral content of tomato grown under salt stress. J. Plant Nutr. 24, 13111323. Al-Karaki, G.N., Hammad, R., Rusan, M., 2001. Response of two tomato cultivars differing in salt tolerance to inoculation with mycorrhizal fungi under salt stress. Mycorrhiza 11, 4347. Al-Karaki, G.N., McMichael, B., Zak, J., 2004. Field response of wheat to arbuscular mycorrhizal fungi and drought stress. Mycorrhiza 14, 263269. Alguacil, M.M., Hernandez, J.A., Caravaca, F., Portillo, B., Roldan, A., 2003. Antioxidant enzyme activities in shoots from three mycorrhizal shrub species afforested in a degraded semi-arid soil. Physiol. Plant. 118, 562570. Alguacil, M.M., Lozano, Z., Campoy, M., Roldan, A., 2010. Phosphorus fertilization management modifies the biodiversity of AM fungi in a tropical savanna forage system. Soil Biol. Biochem. 42, 11141122. Aliasgharzadeh, N., Rastin, N.S., Towfighi, H., Alizadeh, A., 2001. Occurrence of arbuscular mycorrhizal fungi in saline soils of the Tabriz plain of Iran in relation to some physical and chemical properties of soil. Mycorrhiza 11, 119122. Allen, E.B., Cunningham, G.L., 1983. Effects of vesicular-arbuscular mycorrhizae on Distichlis spicata under three salinity levels. New Phytol. 93, 227236. Amtmann, A., Troufflard, S., Armengaud, P., 2008. The effect of potassium nutrition on pest and disease resistance in plants. Physiol. Plant. 133, 682691. Anderson, A.J., 1988. Mycorrhizae—host specificity and recognition. Phytopathology 78, 375378. Andrade, G., Mihara, K.L., Linderman, R.G., Bethlenfalvay, G.J., 1998. Soil aggregation status and rhizobacteria in the mycorrhizosphere. Plant Soil 202, 8996. Aroca, R., Ferrante, A., Vernieri, P., Chrispeels, M.J., 2006. Drought, abscisic acid and transpiration rate effects on the regulation of PIP aquaporin gene expression and abundance in Phaseolus vulgaris plants. Ann. Bot. 98, 13011310. Aroca, R., Ruiz-Lozano, J.M., Zamarre, A.M., Paz, J.A., Garcia-Mina, J.M., Pozo, J.M., et al., 2013. Arbuscular mycorrhizal symbiosis influences strigolactone production under salinity and alleviates salt stress in lettuce plants. J. Plant Physiol. 170, 4755. Asghari, H.R., 2008. Vesicular-arbuscular (VA) mycorrhizae improve salinity tolerance in pre-inoculation subterranean clover (Trifolium subterraneum) seedlings. Int. J. Plant Product 2, 243256. Asghari, H.R., Marschner, P., Smith, S.E., Smith, F.A., 2005. Growth response of Atriplex nummularia to inoculation with arbuscular mycorrhizal fungi at different salinity levels. Plant Soil 273, 245256.

84


Aslam, M., Huffaker, R.C., Rais, D.W., 1984. Early effects of salinity on nitrate assimilation in barley seedlings. Plant Physiol. 76, 321325. Auge, R.M., 2001. Water relations, drought and vesicular-arbuscular mycorrhizal symbiosis. Mycorrhiza 11, 342. Auge, R.M., 2004. Arbuscular mycorrhizae and soil/plant water relations. Can. J. Soil Sci. 84, 373381. Awasthi, R., Tewari, R., Nayyar, H., 2011. Synergy between plants and P solubilizing microbes in soils: effects on growth and physiology of crops. Int. Res. J. Microbiol. 2 (12), 484503. Azcoń, R., El-Atrash, F., 1997. Influence of arbuscular mycorrhizae and phosphorus fertilization on growth, nodulation and N2 (N-15) in Medicago sativa at four salinity levels. Biol. Fert. Soils 24, 8186. Azcoń-Aguilar, C., Barea, J.M., 1996. Arbuscular mycorrhizas and biological control of soil-borne plant pathogens: an overview of the mechanisms involved. Mycorrhiza 6, 457464. Azcoń-Aguilar, C., Barea, J.M., 1997. Applying mycorrhiza biotechnology to horticulture: significance and potentials. Sci. Hortic. 68, 124. Azcoń-Aguilar, C., Azcoń, R., Barea, J.M., 1979. Endomycorrhizal fungi and Rhizobium as biological fertilizers for Medicago sativa in normal cultivation. Nature 279, 325327. Aziz, I., Ayoob, M., Jite, P.K., 2011. Response of Solanum melongena L. to inoculation with arbuscular mycorrhizal fungi under low and high phosphate condition. Not. Sci. Biol. 3 (3), 7074. Baar, J., Ozinga, W.A., Sweers, I.L., Kuyper, T.W., 1994. Stimulatory and inhibitory effects of needle litter and grass extracts on the growth of some ectomycorrhizal fungi. Soil Biol. Biochem. 26, 10731079. Barea, J.M., Pozo, M.J., Azcoń, R., Azcoń-Aguilar, C., 2005. Microbial co-operation in the rhizosphere. J. Exp. Bot. 56, 17611778. Becard, G., Taylor, L.P., Douds, D.D., Pfeffer, P.E., Doner, L.W., 1995. Flavonoids are not necessary plant signal compounds in arbuscular mycorrhizal symbiosis. Mol. Plant Microbe Interact. 8, 252258. Becker, D.M., Bagley, S.T., Podila, G.K., 1999. Effects of mycorrhizal-associated streptomycetes on growth of Laccaria bicolor, Cenococcum geophilum, and Armillaria species and on gene expression in Laccaria bicolor. Mycologia 91, 3340. Bedini, S., Avio, L., Argese, E., Giovannetti, M., 2007. Effects of long-term land use on arbuscular mycorrhizal fungi and glomalin-related soil protein. Agric. Ecosyst. Environ. 120, 463466. Ben Khaled, L., Gomez, A.M., Ouarraqi, E.M., Oihabi, A., 2003. Physiological and biochemical responses to salt stress of mycorrhized and/or nodulated clover seedlings (Trifolium alexandrinum L.). Agronomie 23, 571580. Berger, S., Sinha, A.K., Roitsch, T., 2007. Plant physiology meets phytopathology: plant primary metabolism and plant-pathogen interactions. J. Exp. Bot. 58, 40194026. Bethlenfalvay, G.J., Linderman, R.G., 1992. Mycorrhizae in sustainable agriculture. (ASA Special publication no. 54), Agronomy Society of America, Madison, WI. pp. VIIIXIII. Blaha, G., Stelzl, U., Spahn, C.M.T., Agrawal, R.K., Frank, J., Nierhaus, K.H., 2000. Preparation of functional ribosomal complexes and effect of buffer conditions on tRNA positions observed by cryoelectron microscopy. Meth. Enzymol. 317, 292309. Bodker, L., Kjoller, R., Kristensen, K., Rosendahl, S., 2002. Interactions between indigenous arbuscular mycorrhizal fungi and Aphanomyces euteiches in field-grown pea. Mycorrhiza 12, 712. Bouwmeester, H.J., Roux, C., Lopez-Raez, J.A., Becard, G., 2007. Rhizosphere communication of plants, parasitic plants and AM fungi. Trends Plant. Sci. 12, 224230. Boyetchko, S.M., Tewari, J.P., 1988. The effect of VA mycorrhizal fungi on infection by Bipolaris sorokiniana in barley. Can J. Plant Pathol. 10, 361. Brundrett, M.C., 2004. Diversity and classification of mycorrhizal associations. Biol. Rev. 79, 473495. Brundrett, M.C., 2009. Mycorrhizal associations and other means of nutrition of vascular plants: understanding the global diversity of host plants by resolving conflicting information and developing reliable means of diagnosis. Plant Soil 320, 3777.

References

85

Bruns, T.D., 1995. Thoughts on the processes that maintain local species diversity of ectomycorrhizal fungi. Plant Soil 170, 6373. Burrows, R., Pfleger, F., 2002. Arbuscular mycorrhizal fungi respond to increasing plant diversity. Can. J. Bot. 80, 120130. Cantrell, I.C., Linderman, R.G., 2001. Preinoculation of lettuce and onion with VA mycorrhizal fungi reduces deleterious effects of soil salinity. Plant Soil 233, 269281. Cardon, Z.G., Whitbeck, J.L., 2007. The Rhizosphere. Elsevier/Academic, Boston, 235. Caron, M., Fortin, J.A., Richard, C., 1985. Influence of substrate on the interaction of Glomus intraradices and Fusarium oxysporum f. sp. radicis-lycopersici on tomatoes. Plant Soil 87, 233239. Caron, M., Fortin, J.A., Richard, C., 1986. Effect of Glomus intraradices on the infection by Fusarium oxysporum f. sp. radicis-lycopersici in tomatoes over a 12-week period. Can. J. Bot. 64, 552556. Carvalho, L.M., Caçador, I., Martins-Louçao, M.A., 2001. Temporal and spatial variation of arbuscular mycorrhizas in salt marsh plants of the Tagus estuary (Portugal). Mycorrhiza 11, 303309. Cho, K., Toler, H., Lee, J., Ownley, B., Stutz, J.C., Moore, J.L., et al., 2006. Mycorrhizal symbiosis and response of sorghum plants to combined drought and salinity stresses. J. Plant Physiol. 163, 517528. Christensen, S.A., Kolomiets, M.V., 2011. The lipid language of plant-fungal interactions. Fungal Gen. Biol. 48, 414. Chu, H.Y., Fujii, T., Morimoto, S., Lin, X.G., Yagi, K., Hu, J.L., et al., 2007. Soil microbial biomass, dehydrogenase activity, bacterial community structure in response to long-term fertilizer management. Soil Biol. Biochem. 39, 29712976. Cliquet, J.B., Stewart, G.R., 1993. Ammonia assimilation in Zea mays L. infected with a vesicular arbuscular mycorrhizal fungus Glomus fasciculatum. Plant Physiol. 101, 865871. Colla, G., Rouphael, Y., Cardarelli, M., Tullio, M., Rivera, C.M., Rea, E., 2008. Alleviation of salt stress by arbuscular mycorrhizal in zucchini plants grown at low and high phosphorus concentration. Biol. Fert. Soils 44, 501509. Colpaert, J.V., van Tichelen, K.K., 1996. Decomposition, nitrogen and phosphorus mineralization from beech leaf litter colonized by ectomycorrhizal or litter decomposing basidiomycetes. New Phytol. 134, 123132. Conn, C., Dighton, J., 2000. Litter quality influences on decomposition, ectomycorrhizal community structure and mycorrhizal root surface acid phosphatase activity. Soil Biol. Biochem. 32, 489496. Cordier, C., Gianinazzi, S., Gianinazzi-Pearson, V., 1996. Colonization patterns of root tissues by Phytophthora nicotianae var. parasitica related to reduced disease in mycorrhizal tomato. Plant Soil 185, 223232. Cuartero, J., Bolarin, M.C., Asins, M.J., Moreno, V., 2006. Increasing salt tolerance in the tomato. J. Exp. Bot. 57, 10451058. Curaqueo, G., Barea, J.M., Acevedo, E., Rubio, R., Cornejo, P., Borie, F., 2011. Effects of different tillage system on arbuscular mycorrhizal fungal propagules and physical properties in a Mediterranean agroecosystem in central Chile. Soil Tillage Res. 113, 1118. Curl, E.A., Truelove, B., 1986. The Rhizosphere. Springer, Experientia, 47:395399. Dahlberg, A., 2002. Effects of fire on ectomycorrhizal fungi in fennoscandian boreal forests. Silva Fennica 36, 6980. Dai, J., Hu, J., Lin, X., Yang, A., Wang, R., Zhang, J., et al., 2013. Arbuscular mycorrhizal fungal diversity, external mycelium length, and glomalin-related soil protein content in response to long-term fertilizer management. J. Soils Sedi. 13, 111. Daniell, T.J., Husband, R., Fitter, A.H., Young, J.P.W., 2001. Molecular diversity of arbuscular mycorrhizal fungi colonising arable crops. FEMS Microbiol. Ecol. 36, 203209. Dickie, I.A., Martinez-Garcia, L.B., Koele, N., Grelet, G.A., Tylianakis, J.M., Peltzer, D.A., et al., 2013. Mycorrhizas and mycorrhizal fungal communities throughout ecosystem development. Plant Soil 367, 1139.

86


Dixon, R.K., Garg, V.K., Rao, M.V., 1993. Inoculation of Leucaena and Prosopis seedlings with Glomus and Rhizobium species in saline soil: rhizosphere relations and seedling growth. Arid Soil Res. Rehabil. 7, 133144. Dixon, R.K., Rao, M.V., Garg, V.K., 1994. Water relations and gas exchange of mycorrhizal Leucaena leucocephala seedlings. J. Trop. For. Sci. 6, 542552. Doran, J.W., Linn, D.M., 1994. Microbial ecology of conservation management systems. In: Hatfield, J.L., Stewart, B.A. (Eds.), Soil Biology: Effects on Soil Quality—Advances in Soil Science. Lewis, Boca Raton, FL, pp. 127. Duchesne, L.C., Peterson, R.L., Ellis, B.E., 1989. The time-course of disease suppression and antibiosis by the ectomycorrhizal fungus Paxillus involutus. New Phytol. 111, 693698. Echeverria, M., Scambato, A.A., Sannazzaro, A.I., Maiale, S., Ruiz, O.A., Menendez, A.B., 2008. Phenotypic plasticity with respect to salt stress response by Lotus glaber: the role of its AM fungal and rhizobial symbionts. Mycorrhiza 18, 317329. El-Gamal, N.G., Abd-El-Kareem, F., Fotouh, Y.O., El Mougy, N.S., 2007. Induction of systemic resistance in potato plants against late and early blight diseases using chemical inducers under greenhouse and field conditions. Res. J. Agric. Bio. Sci. 3 (2), 7381. Eom, A., Hartnett, D.C., Wilson, G., 2000. Host plant species effects on arbuscular mycorrhizal fungal communities in tall grass prairie. Oecologia 122, 435444. Erland, S., Taylor, A.F.S., 2002. Diversity of ecto-mycorrhizal communities in relation to the abiotic environment. In: van der Heijden, M., Sanders, I. (Eds.), Mycorrhizal Ecology. Ecological Studies. Springer, Berlin, pp. 163200. Estrada-Luna, A.A., Davies, F.T., 2003. Arbuscular mycorrhizal fungi influence water relations, gas exchange, abscisic acid and growth of micropropagated chile ancho pepper (Capsicum annuum) plantlets during acclimatization and post-acclimatization. J. Plant Physiol. 160, 10731083. Evelin, H., Kapoor, R., Giri, B., 2009. Arbuscular mycorrhizal fungi in alleviation of salt stress: a review. Ann. Bot. 104, 12631280. Feng, G., Zhang, F.S., Li, X.L., Tian, C.Y., Tang, C., Rengel, Z., 2002. Improved tolerance of maize plants to salt stress by arbuscular mycorrhiza is related to higher accumulation of soluble sugars in roots. Mycorrhiza 12, 185190. Filion, M., St. Arnaud, M., Fortin, J.A., 1999. Direct interaction between the arbuscular mycorrhizal fungus Glomus intraradices and different rhizosphere microorganisms. New Phytol. 141, 525533. Finlay, R.D., 2008. Ecological aspects of mycorrhizal symbiosis: with special emphasis on the functional diversity of interactions involving the extraradical mycelium. J. Exp. Bot. 59, 11151126. Founoune, H., Duponnis, R., Ba, A.M., Ei Bouami, F., 2002. Influence of the dual arbuscular endomycorrhizal/ectomycorrhizal symbiosis on the growth of Acacia holosericea (A. Cunn. ex G. Don) in glasshouse conditions. Ann. For. Sci. 59, 9398. Frankenberger, W.T., Arshad, M., 1995. Microbial biosynthesis of auxins. In: Frankenberger, W.T., Arshad, M. (Eds.), Phytohormones in Soil. Marcel Dekker, New York, pp. 3571. Frechill, S., Lasa, B., Ibarretxe, L., Lamsfus, C., Aparicio Trejo, P., 2001. Pea response to saline stress is affected by the source of nitrogen nutrition (ammonium or nitrate). Plant Growth Regul. 35, 171179. Fukuda, A., Nakamura, A., Tanaka, Y., 1999. Molecular cloning and expression of the Na1/H1 exchanger gene in Oryza sativa. Biochim. Biophys. Acta 1446, 149155. Gamalero, E., Trotta, A., Massa, N., Copetta, A., Martinotti, M.G., Berta, G., 2004. Impact of two fluorescent pseudomonads and an arbuscular mycorrhizal fungus on tomato plant growth, root architecture and phosphorous acquisition. Mycorrhiza 14, 185192. Garbaye, J., 1994. Helper bacteria—a new dimension to the mycorrhizal symbiosis. New Phytol. 128, 197210. Garcia-Garrido, J.M., Ocampo, J.A., 1989. Effect of VA mycorrhizal infection of tomato on damage caused by Pseudomonas syringae. Soil Biol. Biochem. 21, 165167.

References

87

Garg, N., Manchanda, G., 2008. Effect of arbuscular mycorrhizal inoculation of salt-induced nodule senescence in Cajanus cajan. J. Plant Growth Regul. 27, 115124. Garg, N., Manchanda, G., 2009. Role of arbuscular mycorrhizae in the alleviation of ionic, osmotic and oxidative stresses induced by salinity in Cajanus cajan L. J. Agron. Crop. Sci. 195, 110123. Gaur, A., Adholeya, A., 2005. Diverse response of five ornamental plant species to mixed indigenous and single isolate arbuscular mycorrhizal inocula in marginal soil amended with organic matter. J. Plant Nutr. 28, 707723. Gaxiola, R.A., Rao, R., Sherman, A., Grisafi, P., Alper, S.L., Fink, G.R., 1999. The Arabidopsis thaliana proton transporters, AtNhx1 and Avp1, can function in cation detoxification in yeast. Proc. Natl. Acad. Sci. USA 96, 14801485. Gehring, C., Whitham, T., 2002. Mycorrhizae-herbivore interactions: population and community consequences. In: van der Heijden, M., Sanders, I. (Eds.), Mycorrhizal Ecology. Ecological Studies, 157. Springer, Berlin, pp. 295316. Genre, A., Bonfante, P., 2010. The making of symbiotic cells in arbuscular mycorrhizal roots. In: Koltai, H., Kapulnik, Y. (Eds.), Arbuscular Mycorrhizas: Physiology and Function. Springer-Verlag, Berlin/ Heidelberg, pp. 5771. George, E., 2000. Nutrient uptake. Contribution of arbuscular mycorrhizal fungi to plant mineral nutrition. In: Kapulnik, Y., Douds, D.D. (Eds.), Arbuscular Mycorrhizas: Physiology and Function. Kluwer, Dordrecht, pp. 307343. Gianinazzi-Pearson, V., Branzanti, B., Gianinazzi, S., 1989. In vitro enhancement of spore germination and early hyphal growth of a vesicular-arbuscular mycorrhizal fungus by host root exudates and plant flavonoids. Symbiosis 7, 243255. Gianinazzi-Pearson, V., Dumas-Gaudot, E., Gollotte, A., Tahiri-Alaoul, A., Gianinazzi, S., 1996. Cellular and molecular defence related root responses to invasion by arbuscular mycorrhizal fungi. New Phytol. 133, 4547. Giovannetti, M., 2008. Structure, extent and functional significance of belowground arbuscular mycorrhizal networks. In: Varma, A. (Ed.), Mycorrhiza: State of the Art, Genetics and Molecular Biology, EcoFunction, Biotechnology, Eco-Physiology, Structure and Systematics, third ed. Springer-Verlag, Berlin/ Heidelberg, pp. 5972. Giovannetti, M., Gianinazzi-Pearson, V., 1994. Biodiversity in arbuscular mycorrhizal fungi. Mycolog. Res. 98 (7), 705715. Giri, B., Mukerji, K.G., 2004. Mycorrhizal inoculant alleviates salt stress in Sesbania aegyptiaca and Sesbania grandiflora under field conditions: evidence for reduced sodium and improved magnesium uptake. Mycorrhiza 14, 307312. Giri, B., Kapoor, R., Mukerji, K.G., 2003. Influence of arbuscular mycorrhizal fungi and salinity on growth, biomass and mineral nutrition of Acacia auriculiformis. Biol. Ferti. Soils 38, 170175. Giri, B., Kapoor, R., Mukerji, K.G., 2007. Improved tolerance of Acacia nilotica to salt stress by arbuscular mycorrhiza, Glomus fasciculatum, may be partly related to elevated K1/Na1 ratios in root and shoot tissues. Microb. Ecol. 54, 753760. Goicoechea, N., Antolin, M.C., Sanchez-Diaz, M., 1997. Gas exchange is related to the hormone balance in mycorrhizal or nitrogen-fixing alfalfa subjected to drought. Physiol. Plant 100, 989997. Govindarajulu, M., Pfeffer, P.E., Jin, H.R., Abubaker, J., Douds, D.D., Allen, J.W., et al., 2005. Nitrogen transfer in the arbuscular mycorrhizal symbiosis. Nature 435, 819823. Graham, T.L., Kim, J.E., Graham, M.Y., 1990. Role of constitutive isoflavone conjugates in the accumulation of glyceollin in soybean infected with Phytophthora megasperma. Mol. Plant Microbiol. 3, 157166. Grattan, S.R., Grieve, C.M., 1998. Salinity-mineral nutrient relations in horticultural crops. Sci. Hortic. (Amsterdam) 78, 127157. Grey, W.E., van Leur, J.A.G., Kashour, G., El-Naimi, M., 1989. The interaction of vesicular-arbuscular mycorrhizae and common root rot (Cochliobolus sativus) in barley. Rachis 8, 1820.

88


Grzesiak, M.T., Grzesiak, S., Skoczowski, A., 2006. Changes of leaf water potential and gas exchange during and after drought in triticale and maize genotypes differing in drought tolerance. Photosynthetica 44, 561568. Guillemin, J.P., Abdel-Fattah, G.M., Trouvelot, A., Gianinazzi, S., Gianinazzi-Pearson, V., 1993. Interactions between soil-applied fungicides, endomycorrhiza fungal activity and plant growth. Trends Agric. Sci. 1, 161172. Guillon, C., St-Arnaud, M., Hamel, C., Jabaji-Hare, S.H., 2002. Differential and systemic alteration of defence-related gene transcript levels in mycorrhizal bean plants infected with Rhizoctonia solani. Can. J. Bot. 80, 305315. Gullemin, J.P., Gianinazzi, S., Gianinazzi-Pearson, V., Marchal, J., 1994. Control of arbuscular endomycorrhizae of Pratylenchus brachyurus in pineapple microplants. Agric. Sci. Fin. 3, 253262. Hamel, C., Dalpe, Y., Lapierre, C., Simard, R., Smith, D.L., 1994. Composition on the vesicular-arbuscular mycorrhizal fungi population in an old meadow as affected by pH phosphorus and soil disturbance. Agric. Ecosyst. Environ. 49, 223231. Hansen, P., 1988. Prediction of macrofungal occurrence in Swedish beech forests from soil and litter variable models. Vegetatio 78, 3144. Hart, M.M., Forsythe, J.A., 2012. Using arbuscular mycorrhizal fungi to improve the nutrient quality of crops; nutritional benefits in addition to phosphorus. Sci. Hortic. (Amsterdam) 148, 206214. Hasegawa, P.M., Bressan, R.A., Zhu, G.K., Bohnert, H.J., 2000. Plant cellular and molecular responses to height salinity. Physiol. Plant 51, 463499. Hatimi, A., 1999. Effect of salinity on the association between root symbionts and Acacia cyanophylla Lind. growth and nutrition. Plant Soil 216, 93101. Hause, B., Schaarschmidt, S., 2009. The role of jasmonates in mutualistic symbioses between plants and soilborn microorganisms. Phytochem. 70, 15891599. Hause, B., Mrosk, C., Isayenkov, S., Strack, D., 2007. Jasmonates in arbuscular mycorrhizal interactions. Phytochem. 68, 101110. Hawkins, H.J., Johansen, A., George, E., 2000. Uptake and transport of organic and inorganic nitrogen by arbuscular mycorrhizal fungi. Plant Soil 226, 275285. He, Z.Q., He, C.X., Zhang, Z.B., Zou, Z.R., Wang, H.S., 2007. Changes in antioxidative enzymes and cell membrane osmosis in tomato colonized by arbuscular mycorrhizae under NaCl stress. Colloids Surf. B: Biointerfaces 59, 128133. Heijden, M.G.A., Klironomos, J.N., Ursic, M., Moutoglis, P., Streitwolf-Engel, R., Boller, T., et al., 1998. Mycorrhizal fungal diversity determines plant biodiversity, ecosystem variability and productivity. Nature 396, 6972. Helgason, T., Fitter, A.H., 2009. Natural selection and the evolutionary ecology of the arbuscular mycorrhizal fungi. J. Exp. Bot. 60, 24652480. Hildebrandt, U., Janetta, K., Ouziad, F., Renne, B., Nawrath, K., Bothe, H., 2001. Arbuscular mycorrhizal colonization of halophytes in Central European salt marshes. Mycorrhiza 10, 175183. Hill, A.E., Shachar-Hill, B., Shachar-Hill, Y., 2004. What are aquaporins for. J. Membr. Biol. 197, 132. Hobbie, S.E., 1992. Effects of plant species on nutrient cycling. Trends Ecol. Evol. 7, 336339. Hodge, A., Campbell, C.D., Fitter, A.H., 2001. An arbuscular mycorrhizal fungus accelerates decomposition and acquires nitrogen directly from organic material. Nature 413, 297299. Hogberg, P., Read, D.J., 2006. Towards a more plant physiological perspective on soil ecology. Trend Ecol. Evol. 21, 548554. Honiges, A., Andelean, A., Xie, X., Yoneyama, K., Wegmann, K., 2012. Towards understanding Orobanche host specificity. Rom. Agri. Res. 29, 313322. Horan, D.P., Chilvers, G.A., 1990. Chemotropism—the key to ectomycorrhizal formation. New Phytol. 116, 297301.

References

89

Husband, R., Herre, E.A., Turner, S.L., Gallery, R., Young, J.P.W., 2002. Molecular diversity of arbuscular mycorrhizal fungi and patterns of host association over time and space in a tropical forest. Mol. Ecol. 11, 26692678. Ishihara, A., Hashimoto, Y., Miyagawa, H., Wakasa, K., 2008. Induction of serotonin accumulation by feeding of rice striped stem borer in rice leaves. Plant Signal Behav. 3, 714716. Jahromi, F., Aroca, R., Porcel, R., Ruiz-Lozano, J.M., 2008. Influence of salinity on the in vitro development of Glomus intraradices and on the in vivo physiological and molecular responses of mycorrhizal lettuce plants. Microbial. Ecol. 55, 4553. Jaizme-Vega, M.C., Sosa-Hernandez, B., Hernandez, J.M., Galan-Sauco, V., 1998. Interaction of arbuscular mycorrhizal fungi and the soil pathogen Fusarium oxysporum f. sp. cubense on the first stages of micropropagated Grande Naine banana. Acta Hortic. 490, 285295. Jang, J.Y., Kim, D.G., Kim, Y.O., Kim, J.S., Kang, H., 2004. An expression analysis of a gene family encoding plasma membrane aquaporins in response to abiotic stresses in Arabidopsis thaliana. Plant Mol. Biol. 54, 713725. Jansa, J., Mozafar, A., Kuhn, G., Anken, T., Ruh, R., Sanders, I.R., et al., 2003. Soil tillage affects the community structure of mycorrhizal fungi in maize roots. Ecol. Appl. 13, 11641176. Jarstfer, A.G., Farmer-Koppenol, P., Sylvia, D.M., 1998. Tissue magnesium and calcium affect mycorrhiza development and fungal reproduction. Mycorrhiza 7, 237242. Jeffries, P., Gianinazzi, S., Perotto, S., Turnau, K., Barea, J.-M., 2003. The contribution of arbuscular mycorrhizal fungi in sustainable maintenance of plant health and soil fertility. Biol. Fertil. Soils 37, 116. Jia, Y., Gray, V.M., Straker, C.J., 2004. The influence of Rhizobium and arbuscular mycorrhizal fungi on nitrogen and phosphorus accumulation by Vicia faba. Ann. Bot. 94, 251258. Jindal, V., Atwal, A., Sekhon, B.S., Rattan, S., Singh, R., 1993. Effect of vesicular-arbuscular mycorrhizae on metabolism of moong plants under NaCl salinity. Plant Physiol. Biochem. 31, 475481. Johansson, I., Karlsson, M., Johanson, U., Larsson, C., Kjellbom, P., 2000. The role of aquaporins in cellular and whole plant water balance. Biochem. Biophys. Acta 1465, 324342. Johnson, D., Vandenkoornhuyse, P.J., Leake, J.R., Gilbert, L., Booth, R.E., Grime, J.P., et al., 2003. Plant communities affect arbuscular mycorrhizal fungal diversity and community composition in grassland microcosms. New Phytol. 161, 503515. Johnson, N., Tilman, D., Wedin, D., 1992. Plant and soil controls on mycorrhizal fungal communities. Ecology 73, 20342042. Juniper, S., Abbott, L.K., 1993. Vesicular-arbuscular mycorrhizas and soil salinity. Mycorrhiza 4, 4547. Juniper, S., Abbott, L.K., 2006. Soil salinity delays germination and limits growth of hyphae from propagules of arbuscular mycorrhizal fungi. Mycorrhiza 16, 371379. Kaldorf, M., Schemelzer, E., Bothe, H., 1998. Expression of maize and fungal nitrate reductase in arbuscular mycorhiza. Mol. Plant Microbe Interact. 11, 439448. Kapoor, A.R., Mukherji, K.G., Kapoor, R., 1998. Microbial interactions in mycorrhizosphere of Anethum graveolens L. Phytomorphol. 48, 383389. Kasiamdari, R.S., Smith, S.E., Smith, F.A., Scott, E.S., 2002. Influence of the mycorrhizal fungus, Glomus coronatum, and soil phosphorus on infection and disease caused by binucleate Rhizoctonia and Rhizoctonia solani on mung bean (Vigna radiata). Plant Soil 238, 235244. Kegler, H., Gottwald, J., 1998. Influence of mycorrhizas on the growth and resistance of asparagus. Arch. Phytopathol. Plant Protect. 31, 435438. Kernaghan, G., Harper, K.A., 2001. Community structure of ectomycorrhizal fungi across an alpine/subalpine ecotone. Ecography 24, 181188. Khan, M.H., Meghvansi, M.K., Panwar, V., Gogoi, H.K., Singh, L., 2010. Arbuscular mycorrhizal fungiinduced signalling in plant defence against phytopathogens. J. Phytol. 2 (7), 5369.

90


Kim, Y.M., Bouras, N., Kav, N.N., Strelkov, S.E., 2010. Inhibition of photosynthesis and modification of the wheat leaf proteome by Ptr ToxB: a host-specific toxin from the fungal pathogen Pyrenophora triticirepentis. Proteomics 10L, 29112926. Kocal, N., Sonnewald, U., Sonnewald, S., 2008. Cell wall-bound invertase limits sucrose export and is involved in symptom development and inhibition of photosynthesis during compatible interaction between tomato and Xanthomonas campestris pv vesicatoria. Plant Physiol. 148, 15231536. Kohlen, W., Charnikhova, T., Lammers, M., Pollina, T., Toth, P., Haider, I., et al., 2012. The tomato carotenoid cleavage dioxygenase 8 (SlCCD8) regulates rhizosphere signaling, plant architecture and affects reproductive development through strigolactone biosynthesis. New Phytol. 196, 535547. Koske, R.E., Gemma, J.N., 1992. Fungal reactions to plants prior to mycorrhizal formation. In: Allen, M.F. (Ed.), Mycorrhizal Functioning: An Integrated Plant—Fungal Process. Chapman and Hall, New York, pp. 336. Krishna, K.R., Bagyaraj, D.J., 1983. Interaction between Glomus fasciculatum and Sclerotium rolfsii in peanut. Can. J. Bot. 61, 23492351. Kulkarni, S.A., Kulkarni, S., Sreenivas, M.N., Kulkarni, S., 1997. Interaction between vesiculararbuscular (VA) mycorrhizae and Sclerotium rolfsii Sacc. in groundnut. Karnataka J. Agric. Sci. 10, 919921. Kumar, A., Sharma, S., Saroj, M., 2010. Influence of arbuscular mycorrhizal (AM) fungi and salinity on seedling growth, solute accumulation and mycorrhizal dependency of Jatropha curcas L. J. Plant Growth Regul. 29 (3), 297306. Lambers, H., Raven, J.A., Shaver, G.R., Smith, S.E., 2008. Plant nutrient-acquisition strategies change with soil age. Trends Ecol. Evol. 23, 95103. Landwehr, M., Hildebrandt, U., Wilde, P., Nawrath, K., Toth, T., Biro, B., et al., 2002. The arbuscular mycorrhizal fungus Glomus geosporum in European saline, sodic and gypsum soils. Mycorrhiza 12, 199211. Larsen, J., Bodker, L., 2001. Interactions between pea root inhabiting fungi examined using signature fatty acids. New Phytol. 149, 487493. Leake, J.R., Johnson, D., Donnelly, D.P., Muckle, G.E., Boddy, L., Read, D.J., 2004. Networks of power and influence: the role of mycorrhizal mycelium in controlling plant communities and agroecosystem functioning. Can. J. Bot. 82, 10161045. Li, S.L., Zhao, S.J., Zhao, L.Z., 1997. Effects of VA mycorrhizae on the growth of eggplant and cucumber and control of diseases. Acta Phytophylac. Sin. 24, 117120. Lin, X., George, E., Marschner, H., 1991. Extension of the phosphorus depletion zone in VA-mycorrhizal white clover in a calcareous soil. Plant Soil 136, 4148. Linderman, R.G., 2000. Effects of mycorrhizas on plant tolerance to diseases. In: Kapulnik, Y., Douds Jr, D.D. (Eds.), Arbuscular Mycorrhizas: Physiology and Function. Kluwer Academic, pp. 345365. Lopez-Raez, J.A., Pozo, M.J., Garcia-Garrido, J.M., 2011. Strigolactones: a cry for help in the rhizosphere. Botany 89, 513522. Lovelock, C.E., Wright, S.F., Clark, D.A., Ruess, R.W., 2004. Soil stocks of glomalin produced by arbuscular mycorrhizal fungi across a tropical rain forest landscape. J. Ecol. 92, 278287. Luan, S., Lan, W., Lee, S.C., 2009. Potassium nutrition, sodium toxicity, and calcium signaling: connections through the CBLCIPK network. Curr. Opin. Plant Biol. 12, 339346. Mark, G.L., Cassells, A.C., 1999. The effect of dazomet and fosetyl-aluminium on indigenous and introduced arbuscular mycorrhizal fungi in commercial strawberry production. Plant Soil 209, 253261. Marschner, H., Dell, B., 1994. Nutrient uptake in mycorrhizal symbiosis. Plant Soil 159, 89102. Mason, E., 1928. Note on the presence of mycorrhizae in the roots of salt marsh plants. New Phytol. 27, 193195. Maurel, C., 2007. Plant aquaporins: novel functions and regulation properties. FEBS Lett. 581, 22272236.

References

91

Mena-Violante, H.G., Ocampo-Jimenez, O., Dendooven, L., Martinez-Soto, G., Gonzalez-Castaneda, J., Davies, F.T., et al., 2006. Arbuscular mycorrhizal fungi enhanced fruit growth and quality of chile ancho (Capsicum annuum L. cv San Luis) plants exposed to drought. Mycorrhiza 16, 261267. Miller, R.M., Jastrow, J.D., 2000. Mycorrhizal fungi influence soil structure. In: Kapulnik, Y., Douds, D.D. (Eds.), Arbuscular Mycorrhizas: Physiology and Function. Kluwer Academic, pp. 318. Miransari, M., 2010. Contribution of arbuscular mycorrhizal symbiosis to plant growth under different types of soil stress. Plant Biol. 12, 563569. Miransari, M., Smith, D.L., 2008. Using signal molecule genistein to alleviate the stress of sub optimal root zone temperature on soybeanBradyrhizobium symbiosis under different soil textures. J. Plant Interact. 3, 287295. Miransari, M., Bahrami, H.A., Rejali, F., Malakouti, M.J., Torabi, H., 2007. Using arbuscular mycorrhiza to reduce the stressful effects of soil compaction on corn (Zea mays L.) growth. Soil Biol. Biochem. 39, 20142026. Miransari, M., Bahrami, H.A., Rejali, F., Malakouti, M.J., 2008. Using arbuscular mycorrhiza to reduce the stressful effects of soil compaction on wheat (Triticumaestivum L.) growth. Soil Biol. Biochem. 40, 11971206. Mohammadi, K., 2011. Soil, Plant and Microbe Interactions. Lambert Academic Publishing Germany. Mohammadi, K., Khalesro, S., Sohrabi, Y., Heidari, G., 2011. A review: beneficial effects of the mycorrhizal fungi for plant growth. J. Appl. Environ. Biol. Sci. 1 (9), 310319. Morton, J.B., Redecker, D., 2001. Two new families of Glomales, Archaeosporaceae and Paraglamaceae, with two new genera Archaeospora and Paraglomus, based on concordant molecular and morphological characters. Mycologia 93, 181195. Munkvold, L., Kjoller, R., Vestberg, M., Rosendahl, S., Jakobsen, I., 2004. High functional diversity within species of arbuscular mycorrhizal fungi. New Phytol. 164, 357364. Nasim, G., 2010. The role of arbuscular mycorrhizae in inducing resistance to drought and salinity stress in crops. In: Ashraf, M., Ozturk, M., Ahmad, M.S.A. (Eds.), Plant Adaptation and Phytoremediation. Springer-Verlag, Berlin/Heidelberg, 119114. Neto, D., Carvalho, L.M., Cruz, C., Martins-Loucao, M.A., 2006. How do mycorrhizas affect C and N relationships in flooded Aster tripolium plants. Plant Soil 279, 5163. Neumann, E., George, E., 2005. Does the percentage of arbuscular mycorrhizal fungi influence growth and nutrient uptake of a wildtype tomato cultivar and a mycorrhiza-defective mutant, cultivated with roots sharing the same soil volume. New Phytol. 166, 601609. Newsham, K.K., Fitter, A.H., Watkinson, A.R., 1995. Arbuscular mycorrhiza protect an annual grass from root pathogenic fungi in the field. J. Ecol. 83, 9911000. Ngosong, C., Jarosch, M., Raupp, J., Neumann, E., Ruess, L., 2010. The impact of farming practice on soil microorganisms and arbuscular mycorrhizal fungi: crop type versus long-term mineral and organic fertilization. Appl. Soil Ecol. 46, 134142. Norman, J.R., Hooker, J.E., 2000. Sporulation of Phytophthora fragariae shows greater stimulation by exudates of nonmycorrhizal than by mycorrhizal strawberry roots. Mycol. Res. 104, 10691073. Nowak, J., 2004. Effects of arbuscular mycorrhizal fungi and organic fertilization on growth, flowering, nutrient uptake, photosynthesis and transpiration of geranium (Pelargonium hortorum LH Bailey “Tango Orange”). Symbiosis 37, 259266. Opik, M., Moora, M., Liira, J., Zobel, M., 2006. Composition of root colonizing arbuscular mycorrhizal fungal communities in different ecosystems around the globe. J. Ecol. 94, 778790. Ortas, I., 2010. Effect of mycorrhiza application on plant growth and nutrient uptake in cucumber production under field conditions. Spanish J. Agric. Res. 8 (1), 116122. Oukarroum, A., El Madidi, S., Schansker, G., Strasser, R.J., 2007. Probing the response of barley cultivars (Hordeum vulgare L.) by chlorophyll a fluorescence OLKJIP under drought stress and re-watering. Environ. Exp. Bot. 60, 438446.

92


Ouziad, F., Wilde, P., Schmelzer, E., Hildebrandt, U., Bothe, H., 2006. Analysis of expression of aquaporins and Na1/H1 transporters in tomato colonized by arbuscular mycorrhizal fungi and affected by salt stress. Environ. Exp. Bot. 57, 177186. Parida, S.K., Das, A.B., 2005. Salt tolerance and salinity effects on plants. Ecotoxicol. Environ. Saf. 60, 324349. Parker, C., 2009. Observations on the current status of Orobanche and Striga problems worldwide. Pest. Manag. Sci. 65, 453459. Parniske, M., 2008. Arbuscular mycorrhiza: the mother of plant root endosymbioses. Nat. Rev. Microbiol. 6, 763775. Pfeiffer, C.M., Bloss, H.E., 1987. Growth and nutrition of guayule (Parthenium argentatum) in a saline soil as influenced by vesicular-arbuscular mycorrhiza and phosphorus fertilization. New Phytol. 108, 315321. Phillips, D.A., Tsai, S.M., 1992. Flavonoids as plant signals to the rhizosphere microbes. Mycorrhiza 1, 5558. Pinochet, J., Calvet, C., Camprubi, A., Fernandez, C., 1996. Interactions between migratory endoparasitic nematodes and arbuscular mycorrhizal fungi in perennial crops: a review. Plant Soil 185, 183190. Pirozynski, K.A., Malloch, D.W., 1975. The origin of land plants: a matter of mycotropism. Biosystems 6, 153164. Podila, G.K., 2002. Signaling in mycorrhizal symbioseselegant mutants lead the way. New Phytol. 154, 541545. Porcel, R., Azcoń, R., Ruiz-Lozano, J.M., 2004. Evaluation of the role of genes encoding for D1-pyrroline-5carboxylate synthetase (P5CS) during drought stress in arbuscular mycorrhizal Glycine max and Lactuca sativa plants. Physiol. Mol. Plant Pathol. 65, 211221. Porcel, R., Azcoń, R., Ruiz-Lozano, J.M., 2005. Evaluation of the role of genes encoding for dehydrin proteins (LEA D-11) during drought stress in arbuscular mycorrhizal Glycine max and Lactuca sativa plants. J. Exp. Bot. 56, 19331942. Porcel, R., Aroca, R., Ruiz-Lozano, J.M., 2012. Salinity stress alleviation using arbuscular mycorrhizal fungi. A review. Agron. Sust. Dev. 32, 181200. Pozo, M.J., Azcoń-Aguilar, C., 2007. Unravelling mycorrhiza-induced resistance. Curr. Opin. Plant Biol. 10, 393398. Pozo, M.J., Dumas-Gaudot, E., Slezack, S., Cordier, C., Asselin, A., Gianinazzi, S., et al., 1996. Induction of new chitinase isoforms in tomato roots during interactions with Glomus mosseae and/or Phytophthora nicotianae var. parasitica. Agronomie 16, 689697. Prashanthi, S.K., Kulkarni, S., Sreenivasa, M.N., Kulkarni, S., 1997. Integrated management of root rot disease of safflower caused by Rhizoctonia bataticola. Environ. Ecol. 15, 800802. Qun, H.Z., Xing, H.C., Bin, Z.Z., Rong, Z.Z., Song, W.H., 2007. Changes of antioxidative enzymes and cell membrane osmosis in tomato colonized by arbuscular mycorrhizae under NaCl stress. Colloids Surf. B: Biointerfaces 59, 128133. Raaijmakers, J.M., Paulitz, T.C., Steinberg, C., Alabouvette, C., Moenne-Loccoz, Y., 2009. The rhizosphere: a playground and battlefield for soil borne pathogens and beneficial microorganisms. Plant Soil 321, 341361. Rabie, G.H., Almadini, A.M., 2005. Role of bioinoculants in development of salt tolerance of Vicia faba plants under salinity stress. African J. Biotechnol. 4, 210222. Rasool, S., Hameed, A., Azooz, M.M., Rehman, M., Siddiqi, T.O., Ahmad, P., 2013. Salt stress: causes, types and responses of plants. In: Ahmad, P., Azooz, M.M., Prasad, M.N.V. (Eds.), Ecophysiology and Responses of Plants under Salt Stress. Springer Science 1 Business Media, pp. 124. Ravnskov, S., Jakobsen, I., 1995. Functional compatibility in arbuscular mycorrhizas measured as hyphal P transport to the plant. New Phytol. 129, 611618. Read, D.J., Leake, J.R., Perez-Morno, J., 2004. Mycorrhizal fungi as drivers of ecosystem processes in heathland and boreal forest biomes. Can. J. Bot. 82, 12431263.

References

93

Rekah, Y., Shtienberg, D., Katan, J., 1999. Spatial distribution and temporal development of Fusarium crown and root rot of tomato and pathogen dissemination in field soil. Phytopathol. 89, 831839. Rempel, C.B., Bernier, C.C., 1990. Glomus intraradices and Cochliobolus sativus interactions in wheat grown under two moisture regimes. Can J. Plant Pathol. 12, 338. Remy, W., Taylor, T.N., Hass, H., Kerp, H., 1994. Four hundred million year old vesicular arbuscular mycorrhizae. Proc. Natl. Acad. Sci. USA 91, 1184111843. Requena, N., Serrano, E., Ocon, A., Breuninger, M., 2007. Plant signal and fungal perception during arbuscular mycorrhiza establishment. Phytochemsitry 68, 3340. Reynolds, H.L., Hartley, A.E., Vogelsang, K.M., Bever, J.D., Schultz, P.A., 2005. Arbuscular mycorrhizal fungi do not enhance nitrogen acquisition and growth of old-field perennials under low nitrogen supply in glasshouse culture. New Phytologist 167, 869880. Rillig, M.C., 2004. Arbuscular mycorrhizae, glomalin, and soil aggregation. Can. J. Soil Sci. 84, 355363. Rinaldelli, E., Mancuso, S., 1996. Response of young mycorrhizal and non mycorrhizal plants of olive tree (Olea europaea L.) to saline conditions. Short term electro physiological and long term vegetative salt effects. Adv. Hort. Sci. 10, 126134. Rosendahl, C.N., Rosendahl, S., 1991. Influence of vesicular-arbuscular mycorrhizal fungi (Glomus spp.) on the response of cucumber (Cucumis sativus L.) to salt stress. Environ. Exp. Bot. 31, 313318. Roth, D.R., Fahey, T.J., 1998. The effects of acid precipitation and ozone on the ectomycorrhizae of red spruce saplings. Water Air Soil Pollut. 103, 263276. Ruhling, A., Tyler, G., 1990. Soil factors influencing the distribution of macro fungi in oak forests of southern Sweden. Hol. Ecol. 13, 1118. Ruiz-Lozano, J.M., 2003. Arbuscular mycorrhizal symbiosis and alleviation of osmotic stress. New perspectives for molecular studies. Mycorrhiza 13, 309317. Ruiz-Lozano, J.M., Azcoń, R., 2000. Symbiotic efficiency and infectivity of an autochthonous arbuscular mycorrhizal Glomus sp from saline soils and Glomus deserticola under salinity. Mycorrhiza 10, 137143. Ruiz-Lozano, J.M., Porcel, R., Aroca, R., 2006. Does the enhanced tolerance of arbuscular mycorrhizal plants to water deficit involve modulation of drought-induced plant genes. New Phytologist 171, 693698. Ruiz-Lozano, J.M., Porcel, R., Aroca, R., 2008. In: Varma, A. (Ed.), Evaluation of the Possible Participation of Drought-Induced Genes in the Enhanced Tolerance of Arbuscular Mycorrhizal Plants to Water Deficit. Mycorrhiza. Springer-Verlag, pp. 185205. Ruiz-Lozano, J.M., Porcel, R., Azcoń, R., Aroca, R., 2012. Regulation by arbuscular mycorrhizae of the integrated physiological response to salinity in plants. New challenges in physiological and molecular studies. J. Exp. Bot. 63, 40334044. Rus, A., Yokoi, S., Sharkhuu, A., Reddy, M., Lee, B., Matsumoto, T.K., et al., 2001. AtHKT1 is a salt tolerance determinant that controls Na1 entry into plant roots. Proc. Natl. Acad. Sci. USA 98, 1415014155. Sanan-Mishra, N., Pham, X.H., Sopory, S.K., Tuteja, N., 2005. Pea DNA helicase 45 overexpression in tobacco confers high salinity tolerance without affecting yield. Proc. Natl. Acad. Sci. USA 102, 509514. Schwartz, S.H., Qin, X., Zeevaart, J.A.D., 2003. Elucidation of the indirect pathway of abscisic acid biosynthesis by mutants, genes and enzymes. Plant Physiol. 131, 15911601. Sharifi, M., Ghorbanli, M., Ebrahimzadeh, H., 2007. Improved growth of salinity-stressed soybean after inoculation with pre-treated mycorrhizal fungi. J. Plant Physiol. 164, 11441151. Shaw, T.M., Dighton, J., Sanders, F.E., 1995. Interactions between ectomycorrhizal and saprotrophic fungi on agar and in association with seedlings of lodgepole pine (Pinus contorta). Mycol. Res. 99, 159165. Shekoofeh, E., Sepideh, H., Roya, R., 2012. Role of mycorrhizal fungi and salicylic acid in salinity tolerance of Ocimum basilicum resistance to salinity. J. Biot. 11 (9), 22232235. Shokri, S., Maadi, B., 2009. Effects of arbuscular mycorrhizal fungus on the mineral nutrition and yield of Trifolium alexandrium plants under salinity stress. J. Agron. 8, 7983.

94


Sieverding, E., 1990. Ecology of VAM fungi in tropical agrosystems. Agric. Ecosyst. Environ. 29, 369390. Smith, F.A., Grace, E.J., Smith, S.E., 2009. More than a carbon economy: nutrient trade and ecological sustainability in facultative arbuscular mycorrhizal symbioses. New Phytol. 182, 347358. Smith, S., Facelli, E., Pope, S., Smith, A.F., 2010. Plant performance in stressful environments: interpreting new and established knowledge of the roles of arbuscular mycorrhizas. Plant Soil 326, 320. Smith, S.E., Read, D.J., 1997. Mycorrhizal Symbiosis. second ed. Academic Press, New York. Smith, S.E., Read, D.J., 2007. Mycorrhizal Symbiosis. third ed. Academic, San Diego. Smith, S.E., Read, D.J., 2008. Mycorrhizal Symbiosis. Academic Press, London. Song, H., 2005. Effects of VAM on host plant in the condition of drought stress and its mechanisms. Elec. J. Biol. 1 (3), 4448. Sottosanto, J.B., Gell, A., Blumwald, E., 2004. DNA array analyses of Arabidopsis thaliana lacking a vacuolar Na1/H1 antiporter: impact of AtNHX1 on gene expression. Plant J. 40, 752771. Sreeramulu, K.R., Onkarappa, T., Swamy, H.N., 1998. Biocontrol of damping off and black shank disease in tobacco nursery. Tob. Res. 24, 14. Steinkellner, S., Lendzemo, V., Langer, I., Schweiger, P., Thanasan, K., Toussaint, J.P., et al., 2007. Flavonoids and strigolactones in root exudates as signals in symbiotic and pathogenic plant-fungus interactions. Molecules 12, 12901306. Strizhov, N., Abraham, E., Okresz, L., Blickling, S., Zilberstein, A., Schell, J., et al., 1997. Differential expression of two P5CS genes controlling proline accumulation during salt stress requires ABA and is regulated by ABA1, ABI1 and AXR2 in Arabidopsis. Plant J. 12, 557569. Subramanian, K.S., Charest, C., 1995. Influence of arbuscular mycorrhizae on the metabolism of maize under drought stress. Mycorrhiza 5, 273278. Subramanian, K.S., Charest, C., 1997. Nutritional, growth, and reproductive responses of maize (Zea mays L.) to arbuscular mycorrhizal inoculation during and after drought stress at tasselling. Mycorrhiza 7, 2532. Tang, M., Chen, H., 1999. Effects of arbuscular mycorrhizal fungi alkaline phosphatase activities on Hippophae rhamnoides drought-resistance under water stress conditions. Trees 14, 112115. Thakur, M., Sohal, B.S., 2013. Role of elicitors in inducing resistance in plants against pathogen infection: A review. ISRN Biochem 2013 (2013), Article ID 762412. Thompson, J.P., Wildermuth, G.B., 1989. Colonization of crop and pasture species with vesicular-arbuscular mycorrhizal fungi and negative correlation with root infection by Bipolaris sorokiniana. Can. J. Bot. 69, 687693. Tilman, D., Wedin, D., Knops, J., 1996. Productivity and sustainability influenced by biodiversity in grassland ecosystems. Nature 379, 718720. Torres-Barragan, A., Zavaleta-Mejia, E., Gonzalez-Chavez, C., Ferrera-Cerrato, R., 1996. The use of arbuscular mycorrhizae to control onion white rot (Sclerotium cepivorum Berk.) under field conditions. Mycorrhiza 6, 253258. Toussaint, J.P., 2007. Investigating physiological changes in the aerial parts of AM plants: what do we know and where should we be heading. Mycorrhiza 17, 349353. Tsang, A., Maun, M.A., 1999. Mycorrhizal fungi increase salt tolerance of Strophostyles helvola in coastal foredunes. Plant Ecol. 144, 159166. Tunnacliffe, A., Wise, M.J., 2007. The continuing conundrum of the LEA proteins. Naturwissenschaften 94, 791812. Turnau, K., Haselwandter, K., 2002. Arbuscular mycorrhizal fungi, an essential component of soil microflora in ecosystem restoration. In: Gianinazzi, S., Schuepp, H. (Eds.), Mycorrhizal Technology: from Genes to Bioproducts. Birkhauser, pp. 137149. Umar, S., Diva, I., Anjum, N.A., Iqbal, M., Ahmad, I., Pereira, E., 2011. Potassium-induced alleviation of salinity stress in Brassica campestris L. Cent. Eur. J. Biol. 6 (6), 10541063. Usha, K., Mathew, R., Singh, B., 2005. Effect of three species of arbuscular mycorrhiza on bud sprout and ripening in grapevine (Vitis vinifera L.) cv. Perlette Biol. Agric. Hortic. 23, 7383.

References

95

van der Heijden, M.G.A., Klironomos, J.N., Ursic, M., Moutoglis, P., Streitwolf-Engel, R., Boller, T., et al., 1998. Mycorrhizal fungal diversity determines plant biodiversity, ecosystem variability and productivity. Nature 396, 6972. Vandenkoornhuyse, P., Husband, R., Daniell, T.J., Watson, I.J., Duck, M., Fitter, A.H., et al., 2002. Arbuscular mycorrhizal community composition associated with two plant species in a grassland ecosystem. Mol. Ecol. 11, 15551564. Vierheilig, H., Piche, Y., 2002. Signaling in arbuscular mycorrhiza: facts and hypotheses. In: Busling, B.S., Manthey, J.A. (Eds.), Flavonoids in Cell Function. Advances in Experimental Medicine and Biology, vol. 505. Kluwer Academic, New York, pp. 2339. Wang, M., Zheng, Q., Shen, Q., Guo, S., 2013. The critical role of potassium in plant stress response. Int. J. Mol. Sci. 14 (4), 73707390. Wardle, D.A., 2002. Communities and Ecosystems: Linking Aboveground and Belowground Components, Monographs in Population Biology, vol. 34. Princeton University Press, Princeton. Wen, Y., Wang, W., Feng, J., Luo, M.C., Tsuda, K., Katagiri, F., et al., 2011. Identification and utilization of a sow thistle powdery mildew as a poorly adapted pathogen to dissect post-invasion non-host resistance mechanisms in Arabidopsis. J. Exp. Bot. 62, 21172129. Wilde, P., Manal, A., Stodden, M., Sieverding, E., Hildebrandt, U., Bothe, H., 2009. Biodiversity of arbuscular mycorrhizal fungi in roots and soils of two salt marshes. Environ. Microbiol. 11, 15481561. Wright, S.F., Upadhyaya, A., 1998. A survey of soils for aggregate stability and glomalin, a glycoprotein produced by hyphae of arbuscular mycorrhizal fungi. Plant Soil 198, 97107. Wright, S.F., Upadhyaya, A., 1999. Quantification of arbuscular mycorrhizal fungi activity by the glomalin concentration on hyphal traps. Mycorrhiza 8, 283285. Wright, S.F., Green, V.S., Cavigelli, M.A., 2007. Glomalin in aggregate size classes from three different farming systems. Soil Tillage Res. 94, 546549. Wu, Q.S., Zou, Y.N., He, X.H., 2010. Contributions of arbuscular mycorrhizal fungi to growth, photosynthesis, root morphology and ionic balance of citrus seedlings under salt stress. Acta Physiol. Plant 32, 297304. Wu, Q.S., Li, G.H., Zou, Y.N., 2011. Roles of arbuscular mycorrhizal fungi on growth and nutrient acquisition of peach (Prunus persica l. batsch) seedlings. J. Anim. Plant Sci. 21 (4), 746750. Wyss, P., Boller, T., Wiemken, A., 1991. Phytoalexin response is elicited by a pathogen (Rhizoctonia solani) but not by a mycorrhizal fungus (Glomus mosseae) in soybean roots. Experientia 47 (4), 395399. Xia, T., Apse, M.P., Aharon, G.S., Blumwald, E., 2002. Identification and characterization of a NaCl-inducible vacuolar Na1 /H1 antiporter in Beta vulgaris. Physiol. Plant 116, 206212. Yano-Melo, A.M., Saggin, O.J., Maia, L.C., 2003. Tolerance of mycorrhized banana (Musa sp. cv. Pacovan) plantlets to saline stress. Agric. Ecosyst. Environ. 95, 343348. Zak, D.R., Holmes, W.E., White, D.C., Peacock, A.D., Tilman, D., 2003. Plant diversity, soil microbial communities and ecosystem function: are there any links. Ecology 84, 20422050. Zeuthen, T., 2001. How water molecules pass through aquaporins. Trends Biochem. Sci. 26, 7781. Zhu, Y.G., Miller, R.M., 2003. Carbon cycling by arbuscular mycorrhizal fungi in soilplant systems. Trends Plant Sci. 8, 407409. Zuccarini, P., Okurowska, P., 2008. Effects of mycorrhizal colonization and fertilization on growth and photosynthesis of sweet basil under salt stress. J. Plant Nutr. 31, 497513.


CHAPTER

Role of Endophytic Microbes in Mitigation of Abiotic Stress in Plants

4

Amrita Kasotia and Devendra Kumar Choudhary

4.1 Introduction Belowground microbial activities affect aboveground ecosystems in the form of eukaryoteplant and prokaryoteplant interactions. An effect of belowground function over aboveground response constitutes an agroecosystem (AES), which is influenced by ecological interactions among communities. Varied topography of land usage and management systems affect AESs, which may lead to changes in the link between below ground and above ground (Beerling and Berner, 2005; Choudhary, 2012). The tremendous diversity of bacteria and fungi associated with plants does not affect the host in a deleterious manner, rather it stimulates growth and induces disease resistance together with tolerance against the adverse effects of the environment. In sustainable agricultural production, microbial diversity makes an association with plants that maintains integrity in the form of rhizospheric and endophytic denizens (Sturz and Nowak, 2000). Endophytes are microorganisms that range from prokaryotes to eukaryotes and that reside in plant tissues without affecting physiological functions, and they produce metabolites. Interaction between plants and endophytes results in the promotion of plant health and reflects a significant application in low-input sustainable agriculture with high productivity (Alhamed and Shebany, 2012; Corradi and Bonfante, 2012; De Pereira et al., 2012; Fan et al., 2012; Jha et al., 2012; Khan et al., 2012; Li et al., 2012; Veneklaas et al., 2012; Aroca et al., 2013; Gagne-Bourgue et al., 2013; Khan and Lee, 2013; Lopez-Raez, 2013; Malfanova et al., 2013; Mapelli et al., 2013; Pineda et al., 2013; Vaishnav et al., 2013). Choudhary (2012) elaborately described mechanisms that are employed by endophytes to alleviate high levels (beyond threshold) of abiotic stress that, in an alternative way, affect plants’ physiological functions. The ubiquitous nature of bacterial endophytes in plant tissues has been reported in some species of legumes isolated from different parts of plants (e.g., flowers, fruits, leaves, stems, roots, and seeds) including root nodules (Sturz et al., 1997; Kobayashi and Palumbo, 2000). Endophytic bacteria at the threshold level may benefit plant tissues by alleviating the environmental stresses and interspecies microbial competition. Sometimes such interaction may also become harmful to plants when microbial population produces molecules that stimulate its own species through quorum sensing that affects plant growth (Sturz et al., 2000). Virtually all plants are hosts to microbial endophytes that colonize living internal tissues of them without initiating any negative impact to the plant (Bacon and White, 2000). In contrast, Strobel and Daisy (2003) suggested that the relationship between plant and endophytes may range from P. Ahmad (Ed): Emerging Technologies and Management of Crop Stress Tolerance, Volume 2. DOI: http://dx.doi.org/10.1016/B978-0-12-800875-1.00004-1 © 2014 Elsevier Inc. All rights reserved.

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mutualistic to pathogenic. Among one million different fungal species, only 105 make an association with plants (Hawksworth and Rossman, 1987), which was further supported by Dreyfuss and Chapela (1994). The most studied fungal endophytes were reported in grass, tall fescue that prevents the attack of phytophagous insects and other grazing animals (Bultman and Murphy, 2000). The first publication about endophytes came in 1904; it highlighted the antagonistic behavior of endophytic fungus recovered from Persian darnel (an annual grass) against troublesome weeds (Freeman, 1904). Grasses provide shelter for fungal endophytes where high endophytic content induces resistance to the attack by several phytophagous pests (Omacini et al., 2001). In addition, researchers have performed considerable work (e.g., Stone et al., 2000) on different plant varieties that reflect exploration of a range of microbial endophytes. The fungal endophytes showed host specificity with fescue and rye grasses, which reflected the nonpathogenic symbiotic associations of fungus with plants (Bacon and De Battista, 1991). The plants that grow in an area affected by environmental stress harbor endophytes that produce secondary metabolites and plants overcome abiotic stress (Hata et al., 1998; Strobel et al., 2004). Schutz (2001) reported several microbial metabolites that have peculiar characteristics of certain biotopes and exhibit specificity with the host. It is anticipated that such organisms even produce high amounts of secondary metabolites with their biotopes under harsh environmental conditions (Schutz et al., 2001). Keeping in mind the role of endophytes, the aim of this chapter is to describe endophyte diversity together with the role of the microbial endophyte in alleviation of abiotic stress to plants to maintain sustainability.

4.2 Endophyte diversity For the last three decades, an archive has been pooled that defines the existence and role of microbial endophytes for agricultural sustainability. Among endophytic fungi, 11 were isolated for the first time from a tropical palm tree (Licualaramasaui) and a novel species was designated Idriella licualae (Rodrigues and Samuals, 1990). The other endophytes were mostly Xylariaceous fungi (Rodrigues et al., 1993). A guild of mitosporic and teleosporic ascomycetes endophytic fungi cause symptomless infections in leaves of vascular plants. Several plants in the temperate region have been studied for endophytic assemblages and tropical plants have been investigated for their endophytic associations (Suryanaraynan et al., 2000). Most studies on endophytes of tropical plants center around one or a few individual hosts and they address the existence of endophytes in a tropical plant community (Kumaresan and Suryanarayanan, 2001; Suryanarayanan et al., 2002). Among the genera, the coelomycete genus Phyllosticta was often present (Suryanarayanan et al., 2001). Kumaresan and Suryanarayanan (2001) demonstrated that in temperate coniferous hosts, evergreen shrubs, and mangrove trees certain fungal endophytes are host-specific. Different ubiquitous genera were isolated in tropical climates, whereas several genera were common in both tropical and temperate climates and included Fusarium, Phomopsis, and Phoma; the members of the Xylariaceae, Colletotrichum, Guignardia, Phyllosticta, and Pestalotiopsis were dominant (Suryanaraynan et al., 2003). Ravindranath et al. (1997) reported exceptionally high endophytic diversity in the Western Ghats of India that fluctuate with a distinct rainfall gradient (Suresh et al., 1999).

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Different isolates of foliary endophytic species of Phyllosticta were isolated and examined by ITS-RFLP analysis for different tropical tree species in India (Pandey et al., 2003). Maciá-Vicente et al. (2008) isolated fungal endophytes from roots of 24 plants and were characterized by phenetic and molecular techniques. The reported genera were comprised of Fusarium and Phoma, followed by Aspergillus, Alternaria, and Acremonium. In addition, members of the family Xylariaceae have been reported from nearly every continent together with conifers, dicots, monocots, ferns, and lycopsids, and they were often very closely related to each other (Brunner and Petrini, 1992; Davis et al., 2003). Among bacterial endophytes, Bacillus species are often studied isolated from tissues of different plant varieties (Philipson and Blair, 1957; Schiller et al., 1977; Sinclair, 1993; Sturz et al., 1997; Kobayashi and Palumbo, 2000; Oehrle et al., 2000). Bai et al. (2002) isolated three spore-forming Bacillus strains from surface sterilized soybean root nodules and such peculiar characteristics made Bacillus strains more applicable to commercial utilization for the agricultural sector (Liu and Sinclair, 1993). The endophytic bacterium, Acetobacter diazotrophicus, was reported for the first time in sugarcane and isolated from interior cortical cells of stem and xylem vessels (Reis et al., 1994). Several edible grasses also harbor endophytic diazotrophic bacteria, including A. diazotrophicus, Herbaspirillum spp., and Azospirillum spp., and they showed characteristics of nif genes similar to those of other nitrogen-fixing bacteria (Sevilla et al., 1997). Loganathan et al. (1999) isolated A. diazotrophicus from the host Eleusine coracana. This endophytic bacterium is important for the region because it could supply part of the nitrogen required by the crop. Verma et al. (2001, 2004) analyzed the diversity of endophytic bacteria present within the seeds of the Jaisurya variety of deep-water rice. Among these endophytes, Pantoea sp. possessed a nitrogenfixing ability but Ochrobactrum sp. was a nonnitrogen fixer. In addition, endophytic actinomycetes were isolated from Vigna unguiculata and Phaseolus vulgaris, among which prominent genera— Streptomyces, Nocardiopsis, Streptosporangium, Actinomadura, and Nocardia—were included (Britto, 1998; Matsuura, 1998). Arnold et al. (2000) reported actinomycetes in a low-land Panamanian forest, which exhibited the highest species diversity and richness; this was further supported by Sardi et al. (1992). Their isolation is an important step for screening of new bioactive compounds. Mundt and Hinckle (1976) recovered the genera Nocardia and Streptomyces from seed and ovules of 27 plant species. Sardi et al. (1992) isolated and observed endophytic actinomycetes from the roots of 28 plant species from northwestern Italy; most of the isolates were classified as Streptomyces together with Streptoverticillium, Nocardia, Micromonospora, and Streptosporangium. Then 16S rRNA gene sequencing was performed so as to retrieve sequence similarity and bacterial identity from sequence databases. The sequences obtained were compared with sequences from the GenBank database of different bacterial strains through the National Center for Biotechnology Information (NCBI) website (http://ncbi.nlm.bih-gov/BLAST). Sequencing of 16S rDNA fragments was performed and the obtained sequences of all isolates were submitted to the NCBI GenBank and allotted accession No. JF699687, JF699692-JF699700. All the sequences obtained from isolates were aligned with each other to determine genetic diversity among the endophytes. A comparison of the 16S rDNA sequence with the reference strain, to which they were matched, was performed. Sequencing data showed that most isolates belonged to genus Pseudomonas spp., a dominant species. Velázquez et al. (2008) reported genetic diversity of bacterial endophytes isolated from sugarcane and analysis of 16S rRNA sequences identified

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species of the genera Bacillus, Staphylococcus, Microbacterium, Micrococcus, Kokuria, Rhizobium, Gluconacetobacter, Comamonas, Xanthomonas, Acinetobacter, and Pantoea. Arau´jo et al. (2002) characterized Xylella fastidiosa—a causal agent of citrus variegated chlorosis (CVC)—by employing denaturing gradient gel electrophoresis (DGGE) and fatty-acid methyl ester (FAME) analysis. There are several species of endophytic bacteria—Bacillus pumilus, Curtobacterium flaccumfaciens, Enterobacter cloacae, Methylobacterium spp., Nocardia sp., Pantoea agglomerans, and Xanthomonas campestris. Methylobacterium species have been isolated from citrus (Arau´jo et al., 2001), Scotch pine (Pirttilá et al., 2000), poplar (Ulrich et al., 2008), and Crotalaria (Abdoulaye et al., 2001); they have the capacity to fix nitrogen (Abdoulaye et al., 2001).

4.3 Sustainable use of endophytes and habitat-imposed abiotic stress The plantendophyte interaction reflects the ability of endophytes to confer stress tolerance and provide strategy to mitigate the impacts of environmental changes on native and cultivated plant communities. Symbiotic endophytes benefit through acquiring nutrients by making intrinsic associations with plants transmitted through seed dissemination (Schardl et al., 2004; Schulz, 2006). Native grass species in coastal and geothermal habitats require symbiotic fungal endophytes for salt and heat tolerance, respectively (Rodriguez et al., 2008). Diazotrophic endophytic bacteria enhance plant growth through biological nitrogen fixation and production and release of plant growthregulating substances, which facilitate the revegetation of an area degraded by anthropogenic activities (Melloni et al., 2004). Endophytes belonging to genera Acinetobacter, Enterobacter, Pantoea, Pseudomonas, and Ralstonia showed plant growth-promotion characteristics in vitro and include phosphate solubilization activity, indole acetic acid (IAA), and the production of siderophore (Sobral et al., 2004; Loaces et al., 2011). How do plants survive under abiotic stress conditions? In arid and semiarid environments, the habitat-elicited stresses reduce crop productivity and lead to soil erosion and degradation. Previous studies described that more than 20% of the total cultivable land around the globe is pathetic and severely affected by environmental stresses. In such environments, several plant species have adapted by developing mechanisms that mitigate and tolerate abiotic stress. Sessile vascular plants have symbiotic endophytes that help in the amelioration of stress by developing mechanisms that cope with a number of abiotic factors. As described in the previous section, symbiotic fungal endophytes mitigate abiotic stress and allow grasses to thrive under harsh conditions. The symbiotic microbes not only provide nutrients and other growth factors but also change plants’ genome through insertion, whereby plants tolerate stresses by producing stress-responsive molecules (Choudhary, 2012). For the last two decades, significant research has been performed on free-living microbes in rhizosphere that provide tolerance to host plants under abiotic stress and include mainly bacteria belonging to different genera including Rhizobium, Bacillus, Pseudomonas, Pantoea, Paenibacillus, Burkholderia, Achromobacter, Azospirillum, Microbacterium, Methylobacterium, Variovorax, Enterobacter, and so on. These microorganisms have opened up per se to alleviate stresses and enhance agricultural productivity (Choudhary, 2012). Under favorable conditions plant growth induced by phytohormones and the level of such molecules are reduced under adverse conditions. Microorganisms (free-living and/or enophytes) under abiotic stress produce IAA, gibberellic acid

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(GA), cytokinin (CK), and compatible solutes that maintain the integrity of plants and other associated plant growth-promotion properties (Egamberdieva and Kucharova, 2009). Plant growth promotion by bacteria under saline conditions has been reported for various plants (Glick et al., 1997; Yildirim and Taylor, 2005; Barassi et al., 2006). Microbes produced CK and antioxidants, whereas abscisic acid (ABA) accumulates in the plant, which reduces the level of reactive oxygen species (ROS) and allows growth under drought conditions (Stajner et al., 1997). Inoculation of Paenibacillus polymyxa conferred drought tolerance in Arabidopsis thaliana through the induction of the drought-responsive gene erd15 (early response to dehydration 15) (Timmusk and Wagner, 1999). Furthermore, inoculation of Azospirillum brasilense Sp245 in wheat (Triticum aestivum) resulted in better water status and induced elastic adjustment that resulted in better grain yield and mineral quality (Mg, K, and Ca) at harvest under drought stress. In addition, tolerance through ACC-D in pepper and tomato plants produced by Achromobacter piechaudii ARV8 conferred induced systemic tolerance (IST) against drought and salt (Mayak et al., 2004). Plant growth regulated by signaling molecules, where the most important is ethylene, controls plant development. The biosynthesis of ethylene is under stringent control of molecular regulation that involves transcriptional and post-transcriptional factors triggered by abiotic stress (Hardoim et al., 2008). The start molecule for ethylene biosynthesis is S-adenosylmethionine (S-AdoMet) that is converted into ACC by the action of enzyme 1-aminocyclopropane-1-carboxylate synthase (ACCS). The ethylene endogenously regulates plant homoeostasis and leads to reduced root and shoot growth under abiotic stress. Mitigation of ACC by ACC-D bacteria reduced the deleterious effect of ethylene and ameliorates plant stress with growth (Glick, 2007); this was further supported by the Saleem et al. experimentations (2007). Plants produced long hairy roots when inoculated with ACC-D-containing bacteria and reflected water-use efficiency under drought conditions (Zahir et al., 2008). Besides, change in the soil’s physicochemical and structural properties in the rhizosphere was brought on by the complex and dynamic interactions among microorganisms wherein microbial exopolysaccharides (EPS) bind with soil particles to form micro- and macroaggregates (Haynes and Swift, 1990). EPS-producing bacteria increase resistance to water stress and also bind with Na1, thus making them unavailable to plants under drought and saline conditions, respectively (Sandhya et al., 2009). The level of compatible solutes (proline, ectoine, and glycine betaine) rose under abiotic stress especially under drought and salt. An increased tolerance to osmotic stress in A. thaliana has been reported by introducing proline gene proBA derived from B. subtilis (Chen et al., 2007). A level of water content was maintained in leaves of Zea mays with an increased production of proline, along with expression of hkt1 (high-affinity K1 transporter 1) under salt stress when plants were coinoculated with Rhizobium and Pseudomonas (Bano and Fatima, 2009). In addition, sugars produced under stress promote plant growth. Besides promoting plant growth in rhizosphere, rhizobia showed a trehalose metabolism that regulates plant growth and yield under abiotic stress (Suarez et al., 2008). Increased plant growth, N content, and nodulation of Phaseolus vulgaris L. under drought stress was promoted by a trehalose-producing consortium of Rhizobium tropici and P. polymyxa (Figueiredo et al., 2008). In addition to producing stress-responsive molecules, microbes emitted volatiles that downregulate expression of the gene hkt1 in roots but up-regulates it in shoots, whereby Na1 level and recirculation of Na1 is reduced in the plant under salt conditions. Pseudomonas chlororaphis O6 induced tolerance in A. thaliana against abiotic stress due to the production of a volatile

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metabolite—2R, 3R-butanediol (Zhang et al., 2008). Salicylic acid (SA), ethylene (ET), and jasmonic acid (JA) signaling pathways were reported in mutants of Arabidopsis under drought conditions (Cho et al., 2008). A bacterium, Burkholderia phytofirmans PsJN, isolated from grapevine tissue and organs (Compant et al., 2005) protected the plants against heat and chilling stress (Bensalim et al., 1998; Ait Bakra et al., 2006). In addition, endophytic fungal-mediated stress response in plants is incurred by producing ABA. The application of exogenous ABA significantly enhanced the ABA content in shoots of non-AM plants, with the expression of genes Lsp5cs and Ls1ea and the gene Lsnced, whereas the application of exogenous ABA decreased ABA content in shoots of AM plants without expression of genes (Aroca et al., 2008). Microbes also help in the production of stress-responsive enzymes in plants under drought conditions; for example, antioxidative catalase is produced in lettuce after coinoculation with Pseudomonas mendocina and Glomus intraradices and/or G. mosseae (Kohler et al., 2008). The statement was supported by an elevated level of a 14-3-3 protein-encoding gene from G. intraradices grown under drought stress (Porcel et al., 2006). In the series of stress-responsive molecules, glutathione and ascorbate played an important role in conferring protection and maintaining the metabolic function of plants under drought conditions when colonized by drought-tolerant G. intraradices and Glomus spp. (Marulanda et al., 2007).

4.4 Conclusion and future prospects The interaction of microbes with plants is a dynamic, sophisticated phenomenon wherein several external factors affect the structure and species composition of the bacterial communities. An understanding of microbial composition that is associated with plants is fundamental to understanding how plants’ biological processes are influenced by environmental factors. Plant growth and development cannot be adequately described without acknowledging microbial interactions. As a poorly investigated store of microorganisms “hidden” within the host plants, endophytes are obviously a rich and reliable source of many secondary metabolites, which may be helpful in providing resistance to plants against insects, nematodes, and pathogenic fungi and bacteria. They live within the intercellular spaces and may confer benefits to the plant and the benefits may be reciprocal, resulting in an enhanced symbiotic system for specific plant characteristics. Therefore, the use of endophytic bacteria and fungi opens up a new area of biotechnological exploitation that drives the necessity to isolate and culture these organisms. The biochemical versatility and diversity of endophytes represents an enormous variety of genes that are still unknown. More and more useful gene functions are being discovered, particularly for environmental remediation and industrial processes. Microorganisms living within plant tissues for all or part of their life cycle, without causing any visible symptoms of their presence, are defined as endophytes. Plants benefit extensively by harboring these endophytic microbes; they promote plant growth and confer enhanced resistance to various pathogens by producing antibiotics. Endophytes also produce unusual secondary metabolites important to plants under stress conditions together with some valuable pharmaceutical substances of biotechnological interest. Endophytes represent a huge diversity of microbial adaptations that have developed in special and sequestered environments, and their diversity and specialized habituation make them an exciting field of study in the search for new metabolites. In view of their widespread application in plant and human

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health and the environment, concerted efforts at endophytic diversity searches, coupled with exploitation, are necessary on account of varied and unique plant diversity.

Acknowledgments Some of the research in this chapter was supported by DBT and SERB grant No. BT/PR1231/AGR/21/340/ 2011 and SR/FT/LS-129/2012, respectively. The authors would also like to acknowledge UGC-RGNF grant No. F1-17.1/RGNF 2012-2013-SC-RAJ-19482.

References Abdoulaye, S.Y., Giraud, E., Jourand, P., Garcia, N., Willems, A., de Lajudie, P., et al., 2001. Methylotrophic Methylobacterium bacteria nodulate and fix nitrogen in symbiosis with legumes. J. Bacteriol. 183, 214220. Ait Bakra, E., Nowak, J., Clement, C., 2006. Enhancement of chilling resistance of inoculated grapevine plantlets with a plant growth promoting rhizobacterium, Burkholderia phytofirmans strain PsJN. Appl. Environ. Microbiol. 72 (11), 72467252. Alhamed, M.F.A., Shebany, Y.M., 2012. Endophytic Chaetomium globosum enhances maize seedling copper stress tolerance. Plant Biol.14 (5), 859863. Arau´jo, W.L., Saridakis, H.O., Barroso, P.A.V., Aguilar-Vildoso, C.I., Azevedo, J.L., 2001. Variability and interactions between endophytic bacteria and fungi isolated from leaf tissues of citrus rootstocks. Can. J. Microbiol. 47, 229236. Arau´jo, W.L., Marcon, J., Maccheroni Jr., W., van Elsas, J.D., van Vuurde, J.W.L., Azevedo, J.L., 2002. Diversity of endophytic bacterial populations and their interaction with Xylella fastidiosa in citrus plants. Appl. Environ. Microbiol. 68, 49064914. Arnold, A.E., Maynard, Z., Gilbert, G.S., Coley, P.D., Kursar, T.A., 2000. Are tropical fungal endophytes hyperdiverse? Ecol. Lett. 3, 267274. Aroca, R., Vernieri, P., Ruiz-Lozano, J.M., 2008. Mycorrhizal and nonmycorrhizal Lactuca sativa plants exhibit contrasting responses to exogenous ABA during drought stress and recovery. J. Exp. Bot. 59 (8), 20292041. Aroca, R., Ruiz-Lozano, J.M., Zamarreńo, A.M., Paz, J.A., Garcia-Mina, J.M., Pozo, M.J., et al., 2013. Arbuscular mycorrhizal symbiosis influences strigolactone production under salinity and alleviates salt stress in lettuce plants. J. Plant Physiol. 170, 4755. Bacon, C.W., De Battista, J., 1991. Endophytic fungi of grasses. In: Arora, D.K., Rai, B., Mukerji, K.G., Knudsen, G. (Eds.), Handbook of Applied Mycology. Marcel Dekker, New York, pp. 231356. Bacon, C.W., White, J.F., 2000. Microbial Endophytes. Marcel Dekker, New York. Bai, Y., D’Aoust, F., Smith, D.L., Driscoll, B.T., 2002. Isolation of plant-growth promoting Bacillus strains from soybean root nodules. Can. J. Microbiol. 48, 230238. Bano, A., Fatima, M., 2009. Salt tolerance in Zea mays (L.) following inoculation with Rhizobium and Pseudomonas. Biol. Fert. Soils 45, 405413. Barassi, C.A., Ayrault, G., Creus, C.M., Sueldo, R.J., Sobero, M.T., 2006. Seed inoculation with Azospirillum mitigates NaCl effects on lettuce. Sci. Hortic. 109, 814. Beerling, D.J., Berner, R.A., 2005. Feedbacks and the coevolution of plants and atmospheric CO2. Proc. Natl. Acad. Sci. USA 102, 13021305.

104


Bensalim, S., Nowak, J., Asiedu, S.K., 1998. A plant growth promoting rhizobacterium and temperature effects on performance of 18 clones of potato. Am. J. Potato Res. 75, 145152. Britto, K.C., 1998. Isolamento e Atividade Antimicrobiana de Actinomicetos Endofı´ticos do feijaõ (Phaseolus vulgaris L.). Monography. Universidade Federal de Pernambuco, Recife, Pernambuco, Brazil, pp. 42. Brunner, F., Petrini, O., 1992. Taxonomy of some Xylaria species and xylariaceous endophytes by isozyme electrophoresis. Mycological Res. 96, 723733. Bultman, T.L., Murphy, J.C., 2000. Do fungal endophytes mediate wound-induced resistance? In: Bacon, C.W., White, J.F. (Eds.), Microbial Endophytes. Marcel Dekker, New York, pp. 421452. Chen, M., Wei, H., Cao, J., Liu, R., Wang, Y., Zheng, C., 2007. Expression of Bacillus subtilis proAB genes and reduction of feedback inhibition of proline synthesis increases proline production and confers osmotolerance in transgenic Arabdopsis. J. Biochem. Mol. Biol. 40 (3), 396403. Cho, S.M., Kang, B.R., Han, S.H., Anderson, A.J., Park, J.Y., Lee, Y.H., et al., 2008. 2R, 3r-butanediol, a bacterial volatile produced by Pseudomonas chlororaphis O6, is invoplved in induction of systemic tolerance to drought in Arabdopsis thaliana. Mol. Plant Microbe Interact. 21 (8), 10671075. Choudhary, D.K., 2012. Microbial rescue to plant under habitat-imposed abiotic and biotic stresses. Appl. Microbiol. Biotechnol. 96, 11371155. Compant, S., Reiter, B., Sessitsch, A., Nowak, J., Clément, C., Barka, E.A., 2005. Endophytic colonization of Vitis vinifera L., by a plant growth-promoting bacterium, Burkholderia sp. strain PsJN. Appl. Environ. Microbiol. 71, 16851693. Corradi, N., Bonfante, P., 2012. The arbuscular mycorrhizal symbiosis: origin and evolution of a beneficial plant infection. PLoS Pathog. 8, e1002600. Davis, E.C., Franklin, J.B., Shaw, A.J., Vilgalys, R., 2003. Endophytic Xylaria (Xylariaceae) among liverworts and angiosperms: phylogenetics, distribution, and symbiosis. Am. J. Bot. 90, 16611667. De Pereira, G.V.M., Magalhaes, K.T., Lorenzetii, E.R., Souza, T.P., Schwan, R.F., 2012. A multiphasic approach for the identification of endophytic bacterial in strawberry fruit and their potential for plant growth promotion. Microbial. Ecol. 63, 405417. Dreyfuss, M.M., Chapela, I.H., 1994. Potential of fungi in the discovery of novel, low-molecular weight pharmaceuticals. In: Gullo, V.P. (Ed.), The Discovery of Natural Products with Therapeutic Potential. Butterworth-Heinemann, London, pp. 4980. Egamberdieva, D., Kucharova, Z., 2009. Selection for root colonizing bacteria stimulating wheat growth in saline soils. Biol. Fertl. Soil 45, 563571. Fan, B., Borriss, R., Bleiss, W., Wu, X., 2012. Gram-positive rhizobacterium Bacillus amyloliquefaciens FZB42 colonizes three types of plants indifferent patterns. J. Microbiol. 50, 3844. Figueiredo, M.V.B., Burity, H.A., Martinez, C.R., Chanway, C.P., 2008. Alleviation of drought stress in common bean (Phaseolus vulgaris L.) by co-inoculation with Paenibacillus polymyxa and Rhizobium tropici. Appl. Soil Ecol. 40, 182188. Freeman, E.M., 1904. The seed fungus of Lolium temulentum L. Darnel Phil. Trans. 196, 127. Gagne-Bourgue, F., Aliferis, K.A., Seguin, P., Rani, M., Samson, R., Jabaji, S., 2013. Isolation and characterization of indigenous endophytic bacteria associated with leaves of switchgrass (Panicum virgatum L.) cultivars. J. Appl. Microbiol. Available from: http://dx.doi.org/10.1111/jam.12088. Glick, B.R., 2007. Promotion of plant growth by bacterial ACC deaminase. Crit. Rev. Plant Sci. 26, 227242. Glick, B.R., Liu, C., Ghosh, S., Dumbrof, E.B., 1997. Early development of canola seedlings in the presence of plant growth promoting rhzobacterium Pseudomonas putida GR 12-2. Soil Biol. Biochem. 29, 12331239. Hardoim, P.R., van Overbeek, S.V., van Elsas, J.D., 2008. Properties of bacterial endophytes and their proposed role in plant growth. Trends Microbiol. 16, 463471. Hata, K., Futai, K., Tsuda, M., 1998. Seasonal and needle age-dependent changes of the endophytic mycobiota in Pinus thunbergii and Pinus densiflora needles. Can. J. Bot. 76, 245250.

References

105

Hawksworth, D.C., Rossman, A.Y., 1987. Where are the undescribed fungi? Phytopathology 87, 888891. Haynes, R.J., Swift, R.S., 1990. Stability of soil aggregates in relation to organic constituents and soil water content. J. Soil Sci. 41, 7383. Jha, B., Gontia, I., Hartmann, A., 2012. The roots of the halophyte Salicornia brachiata are a source of new halotolerant diazotrophic bacteria with plant growth-promoting potential. Plant Soil 356, 265277. Khan, A.L., Lee, I.-J., 2013. Endophytic Penicillium funiculosum LHL06 secretes gibberellin that reprograms Glycine max L. growth during copper stress. BMC Plant Biol. 13, 86. Khan, A.L., Hamayun, M., Kang, S.M., Hussain, J., Lee, I.J., 2012. The newly isolated endophytic fungus Paraconiothyrium sp. LK1 Produces ascotoxin. Molecules 17, 11031112. Kobayashi, D.Y., Palumbo, J.D., 2000. Bacterial endophytes and their effects on plants and use in agriculture. In: James, C.W., White Jr., J.E. (Eds.), Microbial Endophytes. Marcel Dekker Inc., New York, p. 218. Kohler, J., Hernandez, J.A., Caravaca, F., Roldan, A., 2008. Plant growth promoting rhizobacteria and arbuscular mycorrhizal fungi modify alleviation biochemical mechanisms in water stressed plants. Funct. Plant Biol. 35, 141151. Kumaresan, V., Suryanarayanan, T.S., 2001. Occurrence and distribution of endophytic fungi in a mangrove community. Mycol. Res. 105, 13881391. Li, H.Y., Wei, D.Q., Shen, M., Zhou, Z.P., 2012. Endophytes and their role in phytoremediation. Fungal Div. 54, 1118. Liu, Z.L., Sinclair, J.B., 1993. Colonization of soybean roots by Bacillus megaterium BI53-2-2. Soil Biol. Biochem. 25, 849855. Loaces, I., Ferrando, L., Scavino, A.F., 2011. Dynamics, diversity and function of endophytic siderophoreproducing bacteria in rice. Microb. Ecol. 61, 606618. Loganathan, P., Sunita, R., Parida, A.K., Nair, S., 1999. Isolation and characterization of two genetically distant groups of Acetobacter diazotrophicus from a new host plant Eleusine coracana L. J. Appl. Microbiol. 87, 167172. Lopez-Raez, J., 2013. Strigolactones: crucial cues in the rhizosphere. In: de Bruijn, F.J. (Ed.), Molecular Microbial Ecology of the Rhizosphere, Volumes 1 & 2. John Wiley & Sons, Inc., Hoboken, New Jersey, USA, p. 1316. Maciá-Vicente, J.G., Jansoon, H.B., Abdullah, S.K., Descals, E., Salinas, J., Lopez-Llorca, L.V., 2008. Fungal root endophytes from natural vegetation in Mediterranean environments with special references to Fusarium spp. FEMS Microbiol. Ecol. 64, 90105. Malfanova, N., Kamilova, F., Validov, S., Chebotar, V., Lugtenberg, B., 2013. Is L-arabinose important for the endophytic lifestyle of Pseudomonas spp.? Arch. Microbiol. 195, 917. Mapelli, F., Marasco, R., Rolli, E., Barbato, M., Cherif, H., Guesmi, A., et al., 2013. Potential for plant growth promotion of rhizobacteria associated with Salicornia growing in Tunisian hypersaline soils. BioMed. Res. Int. 2013, Article ID 248078. Marulanda, A., Porcel, R., Barea, J.M., Azcon, R., 2007. Drought tolerance and antioxidant activities in lavender plants colonized by native drought tolerant or drought sensitive Glomus species. Microb. Ecol. 54 (3), 543552. Matsuura, T., 1998. Ocorrencia de Actinomicetous Endofiticos Produtores de Antibioticos Isolados de Folhas e Raizes de Feijao Caupi (Vigna unguiculata), MS.Thesis. Universidade Federal de Pernambuco, Recife, Pernambuco, Brazil, pp. 69. Mayak, S., Tirosh, T., Glick, B.R., 2004. Plant growth promoting bacteria that confer resistance to water stress in tomato and pepper. Plant Sci. 166, 525530. Melloni, R., Nobrega, R.S.A., Moreira, F.M.S., 2004. Density and phenotypic diversity of endophytic nitrogen fixing bacteria in soils under rehabilitation after bauxite mining. Rev. Bras. Cienc. Solo 28, 8593. Mundt, J.O., Hinckle, N.F., 1976. Bacteria within ovules and seeds. Appl. Environ. Microbiol. 32, 694698.

106


Oehrle, N.W., Karr, D.B., Kremer, R.J., Emerich, D.W., 2000. Enhanced attachment of Bradyrhizobium japonicum to soybean through reduced root colonization of internally seedborne microorganisms. Can. J. Microbiol. 46, 600606. Omacini, M., Chaneton, E.J., Ghersa, C.M., Mu¨ller, C.B., 2001. Symbiotic fungal endophytes control insect host-parasite interaction webs. Nature 409, 7881. Pandey, A.K., Reddy, M.S., Suryanarayanan, T.S., 2003. ITSRFLP and ITS sequence analysis of a foliar endophytic Phyllosticta from different tropical trees. Mycological Res. 107, 439444. Philipson, M.N., Blair, I.D., 1957. Bacteria in clover root and tissue. Can. J. Microbiol. 3, 125129. Pineda, A., Marcel Dicke, M., Pieterse, C.M.J., Pozo, M.J., 2013. Beneficial microbes in a changing environment: are they always helping plants to deal with insects? Funct. Ecol. 27, 574586. Pirttilá, A.M., Laukkane, H., Pospiech, H., Myllyla¨, R., Hohtola, A., 2000. Detection of intracellular bacteria in buds of Scotch pine (Pinus sylvestris L.) by in situ hybridization. Appl. Environ. Microbiol. 66, 30373077. Porcel, R., Aroca, R., Cano, C., Bago, A., Ruiz-Lozano, J.M., 2006. Identification of a gene from the arbuscular mycorrhizal fungus Glomus intraradices encoding for a 14-3-3 protein that is upregulated by drought stress during the AM symbiosis. Micro. Ecol. 52 (3), 575582. Ravindranath, N.H., Sukumar, R., Dashingar, P., 1997. Climate Change in Forest: Impact and Adaptation. A Regional Assessment for the Western Ghats, India. Stockholm Environmental Institute, Stockholm. Reis, V.M., Olivares, F.L., Dobereiner, J., 1994. Improved methodology for isolation of Acetobacter diazotrophicus and confirmation of its endophytic habitat. World J. Microbiol. Biotechnol. 10, 401405. Rodrigues, K.F., Samuals, G.J., 1990. Preliminary study of endophytic fungi in a tropical palm. Mycol. Res. 94, 827830. Rodrigues, K.F., Leuchtmann, A., Petrini, O., 1993. Endophytes species of Xylaria: cultural and isozymic studies. Sidowia 45, 116138. Rodriguez, R.J., Henson, J., Volkenburgh, E.V., Hoy, M., Wright, L., Beckwith, F., et al., 2008. Stress tolerance in plants via habitat-adapted symbiosis. ISME J. 2, 404416. Saleem, M., Arshad, M., Hussain, S., Bhatti, A.S., 2007. Perspective of plant growth promoting rhizobacteria (PGPR) containing AC deaminase in stress agriculture. J. Ind. Microbiol. Biotechnol. 34, 635648. Sandhya, V., Ali, S.Z., Grover, M., Reddy, G., Venkateswarlu, B., 2009. Alleviation of drought stress effects in sunflower seedlings by exopolysaccharides producing Pseudomonas putida strain P45. Biol. Fert. Soil 46, 1726. Sardi, P., Saracchi, M., Quaroni, B., Borgonovi, G.E., Merli, S., 1992. Isolation of endophytic Streptomyces strains from surface-sterilized roots. Appl. Environ. Microbiol. 58, 26912693. Schardl, S.L., Leuchtmann, A., Spiering, M.J., 2004. Symbioses of grasses with seed-borne fungal endophytes. Annu. Rev. Plant Biol. 55, 315340. Schiller, C.T., Ellis, M.A., Tenne, F.D., Sinclair, J.B., 1977. Effect of Bacillus subtilis on soybean seed decay, germination and stand inhibition. Plant Dis. Rep. 61, 213216. Schulz, B.J.E., 2006. Mutualistic interactions with fungal root endophytes. In: Schulz, B.J.E., Boyle, C.J.C., Sieber, T.N. (Eds.), Microbial Root Endophytes. Springer-Verlag, Berlin, pp. 261280. Schutz, B.J.E., 2001. Endophytic fungi: a source of novel biologically active secondary metabolites. British Mycological Society, International Symposium Proceedings: Bioactive Fungal Metabolites-Impact and Exploitation. University of Wales, Swansea, pp. 20. Sevilla, M., Meletzus, D., Teixeira, K., Lee, S., Nutakki, A., Baldani, I., et al., 1997. Analysis of nif and regulatory genes in Acetobacter diazotrophicus. Soil Biol. Biochem. 29, 871874. Sinclair, J.B., 1993. Control of seedborne pathogens and diseases of soybean seeds and seedlings. Pestic. Sci. 37, 1519. Sobral, K.J., Araujo, W.L., Mendes, R., Geraldi, I.O., Pizzirani-Kleiner, A.A., Azevedo, J.L., 2004. Isolation and characterization of soybean-associated bacteria and their potential for plant growth promotion. Environ. Microbiol. 6, 12441250.

References

107

Stajner, D., Kevresan, S., Gasic, O., Mimica-Dukic, N., Zongli, H., 1997. Nitrogen and Azotobacter chroococcum enhance oxidative stress tolerance in sugar beet. Biol. Plantarum 39 (3), 441445. Stone, J.K., Bacon, C.W., White Jr., J.F., 2000. An overview of endophytic microbes: endophytism defined. Microbial Endophytes: a continuum of interactions with plants. Marcel Dekker, Inc., New York, pp. 329. Strobel, G., Daisy, B., 2003. Bioprospecting for microbial endophytes and their natural products. Microbiol. Mol. Biol. Rev. 67, 491502. Strobel, G.A., Daisy, B., Castillo, U., Harper, J., 2004. Natural products from endophytic microorganisms. J. Nat. Prod. 67, 257268. Sturz, A.V., Nowak, J., 2000. Endophytic communities of rhizobacteria and the strategies required to create yield enhancing associations with crops. Appl. Soil Ecol. 15, 183190. Sturz, A.V., Christie, B.R., Matheson, B.G., Nowak, J., 1997. Biodiversity of endophytic bacteria which colonize red clover nodules, roots, stems and foliage and their influence on host growth. Biol. Fertil. Soil 25, 1319. Sturz, A.V., Christie, B.R., Nowak, J., 2000. Bacterial endophytes: potential role in developing sustainable systems of crop production. Crit. Rev. Plant Sci. 19, 130. Suarez, R., Wong, A., Ramirez, M., Barraza, A., OrozcoMdel, C., Cevallos, M.A., et al., 2008. Improvement of drought tolerance and grain yield in common bean by overexpressing trehalose-6-phosphate synthase in rhizobia. Mol. Plant Microbe Interact. 21 (7), 958966. Suresh, H.S., Bhat, H.R., Dattaraja, H.S., Sukumar, R., 1999. Flora of Mudumalai Wildlife Sanctuary, Nilgiris, Tamil Nadu, Tech. Rep. 64. Centre for Ecological Sciences, Indian Institute of Science, Bangalore. Suryanarayanan, T.S., Kumaresan, V., Johnson, J.A., 2001. Fungal endophytes: the tropical dimension. In: Misra, J.K., Horn, B.W. (Eds.), Trichomycetes and Other Fungal Groups. Science Publishers, Inc, Enfield, pp. 197207. Suryanarayanan, T.S., Murali, T.S., Venkatesan, G., 2002. Occurrence and distribution of fungal endophytes in tropical forests across a rainfall gradient. Can. J. Bot. 80, 818826. Suryanaraynan, T.S., Santhilarasu, G., Muruganandam, V., 2000. Endophytic fungi from Cuscuta reflexa ant its host plants. Fung Diver 4, 117123. Suryanaraynan, T.S., Venkatesan, G., Murali, T.S., 2003. Endophytic fungal communities in leaves of tropical forest trees: diversity and distribution pattern. Curr. Sci. 85, 489493. Timmusk, S., Wagner, E.G.H., 1999. The plant growth-promoting rhizobacterium Paenibacillus polymyxa induces changes in Arabidopsis thalianan gene expression: a possible connection between biotic and abiotic stress responses. Mol. Plant Microbe Interact. 12, 951959. Ulrich, K., Ulrich, A., Ewald, D., 2008. Diversity of endophytic bacterial communities in poplar grown under field conditions. FEMS Microbiol. Ecol. 63, 169180. Vaishnav, A., Jain, S., Kasotia, A., Kumari, S., Gaur, R.K., Choudhary, D.K., 2013. Effect of nitric oxide signaling in bacterial treated soybean plant under salt stress. J. Arch. Microbiol. 195 (8), 571577. Velázquez, E., Rojas, M., Lorite, M.J., Rivas, R., Zurdo-Piˇneiro, J.L., Heydrich, M., et al., 2008. Genetic diversity of endophytic bacteria which could be find in the apoplastic sap of the medullary parenchyma of the stem of healthy sugarcane plants. J. Basic Microbiol. 48, 118124. Veneklaas, E.J., Lambers, H., Bragg, J., Finnegan, P.M., Lovelock, C.E., Plaxton, W.C., et al., 2012. Opportunities for improving phosphorus-use efficiency in crop plants. New Phytol. 195, 306320. Verma, S.C., Ladha, J.K., Tripathi, A.K., 2001. Evaluation of plant growth promoting and colonization ability of endophytic diazotrophs from deep water rice. J. Biotechnol. 91, 127141. Verma, S.C., Singh, A., Chowdhury, S.P., Triphati, A.K., 2004. Endophytic colonization ability of two deepwater rice endophytes, Pantoea sp. and Ochrobactrum sp. using green fluorescent protein reporter. Biotechnol. Lett. 26, 425429. Yildirim, E., Taylor, A.G., 2005. Effect of biological treatments on growth of bean plans under salt stress. Ann. Rep. Bean Improv. Coop. 48, 176177.

108


Zahir, Z.A., Munir, A., Asghar, H.N., Arshad, M., Shaharoona, B., 2008. Effectiveness of rhizobacteria containing ACC-deaminase for growth promotion of peas (Pisum sativum) under drought conditions. J. Microbiol. Biotech. 18, 958963. Zhang, H., Kim, M.S., Sun, Y., Dowd, S.E., Shi, H., Paré, P.W., 2008. Soil bacteria confer plant salt tolerance by tissue-specific regulation of sodium transporter HKT1. Mol. Plant Microbe Interact. 21, 737744.

CHAPTER

Plant Growth-Promoting Bacteria Elicited Induced Systemic Resistance and Tolerance in Plants

5

Shekhar Jain, Anookul Vaishnav, Amrita Kasotia, Sarita Kumari and Devendra Kumar Choudhary

5.1 Introduction In the present agroworld scenario, the first priority of the cultivator is to produce a healthy plant (i.e., a plant without any infectious disease) and to gain high yield in any adverse conditions. There are many microorganisms that affect a plant’s health by causing damage in different ways, ultimately leading to low yield and subsequently low economic value. On the other hand, some environmental factors, such as drought, temperature, salinity, alkalinity, and nutrients, contribute to low production at their extremities. For sustainable agriculture, plants must develop a defensive capacity against various pathogens and show tolerance for adverse environmental conditions. It is difficult to find a place that is exempt from any disease-causing agent, but only natural suppressive soil is the habitat that provides this type of environment (Weller et al., 2002; Choudhary et al., 2007). The wholesome protection of plants against biotic and abiotic stresses is provided by the belowground functioning (microbial activities) of the soil, which works as a protective shield for plants. In this region, plant roots release a substantial amount of elementary molecules, such as C- and N-containing compounds, which are utilized by microbes for growth and functional activities (Ryan and Delhaize, 2001; Choudhary and Johri, 2009). The benign role of microbes in belowground plant functioning is carried out by so-called plant growth-promoting bacteria (PGPB), and the overall effect on plant growth promotion and development, including resistance against pathogens, is accomplished by mechanism-induced systemic resistance (ISR) (Kloepper et al., 1980; Haynes and Swift, 1990; Jain et al., 2013). These bacteria also help in tolerance of abiotic stress by inducing the production of different osmoprotectants through a mechanism known as induced systemic tolerance (IST) (Choudhary, 2012). PGPBmediated ISR is accomplished through competition for an ecotype/biotope, production of allelopathic compounds in the rhizosphere, and induced resistance in plants (Jain et al., 2013). PGPBs are characterized by their colonization with the root and root surface and their ability to promote plant growth. Among PGPB, the predominant genera include Acinetobacter, Agrobacterium, Arthrobacter, Azospirillum, Bacillus, Bradyrhizobium, Frankia, Pseudomonas, Rhizobium, Serratia, Thiobacillus, and others (Lugtenberg et al., 2001; Rothballer et al., 2003; Espinosa-Urgel, 2004; Gamalero et al., 2004; Nivedhitha et al., 2008). Recently researchers used


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CHAPTER 5 PGPB Elicited Induced Systemic Resistance

PGPB to describe mechanisms of ISR and IST in various plant species that alleviate biotic and abiotic stresses and promote plant growth (Alvarez et al., 2012; Colebrook et al., 2012; Filippou et al., 2012; Krasensky and Jonak, 2012; Makandar et al., 2012; Morais Neto et al., 2012; Nishiyama et al., 2012; Nouri et al., 2012; Stearns et al., 2012; Tanou et al., 2012a,b; Wang et al., 2012; Weston et al., 2012; Yang et al., 2012; Zamioudis and Pieterse, 2012; Ayliffe et al., 2013; Balmer et al., 2013; Bellin et al., 2013; Bulgarelli et al., 2013; Christou et al., 2013; Jiang et al., 2013; Jogaiah et al., 2013; Miranda et al., 2013; Mitter et al., 2013; Oka et al., 2013; Olivares et al., 2013; Zolla et al., 2013; Zuń˜iga et al., 2013). In keeping with views of plant growth promotion under biotic and abiotic stresses, the present chapter will unravel the perplexity of ISR and IST mechanisms involved in sustainable development of plants.

5.2 PGPB-elicited response of plants against biotic stress PGPB-mediated resistance in plants completely overcomes the effect of a pathogen and/or related damaging factors (Agrios, 1988; van Loon, 1997). Plants possess a powerful immune system as a protective guard against microbial pathogens and parasites; this system is coordinated by a complex signaling network. According to the types of molecules they recognize as indicators of a pathogen attack, plants have two types of immune system: PAMP-triggered immunity (PTI) and effectortriggered immunity (ETI) (Jones and Dangl, 2006; Eulgem and Somssich, 2007; Vleesschauwer and Ho¨fte, 2009). In spite of having such a strong immune system, sometimes plants are affected by some infectious microbes. These microbes have some ability to escape a plant’s immune system, which is how they can infect plants and possibly lead to reduced quality and quantity of the product. For these types of microbes, plants require a somewhat enhanced level of resistance and this resistance is provided by PGPB (Choudhary and Johri, 2009). Plants develop an enhanced defensive capacity when they are appropriately stimulated by specific environmental stimuli, whereby they can acquire resistance against biotic stress. There are two main forms of induced resistance, systemic acquired resistance (SAR) and ISR (previously mentioned), wherein plant defenses are preconditioned by biotic stimuli through prior infection and/or treatment that results in resistance when challenged. Induction and expression of the genes involved in SAR and ISR are discriminated according to the nature of the elicitor and the regulatory pathways involved. These pathways are induced by a specific signaling molecule or elicitor, which activates different intermediate molecules in a cascading manner and forms a network of interconnected signaling pathways that regulate the plant’s induced defense against pathogens, as shown in Figure 5.1 (Choudhary et al., 2007; Jain et al., 2013). Induction of SAR involved exposure of the plant to virulent, avirulent, and nonpathogenic microbes. A specific time period is required for the establishment of SAR, which depends on type of plant and elicitor. Accumulation of pathogenesis-related (PR) proteins and salicylic acid (SA) is induced in SAR, whereas ISR is triggered by PGPB and does not involve accumulation of PR proteins and/or SA; rather, it relies on pathways regulated by jasmonate (JA) and ethylene (ET) (Pieterse et al., 2001; Yan Z et al., 2002; Choudhary et al., 2007). A study on plantmicrobe interactions found PGPB-elicited ISR against various pathogens to reduce susceptibility to the relevant disease—for example, the carnation (Dianthus caryophillus), with

Pathogen

PGPR

Induction of SAR signal

Induction of ISR signal

Translocation of SAR signal

Translocation of ISR signal

Jar1, eds8 NahG, Sid1 Sid2

etr1, eds4, eds10 ein1-ein7, isr1

Jasmonate (JA) response

Ethylene (ET) response

After challenge inoculation

After challenge inoculation

Salicylate (SA) response

NPR-1

Pathogenesis-related (PR) protein

SAR

111

Before challenge inoculation

Before challenge inoculation

5.2 PGPB-elicited response of plants against biotic stress

Defense-related protein

ISR

FIGURE 5.1 Pathogen-induced SAR and the rhizobacteria-mediated ISR signal transduction pathways.

its reduced susceptibility to wilt caused by the pathogenic fungus Fussarium sp., and cucumber (Cucumis sativus), with its reduced susceptibility to foliar disease caused by Colletotrichum orbiculare, respectively (Van Peer et al., 1991; Wei et al., 1991; Compant et al., 2005) (Table 5.1). ISR and SAR, both of which are induced-resistance processes, take place in plants by activating a different set of genes, the product of which makes plants resistant to any further pathogen attack. Arabidopsis, a model plant, has been widely used for the plantmicrobe interaction. Expression of a specific set of pathogen-inducible defense-related genes was reported in the study of Arabidopsis after induction of SA, JA, and ET pathways. As previously described, whenever plants are affected by any pathogen, accumulation of SA takes place in the infected region and formations of phloem mobile signals are induced. Subsequently, in the distal part of the plant, SA concentration increases and volatile methyl salicylate (MeSA) is released. The accumulation of SA in SAR was proven in the Arabidopsis SA-nonaccumulating mutant plant NahG. NahG expresses the bacterial salicylate hydroxylase (nahG) gene responsible for conversion of SA into catechol, making it incapable of expressing SAR (Pieterse et al., 1998). SA is the primary molecule for SAR, inducing a further signaling cascade to activate the gene responsible for pathogen resistance; it is called the pathogenesis-related (PR) gene because it encodes different PR proteins in the families PR-2, PR-5, and PR-1.

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Table 5.1 PGPB-Mediated Biocontrol of Different Plant Diseases, Pathogens, and Insects PGPBs

Crops

Bacillus amyloliquefaciens Pseudomonas fluorescens

Tomato Tobacco

Bacillus pumilus SE 34 Pseudomonas sp Streptomyces marcescens 90116 Bacillus sp. Bacillus licheniformis Bacillus cereus MJ-1 Pseudomonas sp.

Tobacco Groundnut Tobacco

Paenibacillus polymyxa E681 Enterobacter sp Azospirillum brasilense Pseudomonas aeruginosa Bacillus subtilis G803

Cucumber Pepper Red pepper White clover Medicago Sesame Chickpea Prunus cerasifera L. Mung bean Pepper

Bacillus amyloliquefaciens

Bell pepper

Disease/Pathogen/ Insect

References

Tomato mottle virus Tobacco necrosis virus Blue mold Rhizoctonia bataticola Blue mold

Murphy et al. (2000) Park and Kloepper, (2000) Zhang et al. (2003) Gupta et al. (2002) Zhang et al. (2003)

Cotton aphids Myzus persicae Myzus persicae Acyrthosiphon kondoi

Stout et al. (2002) Lucas et al. (2004) Joo et al. (2005) Kempster et al. (2002)

Fungal disease Fusarium avenaceum Rhizosphere fungi Root rot Myzus persicae

Ryu et al. (2006) Hynes et al. (2008) Russo et al. (2008) Siddiqui et al. (2001) Kokalis-Burelle et al. (2002) Herman et al. (2008)

Myzus persicae Sluzer

In plants all of these PRs have some antimicrobial properties, primarily directed against fungal pathogens (Uknes et al., 1992; Kombrink and Somssich, 1997; Saskia et al., 1999). The NPR-1 protein encoded by the npr-1 gene allows SAR establishment because it activates PRs genes after receiving a signal from SA accumulation (Pieterse et al., 1998). Therefore, the sequence of the signaling events in SAR is such that, after recognition of pathogen, SA accumulation takes place that activates the npr-1 gene followed by PR gene activation. It has been proven that the volatile MeSA can act as a long-distance mobile signal for SAR, whereas MeSA itself appears to be biologically inactive; however, it is in the systemic tissue that MeSA is hydrolyzed to SA by the MeSA-esterase activity of SA-binding protein-2 (Park et al., 2007; Heil and Ton, 2008; Vlot et al., 2008a,b; Vleesschauwer and Ho¨fte, 2009). ISR takes a more diverse and complex route to establish a higher degree of prior resistance with no infection. In place of the PRs gene, defense-related gene activation takes place in ISR via JA- and ET-mediated signaling. A thionin molecule is expressed as a defense-related protein after induction of JA signaling (Epple et al., 1995; Wasternack and Parthier, 1997; Pieterse et al., 1998), including that of proteinase inhibitors (Farmer et al., 1992), whereas pathogen-inducible genes are induced in ET signaling (Saskia et al., 1999). Unlike SAR, ISR is elicited by nonpathogenic rhizobacteria or PGPB and there is no need for initial infection as is required in SAR.

5.2 PGPB-elicited response of plants against biotic stress

113

ISR

JA

ET

Hel, ChiB, Pdf1.2 Pin Atvsp

Herbivory

Insect activity

FIGURE 5.2 Gene activation processes that happen during ISR.

After induction by PGPB, synthesis of JA and ET takes place in the plant and after challenge inoculation, the JA and ET responses activate npr-1 gene expression, which encodes the NPR-1 protein followed by activation of a defense-related gene. NPR-1 proteins are known as master regulators of both defense pathways because after receiving the preceding signal, this protein activates expression of either the PR gene or a defense-related gene for the establishment of SAR and ISR, respectively. Like MeSA, methyl jasmonate (MeJA) also works as a volatile signal for the distal part of the plant. Expression of a different defense-related gene depends on whether that NPR-1 is getting a signal from JA or ET or from both in concert. Saskia et al. (1999) have elaborately described the different defense-related gene activations by JA and ET (Figure 5.2). Expression of the pathogen-inducible genes—Hel (encoding a hevein-like protein), ChiB (encoding a basic chitinase), and Pdf1.2 (encoding a plant defensin)—and the proteins encoded by all three, was shown to have antifungal activity through ET signaling (Samac et al., 1990; Potter et al., 1993; Penninckx et al., 1996). Likewise, the activation of the Hel, ChiB, and Pdf1.2 genes were mediated by JA signaling (Penninckx et al., 1996; Thomma et al., 1998). For the expression of plant defense proteins that exhibit antagonistic and proteinase inhibitory activities, ET- and JAmediated signaling is required in a cohort manner (Penninckx et al., 1998). The pal1 gene, which encodes phenylalanine ammonia-lyase (PAL), plays an important regulatory role in the synthesis of lignin and SA in Arabidopsis; it was found to be induced by JA (Mauch-Mani and Slusarenko, 1996; McConn et al., 1997). JA is also involved in plant protection from insects and herbivores—for example, in the tomato, JA-induced expression of the Pin gene, which encodes for the proteinase inhibitor proteins (Farmer and Ryan, 1992) and protects the plant against herbivory (Heitz et al., 1999). Expression of the Atvsp gene, which encodes the vegetative storage protein (VSP), is also induced by JA signaling in

114


Arabidopsis. VSP possesses acid phosphate activity and by using this activity it retards development of insects and increases their mortality rate. That is how, by activation of such a wide range of different defense-related genes, PGPB-elicited ISR helps protect plants against a broad range of pathogens, insects, and herbivores (Berger et al., 1995).

5.3 PGPB-produced elicitors of ISR against biotic stress A number of bioactive natural chemicals, known as allelochemicals, are produced during plant microbe and microbemicrobe interactions. They are a subset of metabolites that are not required for an organism’s growth, development, and reproduction. Some PGPBs produce different allelochemicals (e.g., siderophores, antibiotics, volatiles), which are used as a weapon against plant pathogens to protect plants from pathogenic diseases. Allelochemicals may work in a competitive manner, such as siderophores, for the acquisition of iron or may directly cause damage by inhibiting the gene machinery of target pathogens such as antibiotics and volatiles (Choudhary et al., 2007).

5.3.1 Siderophore Iron, a transition metal, is one of the most important and essential micronutrients in animals and plants because it is crucial for some life-holding processes such as respiration, photosynthesis, N2-fixation, and so on. In spite of being the fourth most frequent element on earth, it is not readily available in many environments because of the very low solubility of the Fe31 ion. In such ironlimiting environments, it is difficult for plants and microbes to survive and be productive. For the survival of the self and the host plant, PGPB secretes an iron-binding ligand called “siderophore” in such an environment, which makes a complex with the Fe31 ion and thus is available to the host organism (Gupta and Gopal, 2008). Siderophores are low-molecular-weight organic compounds with a very high and specific affinity to chelate iron (Boukhalfa and Crumbliss, 2002). Although a wide range of siderophores are produced by different microorganisms’ pseudobactines, also known as pyoverdin or fluorescein, are the most important that exhibit a distinctive phenotypic trait of the rRNA homology group I species of the genus Pseudomonas (Visca et al., 2007). By sequestering the Fe31 ion, siderophores produced by different PGPBs do not allow growth of pathogenic fungi in the vicinity and showed heterologous siderophores produced by a coinhabitant (Loper and Henkels, 1999; Whipps, 2001; Compant et al., 2005). Fungi also produce siderophores, but these have a lower affinity for ferric ion (O’Sullivan and O’Gara, 1992; Loper and Henkels, 1999; Compant et al., 2005). In addition to protection of ferric iron against biocontrol bacteria and plant deleterious microorganisms, siderophores also trigger immune response in plants (Ho¨fte and Bakker, 2007). Much of the research conducted on pseudobactines during the last decade demonstrates their role in triggering plant resistance. For instance, pseudobactines produced by Pseudomonas putida WCS358 have been shown to suppress Ralstonia solanacearum in Eucalyptus urophylla (Ran et al., 2005), Erwinia carotovora in tobacco (Nicotiana tabacumn) (van Loon et al., 2008), and Botrytis cinerea in tomato (Solanum lycopersicum) (Meziane et al., 2005). Pseudobactines are also effective against viral pathogens; for example, those produced by Pseudomonas fluorescens WCS374r make Arabidopsis plants resistant against turnip crinkle virus (TCV) (Djavaheri, 2007), while those produced by Pseudomonas fluorescens CHA0 protect the tobacco plant from tobacco necrosis virus (TNV)

5.3 PGPB-produced elicitors of ISR against biotic stress

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(Maurhofer et al., 1994). Arora et al. (2001) isolated two strains of PGPB Rhizobium meliloti, RMP3 and RMP5, from Mucna pruriens, which produce siderophores and show strong antagonism against the pathogen Macrophomina phaseolina.

5.3.2 Antibiotics The finding that PGPBs produce antibiotics has significantly increased our knowledge of the biocontrol of disease. Fluorescent pseudomonads produce a wide range of antibiotics, including 2, 4-diacetylphloroglucinol (DAPG), pyoluteorin (PLT), pyrrolnitrin (PRN), phenazine-1-carboxylic acid (PCA), 2-hydroxy phenazines, and phenazine-1-carboxamide (PCN), which have different structural configurations. A wide range of other bacteria also produce different types of antibiotics that target different pathogens and protect plants from different pathogenic diseases, as detailed in Table 5.2 (Raaijmakers and Weller, 1998; Weller et al., 2002; Fernando et al., 2005). Among the aforementioned antibiotics, DAPG, the most frequently reported in PGPB-mediated disease control, is produced by Pseudomonas fluorescens CHA0, which induces resistance against oomycete Hyaloperonospora arabidopsidis (Iavicoli et al., 2003), and the root knot nematode Meloidogyne javanica (Siddiqui and Shaukat, 2003). Pseudomonas chlororaphis Q2-87 produces DAPG to elicit ISR in Arabidopsis against the leaf pathogen Pseudomonas syringae pv. tomato (Vleesschauwer and Ho¨fte, 2009; Weller et al., 2012). Several bacterial strains have the ability to produce a huge array of antibiotics and help in suppression of diverse microbial competitors—for example, Bacillus cereus strain UW85-produced zwittermycin (Silo-Suh et al., 1994; Pal and Gardener, 2006) and kanosamine (Milner et al., 1996). A study performed using Arabidopsis mutants and transgenic lines implicated defense-signaling pathways wherein DAPG-induced resistance follows a signaling route different from that into ISR. This pathway does not depend on the master regulator NPR-1 or functional JAR1 protein but is regulated by the ethylene-insensitive root-1 (eir1) gene, which is ET insensitive in the roots only (Roman et al., 1995; Vleesschauwer and Ho¨fte, 2009). The absence of ISR expression after exogenous exposure of DAPG on the eir1 mutant suggested that an intact ET-signaling pathway is required for the establishment of DAPG-inducible resistance (Iavicoli et al., 2003; Vleesschauwer and Ho¨fte, 2009). PCA, a green-pigmented heterocyclic nitrogenous compound, is produced extracellularly by several PGPBs with antagonistic activity coupled with the accumulation of toxic superoxide radicals in the target cells (Hassett et al., 1992, 1993; Chin-A-Woeng et al., 1998; Fernando et al., 2005). PCA produced by Pseudomonas fluorescens 2-79 and Pseudomonas aureofaciens 30-84 exhibits antagonism against Gaeumannomyces graminis var. tritici (Thomashow et al., 1990). Stem rot disease in canola, which is caused by Sclerotinia, is suppressed by the activity of Pseudomonas chlororaphis strain PA-23 (Zhang and Fernando, 2004). Hu et al. (2005) have isolated strain M-18 from the rhizosphere soil of sweet melon, using 1-aminocyclopropane-1-carboxylate (ACC) as the sole nitrogen source; it was found that this strain has a capability of producting PCA and pyoluteorin antibiotics.

5.3.3 Volatiles In the context of plant defense, PGPB produces volatile organic compounds (VOCs) that promote plant growth and induce systemic resistance, which provides a new insight into PGPBplant interaction. Several types of VOCs produced by bacteria have been reported so far; they play a crucial

116


role in plant defense. Some of the most common VOCs include dodecane, 2-undecanone, 2-tridecanone, 2-tridecanol, tetramethyl pyrazine 2,3-butanediol, 3-hydroxy-2-butanone (acetoin), and others. Among these 2,3-butanediol and 3-hydroxy-2-butanone are the most important, and recent research work on bacteria-produced VOCs verified their role in the elicitation of ISR (Ryu et al., 2003). Two bacterial strains—Bacillus subtilis GB03 and Bacillus amyloliquefaciens IN937a— consistently release 2,3-butanediol and 3-hydroxy-2-butanone, which are not released by Escherichia coli DH5α. Further treatment of A. thaliana plants with these strains has shown that there is significant resistance against challenge inoculation with Erwinia carotovora subsp. carotovora SCC1. Absence of disease protection upon treatment with genetically modified Bacillus strain which is unable to produce 2,3-butanediol confirmed the priming activity of such VOCs to induce resistance against disease (Ryu et al., 2003). Besides Bacillus, several strains of Pseudomonas fluorescens were reported to produce VOCs and have shown more effectiveness in controlling root

Table 5.2 List of Some Antibiotics Produced by Bacteria against Target Pathogen Antibiotic

Source

Target Pathogen

Disease

Reference

2,4-diacetylphloroglucinol Agrocin 84

Pythium spp.

Damping off

Shanahan et al. (1992)

Agrobacterium tumefaciens Aspergillus flavus

Crown gall

Kerr, (1980)

Aflatoxin contamination Wilt

Moyne et al. (2001)

Aphanomyces cochlioides Rhizoctonia solani Erwinia amylovora

Damping off

Islam et al. (2005)

Root rots Fire blight

Wilhite et al. (2001) Sandra et al. (2001)

Iturin A

Pseudomonas fluorescens F113 Agrobacterium radiobacter Bacillus subtilis AU195 Bacillus amyloliquefaciens FZB42 Lysobacter sp. strain SB-K88 Trichoderma virens Pantoea agglomerans C9-1 B. subtilis QST713

Botrytis cinerea and R. solani

Damping off

Mycosubtilin

B. subtilis BBG100

Damping off

Phenazines

P. fluorescens 2-79 and 30-84 P. fluorescens Pf-5

Pythium aphanidermatum Gaeumannomyces graminis var. tritici Pythium ultimum and R. solani R. solani and Pyricularia oryzae Phytophthora medicaginis and P. aphanidermatum

Paulitz and Belanger, (2001); Kloepper et al. (2004) Leclere et al. (2005)

Bacillomycin D Bacillomycin, Fengycin Xanthobaccin A Gliotoxin Herbicolin

Pyoluteorin, Pyrrolnitrin Pyrrolnitrin, Pseudane Zwittermicin A

Burkholderia cepacia Bacillus cereus UW85

Fusarium oxysporum

Take-all Damping off Damping off and rice blast Damping off

Koumoutsi et al. (2004)

Thomashow et al. (1990) Howell and Stipanovic, (1980) Homma et al. (1989) Smith et al. (1993)

5.4 PGPB-elicited plant response against abiotic stress

117

and seedling diseases (Shanahan et al., 1992; Pierson and Weller, 1994; Schnider et al., 1995; Cronin et al., 1997; Duffy and Défago, 1997; Raaijmakers et al., 1997, 1999; Raaijmakers and Weller, 1998, 2001; Landa et al., 2002).

5.4 PGPB-elicited plant response against abiotic stress Abiotic stresses include drought, low temperature, salinity, and alkalinity, all of which adversely influence growth and induce senescence, leading to cell death or reduced crop yield. Plants respond to these stresses by producing different compatible solutes that include organic ions or other lowmolecular-weight organic solutes (Rhodes et al., 2002). These compatible solutes comprised quaternary amino acid derivatives (proline, glycine betain, β-alaninebetaine, and prolinebetaine); tertiary amines (1,4,5,6-tetrahydro-2-methyl-4-carboxyl pyrimidine); mono-, di-, oligo-, and polysaccharides (glucose, fructose, sucrose, trehalose, raffinose, and fructans); sugar alcohols (mannitol, glycerol, and methylated inositols); and sulfonium compounds (choline-O-sulfate, dimethylsulfoniopropionate) (Vinocur and Altman, 2005; Flowers and Colmer, 2008). Despite producing a range of molecules against abiotic stress, plants struggle for survival under stress conditions and show a lower growth rate and poor yield. PGPBs play a crucial role against abiotic stress by enhancing plant tolerance. PGPB-induced tolerance has been proposed, including physical and chemical changes (Figure 5.3). A huge range

PGPB Cytokinin

VOCs EPS ACC Deaminase

ABA accumulation Na+ uptake & translocation

Antioxidant

IAA Biofilm formation & better soil aggregation

Ethylene reduction ROS removal

Better root growth & nutrient uptake

INDUCED SYSTEMIC TOLERANCE

FIGURE 5.3 PGPB-mediated induced systemic tolerance.

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of PGPBs have been reported to provide tolerance to host plants under different abiotic stress environments (Blanco and Bernard, 1994; Dardanelli et al., 2008; Dimkpa et al., 2009; Egamberdieva and Kucharova, 2009; Yang et al., 2009; Choudhary et al., 2012). To date, many bacteria have been found that involve alleviation of different abiotic stresses (Table 5.3). Promotion of root growth that produces a larger root surface area provides uptake of nutrients and water and thus increases their availability to the plant. Inoculation of the Azospirillum and cellfree supernatant of A. brasiliense in the plant has been shown to promote morphological root changes, including the production of phytohormones, auxins, cytokinins, and gibberellins (Spaepen et al., 2008). This is confirmed by exogenous application of IAA to bean roots (Remans et al., 2008a,b). A widespread characteristic of the PGPB is ACC deaminase (ACC-D) activity where bacteria regulate ACC and help abiotically stressed plants survive (Mayak et al., 2004; Saleem et al., 2007; Dimkpa et al., 2009; Lugtenberg and Kamilova, 2009). Under abiotic stress, PGPBs use the immediate ethylene precursor ACC as a source of nitrogen and, using ACC-D, degrade it into 2-oxobutanoate and ammonia, thus indirectly increasing plant growth (Glick et al., 2007; Kang et al., 2010; Bianco and Defez, 2011). Inoculation with bacteria containing ACC-D has been found to induce longer roots that help in the uptake of water from deep soil under drought stress conditions, thereby ameliorating a plant’s water use efficiency under drought conditions (Saleem et al., 2007; Zahir et al., 2008). Researchers performed experiments on ACC-D under abiotic stress conditions and found decreasing levels of ethylene in the rhizosphere (Saravanakumar and Samiyappan, 2007; Bianco and Defez, 2011). In addition, under abiotic stress conditions, the level of osmoprotectant proline increased in plants in the presence of PGPB (Smirnoff and Cumbes, 1989; Barka et al., 2006; Chen et al., 2007; Sziderics et al., 2007; Bianco and Defez, 2009; Bano and Fatima, 2009; Kohler et al., 2009; Sandhya et al., 2010; Jha et al., 2011; Vardharajula et al., 2011). Proline alters the effect of abiotic stress in a different way, such as by scavenging reactive oxygen species (ROS) using antioxidant activity and by stabilizing the protein structure through molecular chaperones (Kavi Kishor et al., 2005; Verbruggen and Hermans, 2008). Researchers performed experiments on microbial determinants under abiotic stress; these included exopolysaccharides (EPS) (Sandhya et al., 2009), trehalose (Figueiredo et al., 2008; Suarez et al., 2008), glycine betaine (GB) (Murata et al., 1992; Mohanty et al., 1993; Jagendorf and Takabe, 2001), potassium (Blumwald, 2000; Maser et al., 2002; Takahashi et al., 2007), and VOCs (Ryu, 2004). VOCs emitted by PGPB down-regulate and up-regulate hkt1 expression in roots and shoots and maintain lower Na1 levels under salt stress (Zhang et al., 2008; Yang et al., 2009). Temperature is another crucial parameter affecting plant growth and development. Most of the normal physiological processes in plants range from approximately 0 C to 40 C. Very high and very low temperatures cause injury effects in different ways. The thermotolerant Pseudomonas putida strain NBRI0987 shows a high level of stress sigma (S) (RpoS) in drought-affected chickpea (Cicer arietinum) rhizosphere under high-temperature stress at 40 C (Srivastava et al., 2008). Similar results were reported for various other crops under high temperatures (Zhang et al., 1997; Ali et al., 2009). Several PGPBs deal with cold- and/or low-temperature stress (Bensalim et al., 1998; Compant et al., 2005; Ait Bakra et al., 2006; Selvakumar et al., 2007a,b). Metabolic processes, such as photosynthesis and respiration, occupy different cellular compartments in living plants. Different ROS, such as superoxide (O22), hydrogen peroxide (H2O2), hydroxyl radical (•OH), and singlet oxygen (1O2), are continuously produced as by-products of

5.4 PGPB-elicited plant response against abiotic stress

119

Table 5.3 PGPB Mediated IST against Abiotic Stress Stress Type Salt

Bacterial Inoculate

Plant Species

Reference

Pseudomonas pseudoalcaligenes, Bacillus pumilus Azospirillum brasilense Pseudomonas mendocina

Rice (Oryza sativa)

Jha et al. (2011)

Barley (Hordeum vulgare) Lettuce (L. sativa L. cv. Tafalla) Pea (Phaseolus vulgaris) Arabidopsis thaliana Maize (Zea mays)

Omar et al. (2009) Kohler et al. (2009)

Azospirillum sp. Bacillus subtilis Pseudomonas syringae, Pseudomonas fluorescens, Enterobacter aerogenes P. fluorescens Azospirillum Achromobacter piechaudii Drought

Pseudomonas spp. Pseudomonas spp. Pseudomonas mendocina Rhizobium tropici, Paenibacillus polymyxa Bacillus Ensifer meliloti bv. mediterranense Bradyrhizobium elkanii Achromobacter piechaudii

Osmotic stress

Temperature

A. brasilense Bacillus subtilis A. brasilense Arthrobacter sp., Bacillus sp. Azospirillum Burkholderia phytofirmans Pseudomonas fluorescens, Pantoea agglomerans, Mycobacterium sp. B. phytofirmans Aeromonas hydrophila, Serratia liquefaciens, Serratia proteamaculans

Dardanelli et al. (2008) Zhang et al. (2008) Nadeem et al. (2007)

Groundnut (Arachis hypogaea) Lettuce (Lactuca sativa) Tomato (Lycopersicon esculentum) Maize (Zea mays L. cv. Kaveri) Asparagus (Asparagus officinalis L.) Lettuce (Lactuca sativa L.) Common bean (Phaseolus vulgaris L.) Lettuce (Lactuca sativa L.) Bean (Phaseolus vulgaris cv. Flamingo) Flat crown (Albizia adianthifolia) Tomato (L. esculentum), pepper (Capsicum annuum) Common bean (P. vulgaris) Arabidopsis Rice (Oryza sativa L.) Pepper (C. annuum) Wheat (T. aestivum) Grapevine (Vitis vinifera) Wheat (Triticum aestivum)

Saravanakumar and Samiyappan, (2007) Barassi et al. (2006) Mayak et al. (2004)

Potato (Solanum tuberosum) Soy bean (Glycine max)

Bensalim et al. (1998) Zhang et al. (1997)

Sandhya et al. (2010) Liddycoat et al. (2009) Kohler et al. (2008) Figueiredo et al. (2008) Arkipova et al. (2007) Mnasri et al. (2007) Swaine et al. (2007) Mayak et al. (2004) German et al. (2000) Zhang et al. (2010) Cassan et al. (2009) Sziderics et al. (2007) Pereyra et al. (2006) Barka et al. (2006) Egamberdiyeva and Hoflich, (2003)

(Continued)

120


Table 5.3 (Continued) Stress Type

Nutrient deficiency

Bacterial Inoculate

Plant Species

Reference

Burkholderia phytofirmans B. phytofirmans Azospirillum sp., Azotobacter chroococcum, Mesorhizobium ciceri, Pseudomonas fluorescens Azotobacter coroocoocum, Azospirillum brasilense, Pseudomonas putida, Bacillus lentus Bacillus sp., Burkholderia sp., Streptomyces platensis Bacillus sp.,

Grapevine (Vitis vinifera) Potato (Solanum tuberosum) Chickpea (Cicer arietinum L.)

Barka et al. (2006) Bensalim et al. (1998) Rokhzadi and Toashih, (2011)

Zea mays L.

Yazdani et al. (2009)

Zea mays L.

Oliveira et al. (2009)

Zea mays L.

Bacillus polymyxa, Mycobacterium phlei, Pseudomonas alcaligenes

Zea mays L. (Zea mays cv. Felix)

Adesemoye et al. (2008) Egamberdiyeva, (2007)

these metabolic pathways (Apel and Hirt, 2004). Major plant ROS-scavenging mechanisms include superoxide dismutase (SOD), ascorbate peroxidase (APX), glutathione reductase (GR), and catalase (CAT) enzymes. PGPBs, too, play a significant role in ROS scavenging (Bianco and Defez, 2009; Omar et al., 2009; Kohler et al., 2010; Sandhya et al., 2010). In addition, nutrient elements, such as phosphorus, potassium, iron, zinc, and copper, possess limited mobility in the soil. In one study, phosphorus accumulation was shown to decrease in plants under salt stress when P-deficiency symptoms were induced (Navarro et al., 2001; Rogers et al., 2003; Parida and Das, 2004). Several PGPB strains solubilize insoluble inorganic phosphate compounds (e.g., tri-calcium phosphate, di-calcium phosphate, hydroxyapatite, and rock phosphate) by producing organic acids (Rodrı`guez and Fraga, 1999; Egamberdiyeva, 2007; Richardson et al., 2009; Khan et al., 2009). Different PGPBs with different/matching PGP activity also showed synergistic effects when inoculated in cohorts (Tchebotar et al., 1998; Parmar and Dadarwal, 1999; Itzigsohn et al., 2000; Hamaoui et al., 2001; Sindhu et al., 2002a,b; Remans et al., 2007, 2008a,b; Elkoca et al., 2008; Yang et al., 2009; Figueiredo et al., 2010; Yadegari and Rahmani, 2010).

5.5 Conclusion and future prospects This chapter focused on the role of PGPBs in the plant protection against biotic stresses—ranging from microorganisms and parasites to nematodes and insects—and in plant tolerance of biotic stresses. They do so by producing different osmoprotectants. PGPB-elicited ISR and IST were elaborately described along with signaling cascades and gene-expression mechanisms. Given a rapidly growing global population, the demand for increased crop yields is ever increasing; that is why it

References

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has become more and more important to use agrochemicals in the form of fertilizers and pesticides. Although agrochemicals show an instant effect on growth and disease control, their effects are not long lasting and they reduce soil fertility. Plant growth-promoting bacteria are now considered the best alternative to these agrochemicals because they have many positive benefits. Besides promoting plant growth, PGPBs defend plants from different disease-causing agents. In this chapter, the role of PGPBs in biotic stress was shown in the form of ISR and allelochemicals; in the abiotic stress tolerance, it was shown in the form of IST. Another role of different PGPB strains alone and synergistically is in enhancing plant tolerance for abiotic stress. Moreover, PGPBs can be used to determine the roles of plantmicrobe interaction and rhizoremediation in the degradation of soil pollutants. To more successfully apply PGPB in the agricultural field, a greater understanding of their ecology is needed.

Acknowledgments The authors gratefully acknowledge DBT grant No. BT/PR1231/AGR/21/340/2011 to DKC. Some of the research in this chapter was supported by SERB grant No. SR/FT/LS-129/2012.

References Adesemoye, A.O., Torbert, H.A., Kloepper, J.W., 2008. Enhanced plant nutrient use efficiency with PGPR and AMF in an integrated nutrient management system. Can. J. Microbiol. 54, 876886. Agrios, G.N., 1988. Plant Pathology. third ed. Academic Press, San Diego, CA, USA. Ait Bakra, E., Nowak, J., Clément, C., 2006. Enhancement of chilling resistance of inoculated grapevine plantlets with a plant growth promoting rhizobacterium, Burkholderia phytofirmans strain PsJN. Appl. Environ. Microbiol. 72, 72467252. Ali, Sk.Z., Sandhya, V., Grover, M., Kishore, N., Rao, L.V., Venkateswarlu, B., 2009. Pseudomonas sp. strain AKM-P6 enhances tolerance of sorghum seedlings to elevated temperatures. Biol. Fert. Soil 46, 4555. Alvarez, S., Go´mez-Bellot, M.J., Castillo, M., Banoń, S., Sánchez-Blanco, M.J., 2012. Osmotic and saline effect on growth, water relations, and ion uptake and translocation in Phlomis purpurea plants. Environ. Exp. Bot. 78, 138145. Apel, K., Hirt, H., 2004. Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu. Rev. Plant Biol. 55, 373399. Arkipova, T.N., Prinsen, E., Veselov, S.U., Martinenko, E.V., Melentiev, A.I., Kudoyarova, G.R., 2007. Cytokinin producing bacteria enhance plant growth in drying soil. Plant Soil 292, 305315. Arora, N.K., Kang, S.C., Maheshweri, D.K., 2001. Isolation of siderophore producing strain of Rhizobium meliloti and their biocontrol potential against Macrophomina phaseolina that causes charcoal rot of groundnut. Curr. Sci. 81, 673677. Ayliffe, M., Periyannan, S.K., Feechan, A., Dry, I., Schumann, U., Wang, M.-B., et al., 2013. A simple method for comparing fungal biomass in infected plant tissues. Mol. Plant-Microbe Inter. 26, 658667. Balmer, D., Planchamp, C., Mauch-Mani, B., 2013. On the move: induced resistance in monocots. J. Exp. Bot. 64, 12491261. Bano, A., Fatima, M., 2009. Salt tolerance in Zea mays (L.) following inoculation with Rhizobium and Pseudomonas. Biol. Fert. Soil 45, 405413.

122


Barassi, C.A., Ayrault, G., Creus, C.M., Sueldo, R.J., Sobrero, M.T., 2006. Seed inoculation with Azospirillum mitigate NaCl effects on lettuce. Sci. Horticul. 109, 814. Barka, E.A., Nowak, J., Clément, C., 2006. Enhancement of chilling resistance of inoculated grapevine plantlets with a plant growth-promoting rhizobacterium, Burkholderia phytofirmas strain PsJN. Appl. Environ. Microbiol. 72, 72467252. Bellin, D., Asai, S., Delledonne, M., Yoshioka, H., 2013. Nitric oxide as a mediator for defense responses. Mol. Plant-Microbe Inter. 26, 271277. Bensalim, S., Nowak, J., Asiedu, S., 1998. A plant growth promoting rhizobacterium and temperature effects on performance of 18 clones of potato. Am. Potato J. 75, 145152. Berger, S., Bell, E., Sadka, A., Mullet, J.E., 1995. Arabidopsis thaliana AtVsp is homologous to soybean VspA and VspB, genes encoding vegetative storage protein acid phosphatases, and is regulated similarly by methyl jasmonate, wounding, sugars, light and phosphate. Plant Mol. Biol. 27, 933942. Bianco, C., Defez, R., 2009. Medicago truncatula improves salt tolerance when nodulated by an indole-3acetic acid-overproducind Sinorhizobium meliloti strain. J. Exp. Bot. 60, 30973107. Bianco, C., Defez, R., 2011. Soil bacteria support and protect plants against abiotic stresses. In: Shanker, A. (Ed.), Abiotic Stress in Plants—Mechanisms and Adaptations. InTech, Rijeka, India, pp. 143170. Blanco, C., Bernard, T., 1994. Osmoadaptation in rhizobia: ectoineinduced salt tolerance. J. Bacteriol. 176, 52105217. Blumwald, E., 2000. Sodium transport and salt tolerance in plants. Curr. Opin. Cell. Biol. 12, 431434. Boukhalfa, H., Crumbliss, A.L., 2002. Chemical aspects of siderophore mediated iron transport. Biometals 15, 325339. Bulgarelli, D., Schlaeppi, K., Spaepen, S., van Themaat, E.V.L., Schulze-Lefert, P., 2013. Structure and functions of the bacterial microbiota of plants. Annu. Rev. Plant Biol. 64, 807838. Cassan, F., Maiale, S., Masciarelli, O., Vidal, A., Luna, V., Ruiz, O., 2009. Cadaverine production by Azospirillum brasiliense and its possible role in plant growth promotion and osmotic stress mitigation. Eur. J. Soil Biol. 45, 1219. Chen, M., Wei, H., Cao, J., Liu, R., Wang, Y., Zheng, C., 2007. Expression of Bacillus subtilis proAB genes and reduction of feedback inhibition of proline synthesis increases proline production and confers osmotolerance in transgenic Arabdopsis. J. Biochem. Mol. Biol. 40, 396403. Chin-A-Woeng, T.F.C., Bloemberg, G.V., van der Bij, A.J., van der Drift, K.M.G.M., Schripsema, J., Kroon, B., et al., 1998. Biocontrol by phenazine-1-carboxamide producing Pseudomonas chlororaphis PCL1391 of tomato root rot caused by Fusarium oxysporum f.sp. radicis-lycopersici. Mol. Plant-Microbe Inter. 10, 7986. Choudhary, D.K., 2012. Microbial rescue to plant under habitat-imposed abiotic and biotic stresses. Appl. Microbiol. Biotechnol. 96, 11371155. Choudhary, D.K., Johri, B.N., 2009. Interactions of Bacillus spp. and plants—with special reference to induced systemic resistance (ISR). Microbiol. Res. 164, 493513. Choudhary, D.K., Prakash, A., Johri, B.N., 2007. Induced systemic resistance (ISR) in plants: mechanism of action. Indian J. Microbiol. 47, 289297. Christou, A., Manganaris, G.A., Papadopoulos, I., Fotopoulos, V., 2013. Hydrogen sulfide induces systemic tolerance to salinity and non-ionic osmotic stress in strawberry plants through modification of reactive species biosynthesis and transcriptional regulation of multiple defence pathways. J. Exp. Bot. 64, 19531966. Colebrook, E.H., Creissen, G., McGrann, G.R.D., Dreos, R., Lamb, C., Boyd, L.A., 2012. Broad-spectrum acquired resistance in barley induced by the Pseudomonas pathosystem shares transcriptional components with Arabidopsis systemic acquired resistance. Mol. Plant-Microbe Inter. 25, 658667. Compant, S., Duffy, B., Nowak, J., Clément, C., Ait Barka, E., 2005. Use of plant growth-promoting bacteria for biocontrol of plant diseases: principles, mechanisms of action, and future prospects. Appl. Environ. Microbiol. 71, 49514959.

References

123

Cronin, D., Moe¨nne-Loccoz, Y., Fenton, A., Dunne, C., Dowling, D.N., O’Gara, F., 1997. Role of 2, 4-diacetylphloroglucinol in the interaction of the biocontrol pseudomonad strain F113 with the potato cyst nematode Globodera rostochiensis. Appl. Environ. Microbiol. 63, 13571361. Dardanelli, M.S., Fernández de Co´rdoba, F.J., Rosario Espuny, M., Rodrı´guez Carvajal, M.A., Soria Dıáz, M. E., et al., 2008. Effect of Azospirillum brasilense coinoculated with Rhizobium on Phaseolus vulgaris flavonoids and Nod factor production under salt stress. Soil Bio. Biochem. 40, 27132721. Dimkpa, C., Weinand, T., Asch, F., 2009. Plantrhizobacteria interactions alleviate abiotic stress conditions. Plant Cell. Environ. 32, 16821694. Djavaheri, M., 2007. Iron-Regulated Metabolites of Plant Growth-Promoting Pseudomonas fluorescens WCS374: Their Role in Induced Systemic Resistance. Utrecht University, The Netherlands, Ph.D. thesis. Duffy, B.K., Défago, G., 1997. Zinc improves biocontrol of Fusarium crown and root rot of tomato by Pseudomonas fluorescens and represses the production of pathogen metabolites inhibitory to bacterial antibiotic biosynthesis. Phytopathology 87, 12501257. Egamberdieva, D., Kucharova, Z., 2009. Selection for root colonizing bacteria stimulating wheat growth in saline soils. Biol. Fertil. Soils 45, 563571. Egamberdiyeva, D., 2007. The effect of plant growth promoting bacteria on growth and nutrient uptake of maize in two different soils. Appl. Soil Ecol. 36, 184189. Egamberdiyeva, D., Hoflich, G., 2003. Influence of growth-promoting bacteria on the growth of wheat in different soils temperatures. Soil Biol. Biochem. 35, 973978. Elkoca, E., Kantar, F., Sahin, F., 2008. Influence of nitrogen fixing and phosphate solubilizing bacteria on nodulation, plant growth and yield of chickpea. J. Plant Nutri. 33, 157171. Epple, P., Apel, K., Bohlmann, H., 1995. An Arabidopsis thaliana thionin gene is inducible via a signal transduction pathway different from that for pathogenesis-related proteins. Plant Physiol. 109, 813820. Espinosa-Urgel, M., 2004. Plant-associated Pseudomonas populations: molecular biology, DNA dynamics, and gene transfer. Plasmid 52, 139150. Eulgem, T., Somssich, I.E., 2007. Networks of WRKY transcription factors in defense signaling. Curr. Opin. Plant Biol. 10, 366371. Farmer, E.E., Ryan, C.A., 1992. Octadecanoid precursors of jasmonic acid activate the synthesis of woundinducible proteinase inhibitors. Plant Cell 4, 129134. Farmer, E.E., Johnson, R.R., Ryan, C.A., 1992. Regulation of expression of proteinase inhibitor genes by methyl jasmonate and jasmonic acid. Plant Physiol. 98, 9951002. Fernando, W.G.D., Nakkeeran, S., Zhang, Y., 2005. In: Siddiqui, Z.A. (Ed.), PGPR: Biocontrol and Biofertilization. Springer, Dordrecht, pp. 67109. Figueiredo, M.V.B., Burity, H.A., Martinez, C.R., Chanway, C.P., 2008. Alleviation of drought stress in common bean (Phaseolus vulgaris L.) by co-inoculation with Paenibacillus polymyxa and Rhizobium tropici. Appl. Soil Ecol. 40, 182188. Figueiredo, M.V.B., Seldin, L., de Araujo, F.F., Mariano, R.L.R., 2010. Plant growth promoting rhizobacteria: fundamentals and applications. In: Maheshwari, D.K. (Ed.), Plant Growth and Health Promoting Bacteria. Springer-Verlag, Berlin/Heidelberg, pp. 2143. Filippou, P., Tanou, G., Molassiotis, A., Fotopoulos, V., 2012. Plant acclimation to environmental stress using priming agents. In: Tuteja, N., Gill, S.S. (Eds.), Plant Acclimation to Environmental Stress. Springer Science & Business Media, pp. 128. Flowers, T.J., Colmer, T.D., 2008. Salinity tolerance in halophytes. New Phytol. 179, 945963. Gamalero, E., Lingua, G., Capri, F.G., Fusconi, A., Berta, G., Lemanceau, P., 2004. Colonization pattern of primary tomato roots by Pseudomonas fluorescens A6RI characterized by dilution plating, flow cytometry, fluorescence, confocal and scanning electron microscopy. FEMS Microbiol. Ecol. 48, 7987.

124


German, M.A., Burdman, S., Okon, Y., Kigel, J., 2000. Effects of Azospirillum brasiliense of root morphology of common bean (Phaseolus vulgaris L.) under different water regimes. Biol. Fert. Soil 32, 294264. Glick, B.R., Cheng, Z., Czarny, J., Duan, J., 2007. Promotion of plant growth by ACC deaminase-producing soil bacteria. Euro. J. Plant Pathol. 119, 329339. Gupta, A., Gopal, M., 2008. Siderophore production by plant growth promoting rhizobacteria. Ind. J. Agric. Res. 42, 153156. Gupta, C.P., Dubey, R.C., Maheshwari, D.K., 2002. Plant growth enhancement and suppression of Macrophomina phaseolina causing charcoal rot of peanut by fluorescent Pseudomonas. Biol. Fertl. Soil 35, 399405. Hamaoui, B., Abbadi, J.M., Burdman, S., Rashid, A., Sarig, S., Okon, Y., 2001. Effects of inoculation with Azospirillum brasiliense on chickpeas (Cicer arietinum) anf faba bean (Vicia faba) under different growth conditions. Agro 21, 553560. Hassett, D.J., Charniga, L., Bean, K., Ohman, D.E., Cohen, M.S., 1992. Response of Pseudomonas aeruginosa to pyocyanin: mechanisms of resistance, antioxidant defenses, and demonstration of manganese-cofactored superoxide dismutase. Infect. Immun. 60, 328336. Hassett, D.J., Woodruff, W.A., Wozniak, D.J., Vasil, M.L., Cohen, M.S., Ohman, D.E., 1993. Cloning of sodA and sodB genes encoding manganese and iron superoxide dismutase in Pseudomonas aeruginosa: demonstration of increased manganese superoxide dismutase activity in alginate-producing bacteria. J. Bacteriol. 175, 76587665. Haynes, R.J., Swift, R.S., 1990. Stability of soil aggregates in relation to organic constituents and soil water content. J. Soil Sci. 41, 7383. Heil, M., Ton, J., 2008. Long-distance signalling in plant defense. Trend Plant Sci. 13, 264272. Heitz, T., Geoffroy, P., Fritig, B., Legrand, M., 1999. The PR-6 family: proteinase inhibitors in plant-microbe and plant-insects interactions. In: Datta, S.K., Muthukrishnan, S. (Eds.), Pathogenesis-Related Proteins in Plants. CRC Press, Boca Raton, FL, pp. 131155. Herman, M.A.B., Nault, B.A., Smart, C.D., 2008. Effects of plant growth promoting rhizobacteria on bell pepper production and green peach aphid infestations in New York. Crop Prot. 27, 9961002. Ho¨fte, M., Bakker, P.A.H.M., 2007. Competition for iron and induced systemic resistance by siderophores of plant growth-promoting rhizobacteria. In: Varma, A., Chincholkar, S.B. (Eds.), Microbial Siderophores. Springer-Verlag, Berlin/Heidelberg, pp. 121134. Homma, Y., Kato, Z., Hirayama, F., Konno, K., Shirahama, H., Suzui, T., 1989. Production of antibiotics by Pseudomonas cepacia as an agent for biological control of soil-borne plant pathogens. Soil Biol. Biochem. 21, 723728. Howell, C.R., Stipanovic, R.D., 1980. Suppression of Pythium ultimum induced damping-off of cotton seedlings by Pseudomonas fluorescens and its antibiotic, pyoluterin. Phytopathology 70, 712715. Hu, H.B., Xu, Y.Q., Chen, F., Zhang, X.H., Hur, B.K., 2005. Isolation and characterization of a new fluorescent Pseudomonas strain that produces both phenazine 1-carboxylic acid and pyoluteorin. J. Microbiol. Biotechnol. 15, 8690. Hynes, R.K., Leung, G.C., Hirkala, D.L., Nelson, L.M., 2008. Isolation, selection, and characterization of beneficial rhizobacteria from pea, lentil and chickpea grown in western Canada. Can. J. Microbiol. 54, 248258. Iavicoli, A., Boutet, E., Buchala, A., Métraux, J.-P., 2003. Induced systemic resistance in Arabidopsis thaliana in response to root inoculation with Pseudomonas fluorescens CHA0. Mol. Plant-Microbe Inter. 16, 851858. Islam, T.M., Hashidoko, Y., Deora, A., Ito, T., Tahara, S., 2005. Suppression of damping-off disease in host plants by the rhizoplane bacterium Lysobacter sp. strain SB-K88 is linked to plant colonization and antibiosis against soilborne peronosporomycetes. Appl. Environ. Microbiol. 71, 37863796.

References

125

Itzigsohn, R., Burdman, S., Okon, Y., Zaady, E., Yonatan, R., Perevolotsky, A., 2000. Plant growth promotion in natural pastures by inoculation with Azospirillum brasiliense under suboptimal growth conditions. Arid Soil Res. Manage. 14, 151158. Jagendorf, A.T., Takabe, T., 2001. Inducers of glycinebetaine synthesis in barley. Plant Physiol. 127, 18271835. Jain, S., Vaishnav, A., Kasotia, A., Kumari, S., Gaur, R.K., Choudhary, D.K., 2013. Bacteria induced systemic resistance and growth promotion in Glycine max L. Merrill upon challenge inoculation with Fusarium oxysporum. Proc. Natl. Acad. Sci. India, Sect. B Biol. Sci. 83, 561567. Jha, Y., Subramanian, R.B., Patel, S., 2011. Combination of endophytic and rhizospheric plant growth promoting rhizobacteria in Oryza sativa shows higher accumulation of osmoprotectant against saline stress. Acta Physiol. Planta. 33, 797802. Jiang, C.-J., Shimono, M., Sugano, S., Kojima, M., Xinqiong Liu, X., Inoue, H., et al., 2013. Cytokinins act synergistically with salicylic acid to activate defense gene expression in rice. Mol. Plant-Microbe Inter. 26, 287296. Jogaiah, S., Ramsandra Govind, S., Tran, L.S., 2012. System biology-based approaches towards understanding drought tolerance in food crops. Crit. Rev. Biotechnol. 33, 2339. Jones, J.D.G., Dangl, J.L., 2006. The plant immune system. Nature 444, 323329. Joo, G.J., Kin, Y.M., Kim, J.T., Rhee, I.K., Kim, J.H., Lee, I.J., 2005. Gibberellins-producing rhizobacteria increase endogenous gibberellins content and promote growth of red peppers. J. Microbiol. 43, 510515. Kang, B.G., Kim, W.T., Yun, H.S., Chang, S.C., 2010. Use of plant growth-promoting rhizobacteria to control stress responses of plant roots. Plant Biotechnol. Rep. 4, 179183. Kavi Kishor, P.B., Sangam, S., Amrutha, R.N., Sri Laxmi, P., Naidu, K.R., Rao, K.R.S.S., et al., 2005. Regulation of proline biosynthesis, degradation, uptake and transport in higher plants: its implications in plant growth and abiotic stress tolerance. Curr. Sci. 88, 424438. Kempster, V.N., Scott, E.S., Davies, K.A., 2002. Evidence for systemic, cross-resistance in white clover (Trifolium repens) and annual medic (Medicago truncatula var truncatula) induced by biological and chemical agents. Biocontrol Sci. Technol. 12, 615623. Kerr, A., 1980. Biological control of crown gall through production of agrocin 84. Plant Dis. 64, 2530. Khan, A.A., Jilani, G., Akhtar, M.S., Naqvi, S.M.S., Rasheed, M., 2009. Phosphorus solubilizing bacteria: occurrence, mechanisms and their role in crop production. Res. J. Agri. Biol. Sci. 1, 4858. Kloepper, J.W., Leong, J., Teintze, M., Schroth, M.N., 1980. Enhanced plant growth by siderophores produced by plant growth-promoting rhizobacteria. Nature 286, 885886. Kloepper, J.W., Ryu, C.M., Zhang, S., 2004. Induce systemic resistance and promotion of plant growth by Bacillus spp. Phytopathology 94, 12591266. Kohler, J., Hernandez, J.A., Caravaca, F., Rolda`n, A., 2008. Plant-growth-promoting rhizobacteria and abuscular mycorrhizal fungi modify alleviation biochemical mechanisms in water-stressed plants. Funct. Plant Biol. 35, 141151. Kohler, J., Hernandez, J.A., Caravaca, F., Rolda`n, A., 2009. Induction of antioxidant enzymes is involved in the greater effectiveness of a PGPR versus AM fungi with respect to increasing the tolerance of lettuce to severe salt stress. Environ. Exp. Bot. 65, 245252. Kohler, J., Caravaca, F., Rolda`n, A., 2010. An AM fungus and a PGPR intensify the adverse effects of salinity on the stability of rhizosphere soil aggregates of Lactuca sativa. Soil Bio. Biochem. 42, 429434. Kokalis-Burelle, N., Vavrina, C.S., Rosskopf, E.N., Shelby, R.A., 2002. Field evaluation of plant growthpromoting rhizobacteria amended transplant mixes and soil solarization for tomato and pepper production in Florida. Plant Soil 238, 257266. Kombrink, E., Somssich, I.E., 1997. Pathogenesis-related proteins and plant defense. In: Carroll, G., Tudzynski, P. (Eds.), The Mycota V, Part A. Plant Relationships. Springer-Verlag, Berlin, pp. 107128.

126


Koumoutsi, A., Chen, X.H., Henne, A., Liesegang, H., Gabriele, H., Franke, P., et al., 2004. Structural and functional characterization of gene clusters directing nonribosomal synthesis of bioactive lipopeptides in Bacillus amyloliquefaciens strain FZB42. J. Bact. 186, 10841096. Krasensky, J., Jonak, C., 2012. Drought, salt, and temperature stress induced metabolic rearrangements and regulatory networks. J. Exp. Bot. 63, 15931608. Landa, B.B., Mavrodi, O.V., Raaijmakers, J.M., Gardene, B.B.M., Thomashow, L.S., Weller, D.M., 2002. Differential ability of genotypes of 2,4-diacetylphloroglucinol-producing Pseudomonas fluorescens strains to colonize the roots of pea plants. Appl. Environ. Microbiol. 68, 32263237. Leclere, V., Bechet, M., Adam, A., Guez, J.S., Wathelet, B., Ongena, M., et al., 2005. Mycosubtilin overproduction by Bacillus subtilis BBG100 enhances the organism’s antagonistic and biocontrol activities. Appl. Environ. Microbiol. 71, 45774584. Liddycoat, S.M., Greenberg, B.M., Wolyn, D.J., 2009. The effect of plant growth-promoting rhizobacteria an asparagus seedling and germinating seeds subjected to water stress under greenhouse conditions. Can. J. Microbiol. 55, 388394. Loper, J.E., Henkels, M.D., 1999. Utilization of heterologous siderophores enhances levels of iron available to Pseudomonas putida in the rhizosphere. Appl. Environ. Microbiol. 65, 53575363. Lucas, G.J.A., Probanza, A., Ramos, B., Palomino, M.R., Gutiérrez Manero, F.J., 2004. Effect of inoculation of Bacillus licheniformis on tomato and pepper. Agronomie 24, 169176. Lugtenberg, B.J.J., Dekkers, L., Bloemberg, G.V., 2001. Molecular determinants of rhizosphere colonization by Pseudomonas. Annu. Rev. Phytopathol. 39, 461490. Lutgtenberg, B., Kamilova, F., 2009. Plant-growth-promoting rhizobacteria. Annu. Rev. Microbiol. 63, 541556. Makandar, R., Nalam, V.J., Lee, H., Trick, H.N., Dong, Y., Shah, J., 2012. Salicylic acid regulates basal resistance to fusarium head blight in wheat. Mol. Plant-Microbe Inter. 25, 431439. Maser, P., Gierth, M., Schroeder, J.I., 2002. Molecular mechanisms of potassium and sodium uptake in plants. Plant Soil 247, 4354. Mauch-Mani, B., Slusarenko, A.J., 1996. Production of salicylic acid precursors is a major function of phenylalanine ammonialyase in the resistance of Arabidopsis to Peronospora parasitica. Plant Cell 8, 203212. Maurhofer, M., Hase, C., Meuwly, P., Métraux, J.-P., Défago, G., 1994. Induction of systemic resistance of tobacco to tobacco necrosis virus by the root colonizing Pseudomonas fluorescens strain CHA0: influence of the gacA gene and of pyoverdine production. Phytopathology 84, 139146. Mayak, S., Tirosh, T., Glick, B.R., 2004. Plant growth promoting bacteria that confer resistance to water stress in tomato and pepper. Plant Sci. 166, 525530. McConn, M., Creelman, R.A., Bell, E., Mullet, J.E., Browse, J., 1997. Jasmonate is essential for insect defense in Arabidopsis. Proc. Natl. Acad. Sci. USA 94, 54735477. Meziane, H., Van der Sluis, I., van Loon, L.C., Ho¨fte, M., Bakker, P.A.H.M., 2005. Determinants of Pseudomonas putida WCS358 involved in inducing systemic resistance in plants. Mol. Plant Path. 6, 177185. Milner, J.L., Silo-Suh, L., Lee, J.C., He, H.Y., Clardy, J., Handelsman, J., 1996. Production of kanosamine by Bacillus cereus UW85. Appl. Environ. Microbiol. 62, 30613065. Miranda, R. de Sousa, Ruppenthal, V., Lopes, L.S., Vieira, C.F., Marques, V.B., Bezerra, M.A., et al., 2013. Phosphorus fertilization improves soybean growth under salt stress. Inter. J. Plant Anim. Sci. 1, 2129. Mitter, B., Brader, G., Afzal, M., Compant, S., Naveed, M., Trognitz, F., et al., 2013. Advances in elucidating beneficial interactions between plants, soil, and bacteria. Adv. Agron. 121, 381445. Mnasri, B., Aouani, M.E., Mhamdi, R., 2007. Nodulation and growth of common bean (Phaseolus vulgaris) under water deficiency. Soil Bio. Biochem. 39, 17441750.

References

127

Mohanty, P., Hayashi, H., Papageorgiou, G.C., Murata, N., 1993. Stabilization of the Mn-cluster of the oxygenevolving complex by glycinebetaine. Biochim. Biophys. Acta 1144, 9296. Morais Neto, L.B., Carneiro, M.S.S., Lacerda, C.F., Costa, M.R.G.F., Fontenele, R.M., Feitosa, J.V., 2012. Effect of irrigation water salinity and cutting age on the components of biomass of Echinochloa pyramidalis. Rev. Bras. Zootecn. 41, 550556. Moyne, A.L., Shelby, R., Cleveland, T.E., Tuzun, S., 2001. Bacillomycin D: an iturin with antifungal activity against Aspergillus flavus. J. Appl. Microbiol. 90, 622629. Murata, N., Mohanthy, P.S., Hayashi, H., Papageorgiou, G.C., 1992. Glycinebetaine stabilizes the association of extrinsic proteins with the photosynthetic oxygen involving PS-II complex against the inhibitory effects of NaCl. FEBS Lett. 296, 187189. Murphy, J.F., Zehnder, G.W., Schuster, D.J., Sikora, E.J., Polston, J.E., Kloepper, J.W., 2000. Plant growthpromoting rhizobacterial mediated protection in tomato against tomato mottle virus. Plant Dis. 84, 779784. Nadeem, S.M., Zahir, Z.A., Naveed, M., Arshad, M., 2007. Preliminary investigations on inducing salt tolerance in maize through inoculation with rhizobacteria containing ACC deaminase activity. Can. J. Microbiol. 53, 11411149. Navarro, J.M., Botella, M.A., Cerda, A., Martinez, V., 2001. Phosphorus uptake and translocation in saltstressed melon plants. J. Plant Physiol. 158, 375381. Nishiyama, R., Le, D.T., Watanabe, Y., Matsui, A., Tanaka, M., et al., 2012. Transcriptome analyses of a salttolerant cytokinin-deficient mutant reveal differential regulation of salt stress response by cytokinin deficiency. PLoS One 7, e32124. Nivedhitha, V.R., Shwetha, B., Deepa, Divya, D.D., Manoj, K., Nagasampige, H., et al., 2008. Plant growth promoting microorganisms (PGPMs) from bamboo rhizosphere. Adv. Biotech. 3335. Nouri, M.Z., Hiraga, S., Yanagawa, Y., Sunohara, Y., Matsumoto, H., et al., 2012. Characterization of calnexin in soybean roots and hypocotyls under osmotic stress. Phytochemistry 74, 2029. O’Sullivan, D.J., O’Gara, F., 1992. Traits of fluorescent Pseudomonas spp. involved in suppression of plant root pathogens. Microbiol. Rev. 56, 662676. Oka, K., Amano, Y., Katou, S., Seo, S., Kei Kawazu, K., Mochizuki, A., et al., 2013. Tobacco MAP kinase phosphatase (NtMKP1) negatively regulates wound response and induced resistance against necrotrophic pathogens and lepidopteran herbivores. Mol. Plant-Microbe Inter. 26, 668675. Olivares, J., Bedmar, E.J., Sanjuán, J., 2013. Biological nitrogen fixation in the context of global change. Mol. Plant-Microbe Inter. 26, 486494. Oliveira, C.A., Alves, V.M.C., Marriel, I.E., Gomes, E.A., Scotti, M.R., Carneiro, N.P., et al., 2009. Phosphate solubilizing microorganisms isolated from rhizosphere of maize cultivated in an oxisol of the Brazilian Cerrado Biome. Soil Biol. Biochem. 41, 17821787. Omar, M.N.A., Osman, M.E.H., Kasim, W.A., Abd El-Daim, I.A., 2009. Improvement of salt tolerance mechanisms of barley cultivated under salt stress using Azospirillum brasiliense. Task Veget. Sci. 44, 133147. Pal, K.K., Gardener, B.M., 2006. Biological control of plant pathogens. T Plant Health Instruct. Available from: http://dx.doi.org/10.1094/PHI-A-2006-1117-02. Parida, A.K., Das, A.B., 2004. Effects of NaCl stress on nitrogen and phosphorous metabolism in a true mangrove Bruguiera parviflora grown under hydroponic culture. J. Plant Physiol. 161, 921928. Park, K.S., Kloepper, J.W., 2000. Activation of PR-1a promoter by rhizobacteria that induce systemic resistance in tobacco against Pseudomonas syringae pv. tabaci. Biol. Control 18, 29. Park, S.-W., Kaimoyo, E., Kumar, D., Mosher, S., Klessig, D.F., 2007. Methyl salicylate is a critical mobile signal for plant systemic acquired resistance. Science 318, 113116.

128


Parmar, N., Dadarwal, K.R., 1999. Stimulation of nitrogen fixation and induction of flavonoid like compounds by rhizobacteria. J. Appl. Microbiol. 86, 3644. Paulitz, T.C., Belanger, R.R., 2001. Biological control in greenhouse systems. Annu. Rev. Phytopathol. 39, 103133. Penninckx, I.A.M.A., Eggermont, K., Terras, F.R.G., Thomma, B.P.H.J., De Samblanx, G.W., Buchala, A., et al., 1996. Pathogen-induced systemic activation of a plant defensin gene in Arabidopsis follows a salicylic acid-independent pathway. Plant Cell 8, 23092323. Penninckx, I.A.M.A., Thomma, B.P.H.J., Buchala, A., Métraux, J.-P., Broekaert, W.F., 1998. Concomitant activation of jasmonate and ethylene response pathways is required for induction of a plant defensin gene in Arabidopsis. Plant Cell 10, 21032113. Pereyra, M.A., Zlazar, C.A., Barassi, C.A., 2006. Root phospholipids in in Azospirillum inoculated wheat seedlings exposed to water stress. Plant Physiol. Biochem. 44, 873879. Pierson, E.A., Weller, D.M., 1994. Use of mixtures of fluorescent pseudomonads to suppress take-all and improve the growth of wheat. Phytopathology 84, 940947. Pieterse, C.M.J., van Wees, S.C.M., van Pelt, J.A., Knoester, M., Laan, R., Gerrits, H., et al., 1998. A novel signalling pathway controlling induced systemic resistance in Arabidopsis. Plant Cell 10, 15711580. Pieterse, C.M.J., Ton, J., van Loon, L.C., 2001. Cross-talk between plant defense signaling pathways: boost or burden? Agri. Biotech. Net 3, 118. Potter, S., Uknes, S., Lawton, K., Winter, A.M., Chandler, D., DiMaio, J., et al., 1993. Regulation of a heveinlike gene in Arabidopsis. Mol. Plant-Microbe Interact 6, 680685. Raaijmakers, J.M., Weller, D.M., 1998. Natural plant protection by 2,4-diacetyl-phloroglucinol-producing Pseudomonas spp. in take-all decline soils. Mol. Plant-Microbe Inter. 11, 144152. Raaijmakers, J.M., Weller, D.M., 2001. Exploiting genotypic diversity of 2,4-diacetylphloroglucinol-producing Pseudomonas spp.: characterization of superior root-colonizing P. fluorescens strain Q8r1-96. Appl. Environ. Microbiol. 67, 25452554. Raaijmakers, J.M., Weller, D.M., Thomashow, L.S., 1997. Frequency of antibiotic-producing Pseudomonas spp. in natural environments. Appl. Environ. Microbiol. 63, 881887. Raaijmakers, J.M., Bonsall, R.F., Weller, D.M., 1999. Effect of population density of Pseudomonas fluorescens on production of 2,4-diacetylphloroglucinol in the rhizosphere of wheat. Phytopathology 89, 470475. Ran, L.X., Li, Z.N., Wu, G.J., van Loon, L.C., Bakker, P.A.H.M., 2005. Induction of systemic resistance against bacterial wilt in Eucalyptusurophylla by fluorescent Pseudomonas spp. Eur. J. Plant Pathol. 113, 5970. Remans, R., Croonenborghs Gutiérrez, R.T., Michiels, J., Vanderleyden, J., 2007. Effect of plant growthpromoting rhizobacteria on nodulation of Phaseolus vulgaris L. are dependent on plant P nutrition. Eur. J. Plant Pathol. 119, 341351. Remans, R., Beebe, S., Blair, M., Manrique, G., Tovar, E., Rao, I., et al., 2008a. Physiological and genetic analysis of root responsiveness to auxin-producing plant growth promoting bacteria in common bean (Phaseolus vulgaris L.). Plant Soil 302, 149161. Remans, R., Ramaekers, L., Shelkens, S., Hernandez, G., Garcia, A., Reyes, G.L., et al., 2008b. Effect of Rhizobium-Azospirillum co-inoculation on nitrogen fixation and yield of two contrasting Phaseolus vulgaris L. genotypes cultivated across different environments in Cuba. Plant Soil 312, 2537. Rhodes, D., Nadolska-Orczyk, A., Rich, P.J., 2002. Salinity, osmolytes and compatible solutes. In: Laüchli, A., Lu¨ttge, U. (Eds.), Salinity: EnvironmentPlantsMolecules. Kluwer, Dordrecht, pp. 181204. Richardson, A.E., Barea, J.-M., McNeill, A.M., Prigent-Cobaret, C., 2009. Acquisition of phosphorus and nitrogen in the rhizosphere and plant growth promotion by microorganisms. Plant Soil 321, 305339.

References

129

Rodrı`guez, H., Fraga, R., 1999. Phosphate solubilizing bacteria and their role in plant growth promotion. Biotechnol. Adv. 17, 319339. Rogers, M.C., Grieve, C., Shannon, M., 2003. Plant growth and ion relations in Lucerne (Medicago sativa L.) in response to the combined effects of NaCl and P. Plant Soil 253, 187194. Rokhzadi, A., Toashih, V., 2011. Nutrient uptake and yield of chickpea (Cicer arietinum L.) inoculated with plant growth-promoting rhizobacteria. Aust. J. Cop. Sci. 5, 4448. Roman, G., Lubarsky, B., Kieber, J.J., Rothenberg, M., Ecker, J.R., 1995. Genetic analysis of ethylene signal transduction in Arabidopsis thaliana: five novel mutant loci integrated into a stress response pathway. Genetic 139, 13931409. Rothballer, M., Schmid, M., Hartmann, A., 2003. In situ localization and PGPR-effect of Azospirillum brasilense strains colonizing roots of different wheat varieties. Symbios 34, 261279. Russo, A., Vettori, L., Felici, C., Fiaschi, G., Morini, S., Toffanin, A., 2008. Enhanced micropropagation response and biocontrol effect of Azospirillum brasilense Sp245 on Prunus cerasifera L. clone Mr.S 2/5 plants. J. Biotechnol. 134, 312319. Ryan, P.R., Delhaize, E., 2001. Function and mechanism of organic anion exudation from plant roots. Annu. Rev. Plant Physiol. Plant Mol. Biol. 52, 527560. Ryu, C.M., 2004. Bacterial volatiles induce systemic resistance in Arabidopsis. Plant Physiol. 134, 10171026. Ryu, C.-M., Hu, C.-H., Reddy, M.S., Kloepper, J.W., 2003. Different signaling pathways of induced resistance by rhizobacteria in Arabidopsis thaliana against two pathovars of Pseudomonas syringae. New Phytol. 160, 413420. Ryu, C.M., Kim, J., Choi, O., Kim, S.H., Park, C.S., 2006. Improvement of biological control capacity of Paenibacillus polymyxa E681 by seed pelleting on sesame. Biol. Control 39, 282289. Saleem, M., Arshad, M., Hussain, S., Bhatti, A.S., 2007. Perspective of plant growth promoting rhizobacteria (PGPR) containing AC deaminase in stress agriculture. J. Ind. Microbiol. Biotechnol. 34, 635648. Samac, D.A., Hironaka, C.M., Yallaly, P.E., Shah, D.M., 1990. Isolation and characterization of the genes encoding basic and acidic chitinase in Arabidopsis thaliana. Plant Physiol. 93, 907914. Sandhya, V., Ali, Sk.Z., Grover, M., Reddy, G., Venkateswarlu, B., 2009. Alleviation of drought stress effects in sunflower seedlings by exopolysaccharides producing Pseudomonas putida strain P45. Biol. Fert. Soil 46, 1726. Sandhya, V., Ali, Sk.Z., Grover, M., Reddy, G., Venkateswarlu, B., 2010. Effect of plant growth promoting Pseudomonas spp. on compatible solutes, antioxidant status and plant growth of maize under drought stress. Plant Growth Regul. 62, 2130. Sandra, A.I., Wright, C.H., Zumoff, L.S., Steven, V.B., 2001. Pantoea agglomerans strain EH318 produces two antibiotics that inhibit Erwinia amylovora in vitro. Appl. Environ. Microbiol. 67, 282292. Saravanakumar, D., Samiyappan, R., 2007. ACC deaminase from Pseudomonas fluorescens mediated saline resistance in groundnut (Arachis hypogea) plants. J. Appl. Microbiol. 102, 12831292. Saskia, C.M., Wees, V., Luijendijk, M., Smoorenburg, I., van Loon, L.C., Pieterse, C.M.J., 1999. Rhizobacteria-mediated induced systemic resistance (ISR) in Arabidopsis is not associated with a direct effect on expression of known defense-related genes but stimulates the expression of the jasmonateinducible gene Atvsp upon challenge. Plant Mol. Biol. 41, 537549. Schnider, U., Keel, C., Blumer, C., Troxler, J., Défago, G., Haas, D., 1995. Amplification of the housekeeping sigma factor in Pseudomonas fluorescens CHA0 enhances antibiotic production and improves biocontrol abilities. J. Bacteriol. 177, 53875392. Selvakumar, G., Kundu, S., Joshi, P., Nazim, S., Gupta, A.D., Mishra, P.K., et al., 2007a. Characterization of a cold tolerant plant growth promoting bacterium Pantoea dispersa 1A isolated from a sub-alpine soil in the North Western Indian Himalayas. World J. Microbiol. Biotechnol. 24, 955960.

130


Selvakumar, G., Mohan, M., Kundu, S., Gupta, A.D., Joshi, P., Nazim, S., et al., 2007b. Cold tolerance and plant growth promotional potential of Serratia marcescens strain SRM (MTCC 8708) isolated from flowers of summer squash. Lett. Appl. Microbiol. 46, 171175. Shanahan, P., O’Sullivan, D.J., Simpson, P., Glennon, J.D., O’Gara, F., 1992. Isolation of 2,4-diacetylphloroglucinol from a fluorescent pseudomonad and investigation of physiological parameters influencing production. Appl. Environ. Microbiol. 58, 352358. Siddiqui, I.A., Ehteshamul-Haque, S., Shaukat, S.S., 2001. Use of rhizobacteria in the control of root rot-root knot disease complex of mungbean. J. Phytopathol. 149, 337346. Siddiqui, M.A., Shaukat, S.S., 2003. Suppression of root-knot disease by Pseudomonas fluorescens CHA0 in tomato: importance of bacterial secondary metabolite, 2,4-diacetylpholoroglucinol. Soil Biol. Biochem. 35, 16151623. Silo-Suh, L.A., Lethbridge, B.J., Raffel, S.J., He, H., Clardy, J., Handelsman, J., 1994. Biological activities of two fungistatic antibiotics produced by Bacillus cereus UW85. Appl. Environ. Microbiol. 60, 20232030. Sindhu, S.S., Gupta, S.K., Suneja, S., Dadarwal, K.R., 2002a. Enhancement of green gram nodulation and growthby Bacillus species. Biologi Planta 45, 117120. Sindhu, S.S., Suneja, S., Goel, A.K., Pramar, N., Dadarwal, K.R., 2002b. Plant growth promoting effects of Pseudomonas sp. on co-inoculation with Mesorhizobium sp. cicer strain under sterile and wilt sick soil conditions. Appl. Soil Ecol. 19, 5764. Smirnoff, N., Cumbes, Q.J., 1989. Hydroxyl radical scavenging activity of compatible solutes. Phytochemistry 28, 10571060. Smith, K.P., Havey, M.J., Handelsman, J., 1993. Suppression of cottony leak of cucumber with Bacillus cereus strain UW85. Plant Dis. 77, 139142. Spaepen, S., Boddelaere, S., Croonenborghs, A., Vanderleyden, J., 2008. Effect of Azospirillum brasiliense indole-3-acetic acid production on inoculated wheat plants. Plant Soil 312, 1523. Srivastava, S., Yadav, A., Seem, K., Mishra, S., Chaudhary, V., Srivastava, C.S., 2008. Effect of high temperature on Pseudomonas putida NBRI0987 biofilm formation and expression of stress sigma factor RpoS. Curr. Microbiol. 56, 453457. Stearns, J.C., Woody, O.Z., McConkey, B.J., Glick, B.R., 2012. Effects of bacterial ACC deaminase on Brassica napus gene expression. Mol. Plant-Microbe Inter. 25, 668676. Stout, M.J., Zehnder, G.W., Baur, M.E., 2002. Potential for the use of elicitors of plant defence in arthropod management programs. Arch. Insect Biochem. Physiol. 51, 222235. Suarez, R., Wong, A., Ramirez, M., Barraza, A., del Carmen Orozco, M., Cevallos, M.A., et al., 2008. Improvement of drought tolerance and grain yield in common bean by overexpressing trehalose-6phosphate synthase in rhizobia. Mol. Plant Microbe Inter. 21, 958966. Swaine, E.K., Swaine, M.D., Killham, K., 2007. Effects of drought on isolates of Bradyrhizobium elkanii cultured from Albizia adianthifolia seedlings on different provenances. Agroforest. Syst. 69, 135145. Sziderics, A.H., Rasche, F., Trognitz, F., Sessitsch, A., Wilhelm, E., 2007. Bacterial endophytes contribute to abiotic stress adaptation in pepper plants (Capsicum annum L.). Can. J. Microbiol. 53, 11951202. Takahashi, R., Liu, S., Takano, T., 2007. Cloning and functional comparison of a high-affinity K1 transporter gene PhaHKT1 of salt-tolerant and salt-sensitive reed plants. J. Exp. Bot. 58, 43874395. Tanou, G., Filippou, P., Belghazi, M., Job, D., Diamantidis, G., Fotopoulos, V., et al., 2012a. Oxidative and nitrosative-based signaling and associated post-translational modifications orchestrate the acclimation of citrus plants to salinity stress. Plant J. 72, 585599. Tanou, G., Fotopoulos, V., Molassiotis, A., 2012b. Priming against environmental challenges and proteomics in plants: update and agricultural perspectives. Front. Plant Sci. 3, 216. Tchebotar, V.K., Kang Jr., U.G., Asis, C.A., Akao, S., 1998. The use of GUS-reporter gene to study the effect of Azospirillum-rhizobium co-inoculation on nodulation of white clover. Bio. Fert. Soil 27, 349352.

References

131

Thomashow, L.S., Weller, D.M., Bonsall, R.F., Pierson, L.S., 1990. Production of the antibiotic phenazine-1carboxylic acid by fluorescent Pseudomonas species in the rhizosphere of wheat. Appl. Environ. Microbiol. 56, 908912. Thomma, B.P.H.J., Eggermont, K., Penninckx, I.A.M.A., Mauch- Mani, B., Cammue, B.P.A., Broekaert, W.F., 1998. Separate jasmonate-dependent and salicylic acid-dependent defense response pathways in Arabidopsis are essential for resistance to distinct microbial pathogens. Proc. Natl. Acad. Sci. USA. 95, 1510715111. Uknes, S., Mauch-Mani, B., Moyer, M., Potter, S., Williams, S., Dincher, S., et al., 1992. Acquired resistance in Arabidopsis. Plant Cell 4, 645656. van Loon, L.C., 1997. Induced resistance in plants and the role of pathogenesis-related proteins. Eur. J. Plant Pathol. 103, 753765. van Loon, L.C., Bakker, P.A.H.M., Van der Heijdt, W.H.W., Wendehenne, D., Pugin, A., 2008. Early responses of tobacco suspension cells to rhizobacterial elicitors of induced systemic resistance. Mol. PlantMicrobe Inter. 21, 16091621. Van Peer, R., Niemann, G.J., Schippers, B., 1991. Induced resistance and phytoalexin accumulation in biological control of Fusarium wilt of carnation by Pseudomonas sp. strain WCS417r. Phytopathology 81, 728734. Vardharajula, S., Ali, S.Z., Grover, M., Reddy, G., Bandi, V., 2011. Drought-tolerant plant growth promoting Bacillus spp.: effect on growth, osmolytes, and antioxidant status of maize under drought stress. J. Plant Inter. 6, 114. Verbruggen, N., Hermans, C., 2008. Proline accumulation in plants: a review. Amino Acid 35, 753759. Vinocur, B., Altman, A., 2005. Cellular basis of salinity tolerance in plants. Environ. Exp. Bot. 52, 113122. Visca, P., Imperi, F., Lamont, I.L., 2007. Pyoverdine siderophores: from biogenesis to biosignificance. Trends Microbiol. 15, 2230. Vleesschauwer, D., Ho¨fte, M., 2009. Rhizobacteria-induced systemic resistance. Adv. Bot. Res. 51, 223281. Vlot, A.C., Klessig, D.F., Park, S.W., 2008a. Systemic acquired resistance: the elusive signal(s). Curr. Opin. Plant Biol. 11, 436442. Vlot, A.C., Liu, P.-P., Cameron, R.K., Park, S.-W., Yang, Y., Kumar, D., et al., 2008b. Identification of likely orthologs of tobacco salicylic acid-binding protein 2 and their role in systemic acquired resistance in Arabidopsis thaliana. Plant J. 56, 445456. Wang, Y., Li, L., Cui, W., Xu, S., Shen, W., Wang, R., 2012. Hydrogen sulfide enhances alfalfa (Medicago sativa) tolerance against salinity during seed germination by nitric oxide pathway. Plant Soil 351, 107119. Wasternack, C., Parthier, B., 1997. Jasmonate-signaled plant gene expression. Trends Plant Sci. 2, 302307. Wei, L., Kloepper, J.W., Tuzun, S., 1991. Induction of systemic resistance of cucumber to Colletotrichum orbiculare by select strains of plant growth-promoting rhizobacteria. Phytopathology 81, 15081512. Weller, D.M., Raaijmakers, J.M., McSpadden Gardener, B.B., Thomashow, L.S., 2002. Microbial populations responsible for specific soil suppressiveness to plant pathogens. Annu. Rev. Phytopathol. 40, 309348. Weller, D.M., Van Pelt, J.A., Mavrodi, D.V., Pieterse, C.M.J., Bakker, P.A.H.M., van Loon, L.C., 2012. Induced systemic resistance (ISR) in Arabidopsis thaliana against Pseudomonas syringae pv. tomato by 2,4-diacetylphloroglucinol (DAPG)-producing Pseudomonas fluorescens. Phytopathology 102, 403412. Weston, D.J., Pelletier, D.A., Morrell-Falvey, J.L., Tschaplinski, T.J., Jawdy, S.S., Lu, T.-Y., et al., 2012. Pseudomonas fluorescens induces strain-dependent and strain-independent host plant responses in defense networks, primary metabolism, photosynthesis, and fitness. Mol. Plant-Microbe Inter. 25, 765778. Whipps, J.M., 2001. Microbial interactions and biocontrol in the rhizosphere. J. Exp. Bot. 52, 487511. Wilhite, S.E., Lunsden, R.D., Strancy, D.C., 2001. Peptide synthetase gene in Trichoderma virens. Appl. Environ. Microbiol. 67, 50555062.

132


Yadegari, M., Rahmani, A., 2010. Evaluation of bean (Phaseolus vulgaris) seeds inoculation with Rhizobium phaseoli and plant growth promoting Rhizobacteria (PGPR) on yield and yield components. Afri. J. Agri. Res. 5, 792799. Yan, Z., Reddy, M.S., Ryu, C.M., Mc Inroy, J.A., Wilson, M., Kloepper, J.W., 2002. Induced systemic protection against tomato late blight elicited by PGPR. Phytopathology 92, 13291333. Yang, J., Kloepper, J.W., Ryu, C.-M., 2009. Rhizosphere bacteria help plants tolerate abiotic stress. Trend Plant Sci. 14, 14. Yang, Y., Zheng, Q., Liu, M., Long, X., Liu, Z., Shen, Q., et al., 2012. Difference in sodium spatial distribution in the shoot of two canola cultivars under saline stress. Plant Cell Physiol. 53, 10831092. Yazdani, M., Bahmanyar, M.A., Pirdashti, H., Esmaili, M.A., 2009. Effect of phosphate solubilization microorganisms (PSM) and plant growth promoting rhizobacteria (PGPR) on yield and yield components of corn (Zea mays, L.). World Acd. Sci. Eng. Techn. 49, 9092. Zahir, Z.A., Munir, A., Asghar, H.N., Arshad, M., Shaharoona, B., 2008. Effectiveness of rhizobacteria containing ACC-deaminase for growth promotion of peas (Pisum sativum) under drought conditions. J. Microbiol. Biotechnol. 18, 958963. Zamioudis, C., Pieterse, C.M.J., 2012. Modulation of host immunity by beneficial microbes. Mol. PlantMicrobe Inter. 25, 139150. Zhang, F., Dashti, N., Hynes, R.K., Smith, D.L., 1997. Plant growth promoting rhizobacteria and soybean [Glycine max (L.) Merr] growth and physiology at suboptimal root zone temperatures. Annu. Bot. 79, 243249. Zhang, H., Sekiguchi, Y., Hanada, S., Hugenholtz, P., Kim, H., Kamagata, Y., et al., 2003. Gemmatimonas aurantiaca gen. nov., sp. nov., a Gram-negative, aerobic, polyphosphate accumulating microorganism, the first cultured representative of the new bacterial phylum Gemmatimonadetes phyl. nov. Int. J. Syst. Evol. Microbiol. 53, 11551163. Zhang, H., Kim, M.S., Sun, Y., Dowd, S.E., Shi, H., Paré, P.W., 2008. Soil bacteria confer plant salt tolerance by tissue-specific regulation of sodium transporter HKT1. Mol. Plant-Microbe Inter. 21, 737744. Zhang, H., Murzello, C., Sun, Y., Kim, S., Xie, X., Jeter, R.M., et al., 2010. Choline and osmotic-stress tolerance induced in Arabidopsis by the soil microbe Bacillus subtilis (GB03). Mol. Plant-Microbe Inter. 23, 10971104. Zhang, Y., Fernando, W.G.D., 2004. Presence of biosynthetic genes for phenazine-1-carboxylic acid and 2,4-diacetylphloroglucinol and pyrrolnitrin in Pseudomonas chlororaphis strain PA-23. Can. J. Plant Pathol. 6, 430431. Zolla, G., Badri, D.V., Bakker, M.G., Manter, D.K., Vivanco, J.M., 2013. Soil microbiomes vary in their ability to confer drought tolerance to Arabidopsis. Appl. Soil Ecol. 68, 19. Zuń˜iga, A., Poupin, M.J., Donoso, R., Ledger, T., Guiliani, N., Gutiérrez, R.A., et al., 2013. Quorum sensing and Indole-3-Acetic acid degradation play a role in colonization and plant growth promotion of Arabidopsis thaliana by Burkholderia phytofirmans PsJN. Mol. Plant-Microbe Inter. 26, 546553.

CHAPTER

Arbuscular Mycorrhizal Fungi and Metal Phytoremediation: Ecophysiological Complementarity in Relation to Environmental Stress

6 Patrick Audet

6.1 Introduction Metal pollution1 represents an ongoing legacy of modern anthropogenic activities due to both the pervading and intensive use of fossil fuels and nonrenewable mineral resources across many (if not most) facets of contemporary industrial and agricultural development (Alkorta et al., 2004; Wuana and Okieimen, 2011). Within the context of mining and industrial manufacturing, increasing metals in the environment are generally derived from the refinement of crude/raw materials (e.g., smelting), the consumption of fuels (e.g., coal) during this processing, and the concomitant production of industrial wastewater and refuse materials both during initial extraction and later refinement. Similarly, in agriculture, the introduction of metal contaminants to agroecosystems usually stems from the application of chemical pesticides, livestock additives, and fertilizers; their potential redistribution in the form of recuperated sludge and biosolids; and their persistence in agricultural runoff. Upon their release into the environment (often in excess of their typical or naturally occurring concentration ranges), heavy metals persist in ecosystems based on their degree of chemical speciation and relative bioavailability. Depending on the metals in question and the biogeochemical properties of the growth substrate, metals are frequently taken up and potentially biomagnified by plants and animals, thereby exacerbating their detrimental effects across various trophic levels. Although metals and mineral nutrients being present and bioavailable within appropriate concentration ranges are essential components of metabolic functions, excess metal influx into the environment (e.g., into soils or aquatic systems) doubtlessly causes direct toxicity effects, as well as potentially inducing nutrient imbalances due to subsequent changes in the surrounding growth properties as a result of reciprocally antagonistic effects. Consequently, the burden of metal 1

In this analysis, metal contamination and metal pollution refer to excess or higher than tolerable concentrations of essential (e.g., Cr, Cu, Fe, Mn, Ni, and Zn) and nonessential (e.g., As, Cd, Co, and Pb) transition metals and metalloids in the environment. Historically, and throughout the field of environmental science and toxicology, metal pollutants have otherwise been commonly known as “heavy metals,” which is a term more strictly ascribed to particular transition metals “with atomic mass over 20 and specific gravity above 5” (Rascio and Navari-Izzo, 2011).


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pollution provides a considerable ecological challenge resulting in both direct and indirect impacts to ecosystem function affecting nearly all types of terrestrial and aquatic environments. For these reasons, the remediation of metal-contaminated environments (whether in the context of postindustrial or even agricultural landscapes) has, over recent decades, become a necessary focus of applied research efforts worldwide and now incorporates various components of ecotoxicology, environmental physiology, biogeochemistry, and soil microbiology.

6.1.1 Metal phytoremediation A defining advancement in the multidisciplinary field of bioremediation has been the identification and application of physiologically unique plants and allied species toward the colonization, stabilization, and even detoxification of degraded environments through the process of phytoremediation referring to the “plant remedy.” Evidently, phytoremediation research now comprises a variety of processes and mechanisms having the potential to limit and/or counteract the deleterious effects of metal pollution. The most common and well-studied mechanisms identified have been phytocentric,2 and these have primarily been classified based on the plants’ intrinsic abilities to directly take up and sequester (i.e., phytoextract) exceedingly high metal concentrations and total content in their above- and belowground tissues. Likewise, some complementary pedocentric approaches3 have then focused on strategies for chemically enhancing phytoextraction processes such as through the application of chelators and subsequent modification of edaphic parameters to increase metal availability to plants. As a result, biochemical pathways of plant uptake and phytosequestration are now well defined fromroots-to-shoots, even at the cellular and molecular scales, and attempts at applying such biotechnologies have been made at higher ecological scales based on this mechanistic understanding. Then again, these processes alone are not entirely conducive to the complete recovery of contaminated ecosystems and, as is often the case of natural ecosystem (Dickinson et al., 2009), the ability of most plants or crops to tolerate environmentally stressful conditions can be attributed as much to their intrinsic or constitutive physiological attributes (Baker and Walker, 1990) as to their ability to recruit various extrinsic interactions involved in these very same or complementary processes. From this rather holistic perspective (referring to the multilateral role of above- and belowground components within ecosystem function), recent investigative interests focusing on plants and their allied soilsymbionts would suggest an equally important and multilateral impact of soil microbes due to their ability to bind and precipitate (i.e., phytostabilize) excess metals in the root zone (Miransari, 2011; Audet, 2012, 2013; Meier et al., 2012a,b; Rajkumar et al., 2012; Zare-Maivan, 2013). Thus, this should attest to the complexity of natural systems and the evolutionary context underpinning their resilience in relation to environmental stressors (van der Heijden et al., 1998; 2003). One such emerging and widely investigated biotechnology for the management of plants in relation to biotic and abiotic stresses is the mycorrhizal symbiosis referring to “fungus roots” that are “living together” (Boucher et al., 1982; Leung and Poulin, 2008). This ancient mutualistic association between soil fungi and vascular plant roots represents a dynamic and ecologically diverse 2

For more comprehensive details, refer to the general review by Pilon-Smits (2005) and recent topical reviews by Miransari (2011), Rascio and Navari-Izzo (2011), Bhargava et al. (2012), Rajkumar et al. (2012), and Ali et al. (2013) regarding phytoextraction, phytofiltration, phytovolatilization, phytorhizodegradation, and phytodesalination. 3 For more comprehensive details refer to Kahn et al. (2000), McGrath and Zhao (2003), Lasat (2002), Lebeau et al. (2008), Lestan et al. (2008), Evangelou et al. (2007), and Hassan and Aarts (2011).

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interaction that plays a critical role in plant nutrition and soil stabilization across a range of environmental conditions (Koide, 1991, 1993), including metal/nutrient deficiency and toxicity (Leyval et al., 1997; Gu¨hre and Pazkowski, 2006). Representing a major component in the structure and fertility of soils (van der Heijden et al., 1998, 2003), mycorrhizal fungi are well recognized as contributing to both the enhanced uptake of macronutrients (i.e., nitrogen and phosphorus) and limiting trace/metal nutrients under environmentally deficient growth conditions. At the opposite end of the spectrum of environmental stress, mycorrhizal fungi can bind metals and limit their translocation to mitigate the effects of nutrient toxicity (Corradi and Charest, 2011). As evidenced across a range of investigative contexts, these combined properties have commonly been suggested as being beneficial components in the functioning and recovery of metalcontaminated ecosystems, and many authors have suggested that mycorrhizal associations could be harnessed within the context of multilateral phytoremediation strategies to facilitate more effective recovery of affected systems (Joner et al., 2000; Miransari, 2011; Audet, 2012; Meier et al., 2012a,b; Rajkumar et al., 2012; Zare-Maivan, 2013). Indeed, such multilateral processes (albeit sometimes benign depending on environmental conditions) are critical to the functioning of natural ecosystems and, when combined with intrinsic plant stress-tolerance properties (e.g., phytoextraction and hypertolerance), could increase phytoremediation efficiency (Meier et al., 2012a,b; Pongrac et al., 2013). However, proportionally less emphasis has been placed on the potential ecological and evolutionary boundaries that could prevent any such synergy. Whereas biogeochemical mechanisms surrounding plantsoil interactions in relation to metal stress have, for the most part, been well covered in the peer literature (Miransari, 2011; Meier et al., 2012a,b; Rajkumar et al., 2012), the purpose of this analysis is to identify and summarize these beneficial processes and to elaborate on plantphysiological investigations (i.e., stemming primarily from greenhouse study) hopefully to facilitate their application in the field.

6.1.2 Objectives Focusing especially on the arbuscular mycorrhizal (AM) fungi, the most widely investigated form of mycorrhizal symbiosis within the context of both crop production and metal phytoremediation, a large portion of this chapter is dedicated to examining the primary mechanisms by which plantsoil interactions shape plant stress tolerance in relation to metal stress (i.e., from deficiency to toxicity conditions). It also further outlines how these properties could be applied to the phytoremediation of metal-polluted environments. Core mechanisms to be addressed include: enhanced metal/nutrient uptake, metal/nutrient biosorption and precipitation, and soil particulate micro- and macroaggregation. Here, biochemical pathways and plant physiological effects are emphasized especially within the context of metal-contaminated environments. The second portion of this chapter examines the combined and multilateral effects (just described) in a combined ecophysiological depiction of the dynamics of AM-symbiosis as a function of plant metal stress tolerance. In doing so, some of the ecophysiological boundaries in upscaling these processes are discussed, particularly relating to the cost of maintaining the symbiotic infrastructure of the mycorrhizal fungi; and the burden of metal stress that imposes significant limitation as to the viability and efficacy of these processes at the scale of remediating degraded landscapes. Whereas these attributes could be highly favorable in improving the efficiency of metal phytoremediation, it may arise that the integration and application of AM fungi as a field-scale

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biotechnology in the phytoremediation of metal-contaminated environments may not be as fluid and/or as directly achievable as once believed (Neagoe et al., 2013). In all likelihood, these processes may have beneficial implications for environmental remediation practices, as recently proposed by Anastasi et al. (2013), Danesh et al. (2013), Jafari et al. (2013), and Sepehri et al. (2013). Yet, the successful integration of any such processes into field-level applications hinges on identifying and then accounting for boundaries set by biogeochemical conditions of metal-contaminated environments and the ecophysiological factors underpinning plantsoil interactions.

6.2 Arbuscular mycorrhizal fungi and plant stress tolerance Having appeared at least 450 million years ago (according to the fossil record), and putatively stemming from both parasitic and saprophytic origins (Purin and Rillig, 2008), the AM symbiosis is an ancient and ubiquitous interaction occurring between numerous fungal species of the Glomeromycota phylum and an estimated (and possibly greater than) 90% of all herbaceous plants (Remy et al., 1994; Redecker et al., 2000; Schu¨ßler et al., 2001). A defining feature of this and all other types of mycorrhizal symbioses (Peterson et al., 2004) is the development of the mycorrhizosphere (Figure 6.1a). This biological sphere of interaction consists of the combined zones of influence of the roots (rhizosphere) and extra radical hyphae (hyphosphere). It encompasses a highly active and multilateral interface between the host plants, AM-fungi, and the proximal soil environment (Garbaye, 1991; Duponnois et al., 2008). Fundamentally, the symbiosis is believed to develop because the photosynthetic capacity in plant shoots exceeds the uptake capacity and/or soil nutrient supply to support plant growth. Plant investment toward the development of the mycorrhizospheric network involves a considerable plant carbon allocation and occasionally represents up to and possibly more than 20% of the plant’s total carbon budget depending on environmental conditions. This carbon exchange is required to actively sustain the symbiotic infrastructure and maintain the functional viability of the mycorrhizal symbiont (Schwab et al., 1991; Tinker et al., 1994; Douds et al., 2000). In exchange, this extrinsic investment of photosynthates provides the host plant with a number of beneficial ecophysiological services typically pertaining to the enhancement of the plant’s resource-acquisition capability and the stabilization of its proximal soil environment (Brussaard et al., 2007). For the purpose of distinguishing these mechanisms and their impact on the host plant and/or the proximal growth environment, Audet (2012) refers to the benefits of symbiotic associations as being either direct or indirect. As it should become more apparent further into this chapter, direct benefits of the interaction stem from processes mediated directly from the bidirectional exchange of resources between both symbionts. For example, the transfer of soil nutrients by the AM fungus in exchange for plant carbohydrates. To the contrary, the indirect benefits of the interaction stem from peripheral processes that impact conditions or circumstances of the proximal growth environment that may indirectly benefit the host plant but also adjacent species (e.g., the modification of soil nutrient solubility or stabilization of the soil matrix). The AM symbiosis is a highly dynamic association due to its adaption to and successful colonization of nearly all known terrestrial ecosystems, then implying a wide range and variety of environmental conditioning. It is within this context that the symbiosis has been extensively studied across the fields of plant physiology and soil microbiology, and it is widely recognized for

6.2 Arbuscular mycorrhizal fungi and plant stress tolerance

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FIGURE 6.1 Conceptual summary of energy flows underpinning the mycorrhizal symbiosis (a) distinguishing the rhizosphere, hyphosphere, and mycorrhizosphere soil environments. Mechanistic depictions of (b) enhanced metal/nutrient uptake, (c) metal/nutrient biosorption and precipitation, and (d) soil particular micro- and macroaggregation are shown according to Audet (2012).

benefiting both plant and AM-fungal symbionts (or partners) when subjected to various environmental stressors, notably including drought, nutrient deficiency, and metal toxicity. Unlike other forms of mycorrhizal symbiosis, the AM fungi4 are ecologically unique given their status as obligate symbionts, meaning that they are dependent on successful colonization of the 4

When compared to other forms of mycorrhizal symbiosis (refer to the comprehensive morphological investigation by Peterson et al., 2004), the AM fungi are morphologically characterized by the formation of an intra- and extraradical mycelium (i.e., coenocitic/aseptate hyphae) acting as “root” analogues, arbuscules representing the primary rootfungal interface (along with intraradical hyphae), vesicles acting as energy storage structures, and thick-walled spores representing the fungi’s reproductive unit.

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plant host and viable formation of the mycorrhizosphere to complete their life cycle (Johnson et al., 1997; Jones and Smith, 2004). Otherwise, the fungi remain in a dormant stage until a suitable plant host and appropriate environmental conditions facilitate the early biochemical stages of spore germination, fungalroot, recognition, colonization, and so on (Koide, 2000; Mendgen and Hahn, 2002; Vierheilig and Piché, 2002; Harrison, 1999, 2005). Whereas the same cannot strictly be said of the plant host being an obligate symbiont, there is ample evidence indicating that native and/or endemic plant species rely on particular AM fungi and soil microbial profiles for their growth and that these relationships constitute a veritable mutualism (Schwartz and Hoeksema, 1998; Janos, 2007). These associations have then been found to contribute in shaping above- and belowground biodiversity patterns at larger scales of species assembly and ecosystem function.5 As mentioned previously, AM-mediated processes having particular implications for metal phytoremediation can be grouped and depicted generically as being either direct or indirect, and these typically include the processes of enhanced metal/nutrient uptake (Figure 6.1b), metal/nutrient biosorption and precipitation (Figure 6.1c), and soil particulate micro- and macroaggregation (Figure 6.1d). Over the past three decades, plant and soil scientists have provided an advanced understanding of these mechanisms (described in more detail later), through cellular and molecular analyses and corroboration mostly at the scale of comparative physiological assessments of greenhouse and field-trial grown plants.

6.2.1 Enhanced metal/nutrient uptake Plant productivity (both within the context of natural and agricultural systems) is generally limited by the availability of nitrogen and/or phosphorus (Vilousek and Howarth, 1991; George et al., 1995; Fitter et al., 2011) and, of course, depending on climate, geography, and soil type. Deficiency of either of these macronutrients is known to result in stunted plant growth and other general symptoms of suboptimal metabolic function (Mengel et al., 2001; Cleveland et al., 2002). The role of AM fungi in the acquisition of N and P has been well described across various stages of nutrient acquisition, notably from fungal assimilation to symbiotic exchange with host plants, including known transporters and enzymes (Schachtman et al., 1998; Jin et al., 2005; Chalot et al., 2006; Govindarajulu et al., 2005; Javot et al., 2007). This represents a major fundamental contribution to our understanding of the AMplant relationship and, more generally, to the direct benefits of symbiotic association. However, for the purposes of this analysis (i.e., within the context of metal/nutrient uptake and metal phytoremediation), we focus more intently on micronutrient (metal) uptake. Analogous to the processes of AMplant N and P acquisition, there is a considerable body of literature describing the beneficial role of AM fungi in relation to soilmetal deficiency conditions (Blinkley and Vitousek, 1989). In this regard, it has been suggested that this up-regulation of macronutrient uptake could be a response to actual limiting/deficiency conditions or even as a response to metal-induced soil nutrient imbalances stemming from altered edaphic conditions (e.g., pH, nutrient-holding capacity, or porosity) and/or metal/nutrient influx (e.g., pollution or fertilizer 5

A number of pioneering works by Bever et al. (1997), Wardle et al. (1998, 2004), Bever (1999, 2003), Klironomos (2002) have identified unique AM fungal profiles in relation to native or endemic plants and subsequent feedback between above- and belowground species. This feedback is thought to shape the broader assembly of biodiversity and possibly even ecosystem function.


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amendment). Geographically, the metal deficiency soil nutrition scenarios can be naturally occurring among temperate environments (having alfisols and vertisols) or similarly alkaline soils as well as tropical environments (having ultisols and oxisols), and such deficiencies can be exacerbated by long-term weathering and seasonal erosion. Meanwhile, under conditions of excess or higher than average metal concentrations (e.g., those found among metal-contaminated environments), metal-induced deficiencies can also arise as a result of mutual antagonisms, referring to changes in soilmetal bioavailability due to the preferential uptake of competing metal ions. As shown in Figure 6.2, the AM-mycorrhizosphere enables plants to circumvent the challenges of metal/nutrient deficiency by increasing the resource uptake capacity of the rhizosphere alone (Schwab et al., 1991; Eckhard et al., 1994; Marschner, 1995; Liu et al., 2000). This is achieved by increasing the roots’ resource-acquisition zone due to nutrient scavenging by the expansive hyphosphere, but also by greater nutrient uptake efficiency within the mycorrhizosphere due to the exudation of organic chelators (Cahill and McNickle, 2011). This facilitates both active

FIGURE 6.2 Generalized biochemical pathway for mycorrhizal-enhanced metal/nutrient uptake from the soil solution, to the mycorrhizal hyphae (intra- and extraradical mycelium) and then to the roots. Source: Pathway adapted from Meharg (2003); modified according to Gu¨hre and Pazkowski (2006) ´ and Gonzalez-Guerrero et al. (2009).

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and passive transport of metalchelator complexes from the soil environment, through the fungal mycelium, to the host root cells. A commonality in the biochemical mechanisms of action seems to exist for the uptake of most metals and metalloids, as covered in research reviews by Meharg (2003), Gu¨hre and Pazkowski (2006), and González-Guerrero et al. (2009). This generalized pathway is significant because it involves the exudation of organic chelators into the soil solution, the active uptake of chelated-metal complexes, and subsequent transfer of these metals via glutathione S-transferases within the fungal mycelium. The metals are then exchanged with and ultimately assimilated by host plants and also sequestered via the internal complexation of metal ions (i.e., due to metallothione in binding). These latter processes seem to enable the “packaging” of less reactive metal complexes and to facilitate fungal storage into vacuolar compartments as well as integration into the fungal metabolism. Molecular investigative approaches have accurately corroborated this depiction as indicated by the up-regulation of fungal membrane transporters, metallothein in proteins, and glutathione complexes in fungal tissues when subjected to increasing metal/nutrient exposure (González-Guerrero et al., 2005, 2007, 2009, 2010a,b; Lo´pez-Pedrosa et al., 2006). As such, ongoing assessments of these pathways are anticipated to contribute in populating nearly the entire sequence of fungal uptake, assimilation, and transfer to host roots; this understanding appears to support a comodulation of metal uptake and transfer depending on environmental conditions (Burleigh et al., 2003; Lo´pez-Millán et al., 2004; Hassan et al., 2011), then having important affects for host plant tissue development (Aloui et al., 2011; Garg and Aggarwal, 2012; Zitka et al., 2012; Hassan et al., 2013). Reciprocally, photosynthates in the form of hexose are exchanged across the plantfungal periarbuscular interface to be allocated to the intra- and extraradical mycelium carbon pool that then defines the mutualism. Of course, estimates of mycorrhizal nutrient uptake efficiency (i.e., the relative effect of mycorrhizal colonization toward host plants as a percentage of the ratio of effects on nonmycorrhizal individuals subjected to the similar conditions) may vary depending on soil nutrient availability and plant investment in the mycorrhizosphere. Nevertheless, numerous studies (e.g., Eckhard et al., 1994; Marschner, 1995; Liu et al., 2000) have commonly reported up to 25 to 50% greater nutrient uptake, resulting in variably improved physiological status among plants. Indeed, a high proportion of available literature primarily supports the mechanism of enhanced plant nutrition under deficiency conditions and this perspective justifiably dominates public perception as to the essential role of AM fungi in ecosystem function. There are indications, however, that these effects should continue to be beneficial even across the entire spectrum of metal exposure from deficiency even to toxicity conditions. Although it may appear anachronistic that AM fungi could, in principle, grossly increase the uptake of toxic metals leading to detrimental plant physiological effects, the fact that the extraradical and intraradical hyphae are actively involved in packaging metals for transport throughout the fungal mycelium and transfer to the host plant may be indicative of a highly selective mutualism that prevents any such issues (González-Guerrero et al., 2009). Indeed, this selective uptake and transfer of limiting metal nutrients is also beneficial under excess metal exposure conditions due to the implications of metal imbalances arising in the rhizosphere. That being said, examination of further indirect benefits of the associations, relating primarily to its role in metal/nutrient biosorption and precipitation, reveals an alternative mechanism leading to metal stress avoidance (i.e., a lesser metal stress burden) when subjected to toxic conditions.


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6.2.2 Metal/nutrient biosorption and precipitation Notwithstanding the direct benefits of AM symbiosis in plant resource acquisition for which the association is more famously known (e.g., N and P uptake described by others and metal/nutrient uptake described earlier), the mycorrhizosphere perhaps plays a more significant role in metal phytoremediation by stabilizing the proximal growth environment. These indirect benefits refer to mechanisms that are not directly mediated by bidirectional transfer between the symbionts yet still dramatically benefit plant growth, particularly in relation to environmental stress. In many ways, these indirect benefits are inextricably intertwined with direct benefits and provide complementary processes, for example, to nutrient acquisition albeit in the peripheral growth environment. However, when assessed individually or from strictly reductionist perspectives, they can appear perplexing in the classic depiction of mutualism due to their somewhat altruistic ecological outcomes toward nonhosts (Boucher et al., 1982; Leung and Poulin, 2008; Pongrac et al., 2013). Nevertheless, specific to the context of metal phytoremediation, a rather beneficial attribute of the AM symbiosis is the modulation of soil metal/nutrient bioavailability via mycorrhizospheric metal/nutrient biosorption and precipitation (González-Chavez et al., 2002; González-Guerrero et al., 2008). As illustrated in Figure 6.2, these attributes are due primarily to the biochemical properties at the surface of the roots and fungal mycelium (Gadd, 1993; Galli et al., 1994) and occur as by-products of mycorrhizal proliferation in the soil solution. The metal-binding capacity of soil (then contributing to its nutrient holding properties) is primarily dictated by its essential composition, whereby soils having a higher proportion of organic matter (e.g., humic and fluvic acids) typically have a greater metal/nutrient retention capacity and redox potential (McBride, 1994). Roots and fungal hyphae (being organic tissues) increase metal/ nutrient biosorption due to their preferential binding of metal ions to negatively charged surface constituents, including carboxyl, hydroxide, oxy-hydroxide, and sulfhydryl groups (Gadd, 1993; Galli et al., 1994; Leyval et al., 1997). Analyses strictly comparing mycorrhizospheric versus rhizospheric and bulk soil environments suggest that phenolic polymers and melanins should also represent effective binding sites (Fogarty and Tobin, 1996). Meanwhile, spatial visualization investigations by González-Chavez et al. (2002) have helpfully localized these processes throughout the mycorrhizosphere, thereby corroborating the importance of this mechanism in regulating soilmetal concentrations. As such, the basic proliferation and enmeshment of roots and hyphae in soils is sufficient to alter soil nutrient-holding properties versus bare/bulk soils (Leyval et al., 1997; Giller et al., 1998). Active exudation of organic chelators (e.g., those described earlier as being involved in AM-enhanced metal/nutrient uptake) likely also play a role in the formation of metalligand complexes that could then precipitate in the soil solution or, instead, be taken up by roots and hyphae depending on environmental conditions and nutrient demand. Under nonstressful (or optimal) soil nutrient conditions, the combined processes of AMenhanced metal uptake (see Figure 6.2) and AM-metal biosorption and precipitation (Figure 6.3) would demonstrate the close modulation of nutrient availability and uptake by plants. Meanwhile, under excess metal conditions, AM metal binding often buffers the soil environment by tempering and offering phytoprotective effects of metal toxicity and nutrient imbalances (Rangel et al., 2013). In this particular case, and as shown later on with examples from Audet and Charest (2006, 2009,

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2010a, 2013), AM metal binding can significantly reduce excess and potentially harmful metal uptake up to 50%, thereby reducing the burden of metal stress corresponding with greater health status in the host plants; this has been shown by many authors for both essential and nonessential metals across a wide range of plant and fungal species (refer to reviews by Christie et al., 2004; Hildebrandt et al., 2007; Cavagnaro et al., 2010). As such, beneficial effects often correspond to plants having a higher investment (or levels of AM-root colonization) than control plants. Consequently, plant investment in the mycorrhizosphere under metal toxicity conditions has been suggested to represent an extrinsic stressavoidance mechanism that could complement known intrinsic plant detoxification mechanisms (e.g., metallothienin and phytochelatin metabolisms) (Cobbett, 2000; Cobbett and Goldsbrough, 2002). This is in order to externally regulate (albeit passively) the toxicity of metals found in the proximal growth environment, and thereby reduce oxidative stress in plant tissues (Schu¨tzendu¨bel and Polle, 2002).

FIGURE 6.3 Generalized biogeochemical pathway for metal/nutrient biosorption and precipitation by roots and/or extraradical hyphae. Source: Pathway adapted from Bradl (2004), Gadd (1993), Galli et al. (1994), ´ ´ Gonzalez-Chavez et al. (2002), and Gonzalez-Guerrero et al. (2008).


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6.2.3 Soil particulate microaggregation Coinciding with the effects of mycorrhizal metal binding, the final mechanism of interest regarding AM symbiosis in metal phytoremediation again relates to the role of the mycorrhizosphere in stabilizing the soil matrix via mycorrhizal-induced soil aggregation (Figure 6.4). In this regard, the proliferation of the mycorhizosphere implies the penetration of roots and fungal hyphae into soil micropores to then significantly enhance the soil’s aggregation properties and subsequently improve water retention and nutrient-holding capacity (Beare et al., 1995; Rillig and Mummey, 2006; Rillig et al., 2010). In fact, the greater degree of mycorrhizal branching and ramification produces localized forces that facilitate the formation of microaggregates due to the alignment of soil particulate matter and then the formation of macroaggregates due to mycorrhizal enmeshment (Miller and Jastrow, 1990; Piotrowski et al., 2004; Rillig and Mummey, 2006). In both cases, the soil matrix

FIGURE 6.4 Generalized depiction of soil particulate micro- and macroaggregation. Enhancement of soil matrix structure and nutrient/resource holding capacity is shown with emphasis on the processes of hyphal exudation (e.g., leading to pH modification and microbial recruitment), alignment of soil particles (e.g., microaggregation), and hyphal enmeshment (e.g., macroaggregation). Source: Pathway adapted from Miller and Jastrow (1990) and Rillig and Mummey (2006).

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structure is bolstered leading to enhanced resilience in relation to, for example, soil drying, flooding, compaction, and/or nutrient leaching/erosion (Augé, 2004), not to mention further effects associated with AM metal-binding and nutrient-holding capacities. Although enhanced soil structure properties are not exclusive to the AM fungi (Gadd, 1993), comparisons of mycorrhizosphere and hyphosphere environments versus rhizosphere and bulk soil environments (as discussed before) putatively associated increased soil aggregation with greater physical entanglement of roots, hyphae, and soil (Beare et al., 1995). These processes are believed to be facilitated by the exudation of root mucilage as well as the production of glomalin- and glomalin-related proteins by fungi that, together, increase soil clustering (Purin and Rillig, 2008). Given the combined effects of soil clustering, particulate alignment and microaggregation, and finally mycorrhizal enmeshment, the mycorrhizospheric network would appear to supply an essential soil “skeletal” structure that enhances nutrient-holding capacity and water retention, which would certainly prove to be beneficial under environmental stress. The physiological consequences of these processes to host plants have primarily been demonstrated in regard to plantwater relationships and, more specifically, drought stress and drought recovery due to their direct impact on soil water-holding capacity and relative moisture. In other words, these aggregates increase water infiltration due to the more hydratable (or water stable) soil matrix compared to bulk soil (Rillig et al., 2010). Then again, retention of water (along with pH) also directly impacts soil nutrient bioavailability, therefore AM-induced soil aggregation should have generally beneficial attributes that indirectly shape edaphic conditions in favor of plant hosts (Fourest and Roux, 1992). Another consequence of mycorrhizal proliferation and the exudation of root mucilage and fungal glomalin-related compounds is the localized micromodification of pH and active recruitment of allied soil microbia (Newsham et al., 1995; Brussaard et al., 1997; Wardle et al., 1998, 2004; Bonfante and Anca, 2011). These rather subtle changes may not drastically alter nutrient uptake patterns or soil bioavailability to the extent of impacting plant physiological attributes, per se, but they are still believed to shape soil abiotic and biotic profiles in favor of host plants. Works by Fitter and Garbaye (1994), Andrade et al. (1997), Bianciotto and Bonfante (2002), and Frey-Klett et al. (2007) identified a remarkable microbial subflora associated especially with the AM fungi themselves, implying further recruitment of soil microflora. In this regard, it has been suggested that some soil microbes could act as mycorrhiza helpers and that they could be intrinsically involved in the promotion of mycorrhizospheric development and general function of the mycorrhizal symbiosis (Garbaye, 1994; Barea et al., 2005; Frey-Klett et al., 2007), aspects certainly deserving of more in-depth analysis. Even though any decisive or predominant mechanisms as to their role in the symbiosis have yet to be determined, it is still apparent that mycorrhizal proliferation and exudation should have a localized impact on edaphic properties including metal/nutrient solubilization, aggregation, and so on. In turn, these cumulative impacts are suspected to alter aboveground patterns and processes, and thereby shape composition of vegetation. Indeed, it would seem that these processes (albeit incompletely defined at present) would complement each of the processes of AM-enhanced metal/ nutrient uptake and metal binding described previously. Thus, the combined and cumulative effects of these respective mechanisms should highly benefit host plant growth and development across the entire range of metal exposure, that is, from deficiency to toxicity conditions.

6.3 Adopting arbuscular mycorrhizal plants into metal phytoremediation

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6.3 Adopting arbuscular mycorrhizal plants into metal phytoremediation When addressed individually and primarily from a reductionist perspective (as before), the various mechanisms of AMplantsoil interactions provide a unique and in-depth assessment of the inextricably intertwined role of the mycorrhizal symbiosis in plant physiological and ecological function, even up to the scale of biochemical and molecular pathways. Indeed, many of these properties could have considerable implications when applied in the purpose of metal phytoremediation or as agricultural biotechnologies. Then again, it is only by assessing these processes from a combined and multilateral perspective that the true dynamics of this association are shown in relation to environmental stress. Given the interplay between mycorrhizal-enhanced uptake and metal biosorption, the role of the AM symbiosis in metal stress (and metal phytoremediation) may sometimes appear antagonistic, particularly since one mechanism is known to increase metal uptake whereas the other reduces it. However, when combined, these properties seem to represent rather plastic or readily adaptable mechanistic attributes of the association when subjected to changing environmental conditions. One such conceptual perspective was first proposed by Audet and Charest (2007a,b) based on meta-analyses of available metal phytoremediation literature and subsequent investigative analysis specifically using targeted experimental design strategies (Audet and Charest, 2009, 2010a; Audet and Charest, 2013). To summarize classic and widely accepted depictions of plant metal/nutrient uptake, growth response, and physiological status (e.g., Epstein, 1972; Foy et al., 1978), plants respond rather predictably and consistently to increasing soil metal exposure punctuated by distinct ranges of nutrient deficiency, adequacy, and then luxury and toxicity conditions (Figure 6.5a). As is the case for all plants, optimal physiological development occurs when sufficient macro- and micronutrients and water are available and in proportional balance to one another. Evidently, if any of these soil resources are too few to meet the plant’s essential metabolic requirements, its physiology typically expresses growth stunting and/or chlorosis; this being the case equally under conditions of macro- or micronutrient deficiency. At the opposite end of the soil metal exposure spectrum, symptoms of growth stunting, chlorosis, and/or necrosis arise under toxicity conditions; again, this being the case equally whether under conditions of macro- or micronutrient toxicity as well as nonessential metal toxicity. Consequently, the relative growth profile (expressed as the percentage of the maximum growth potential) is generally parabolic, whereby local adaption and variation of plant species (i.e., resulting in varying degrees of plant stress tolerance) will result in subtle changes in this pattern. The impact of AM fungi on these profiles is rather dynamic given the dual mechanisms of mycorrhizal-enhanced uptake and then metal biosorption (Figure 6.5b). At the deficiency end of the spectrum, mycorrhizal nutrient scavenging is often sufficient to increase the plant’s resource uptake capacity to supplement its essential metabolic requirements. Meanwhile, when subjected to metal toxicity conditions, metal biosorption can significantly decrease uptake and thereby reduce the plant’s metal toxicity burden. The resulting AMplant growth profile implies that the beneficial effects of the mycorrhizal fungi on growth (e.g., nutrient supplementation and metal stress avoidance) are most apparent at either end of the metal exposure range, depending on the plant’s investment in mycorrhizal infrastructure. Meanwhile, under seemingly less stressful environmental conditions, such as having adequate or luxury nutrient available, mycorrhizal effects can be negligible or perhaps even benign. This does

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FIGURE 6.5 Summary of (a) plant metal uptake and growth response and (b) putative mycorrhizal effects. Source: Schema adapted from Audet (2012) and Audet and Charest (2007a,b, 2008).

not mean that the AM symbiosis is necessarily inactive, but rather that the benefits of mycorrhizal association may be offset by the cost of maintaining the symbiosis. Overall, these processes result in both dynamic plant metal uptake and growth response profiles that are likely to be tempered by local variation, intrisinc plant stress tolerance, and extrinsic plant investment in AM symbiosis (among other beneficial soil microbial processes). Of course, this depiction is merely hypothetical. Then again, since this model is based on meta-analyses of well-known processes, the depiction is a suitable starting point for further investigation and, so far, accommodating of the latest findings and minor variations associated with different experimental designs, and so on.

6.3.1 Plantsoil experimental perspectives Demonstratively and being representative of many similar greenhouse experimental design conditions across the field of plant ecophysiology (e.g., Li and Christie, 2001; Christie et al., 2004; Cavagnaro, 2008; Cavagnaro et al., 2010), compartmental-pot greenhouse experiments (Figure 6.6), such as those by Audet and Charest (2006, 2010a,b, 2013), have proven effective in distinguishing the effects of AM-enhanced nutrient supplementation and metal stress avoidance, as well as


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FIGURE 6.6 Schema of compartmental-pot system showing (a) the central root compartment (CC) and peripheral ´ treatment compartment (PC) for roots and/or hyphae. The precis further indicates the proliferation of (b) roots only (rhizosphere), (c) roots and hyphae (mycorrhizosphere), and (d) extraradical hyphae only (hyphosphere). Source: Based on Audet and Charest (2010a).

comparing the role of roots and/or hyphae in modulating the soil environment. In this instance, a key attribute of the compartmental-pot system is that different belowground “spheres of influence” (e.g., rhizosphere, mycorrhizosphere, and hyphosphere) can be separated to compare the relative effects of roots and/or hyphae toward plant physiological and edaphic factors. Although such studies are no substitute for field trials and the complexity of whole ecosystems, comparing root and/or hyphal effects in relation to increasing metal-exposure levels (often of single metal/micronutrient doses ranging from low to high concentrations) contributes especially in expanding our understanding as to the multilateral role of AM symbiosis in plant growth and development. Here, using zinc (Zn) as a typical metal nutrient and environmental contaminant,6 it has been shown how the mycorrhizosphere (implying roots and hyphae) reduces metal uptake up to 50% (Figure 6.7) compared to the rhizosphere (roots only) to then reduce the burden of metal toxicity when subjected to potential toxic metal concentrations (e.g., .200 ppm). This is a considerable reduction in metal stress that, in this case, decreased the incidence of leaf chlorosis and provided a growth advantage for AM versus non-AM plants. What is more, and as predicted from the perspective that AM fungi actively increase nutrient uptake even when subjected to moderate- to highnutrient/metal exposure levels, hyphosphere treatments (implying hyphae only) also increased 6 That is, Zn is en essential micronutrient that can reach phytotoxic concentrations. When used for study in plant ecophysiological assessments, deficiency and toxicity effects can be drawn out across a wider exposure range compared to more acutely toxic metals (Barceloux, 1999).

FIGURE 6.7 Metal (Zn) concentrations found in “dwarf” sunflower (Helianthus annuus): (a) flower, (b) shoot (leaves and stems), and (c) root portions are shown. Mean (n 5 4) and standard errors for the rhizosphere (black), mycorrhizosphere (gray), and hyphosphere (white) treatments are shown. Shared letters designate treatments that are not significantly different according to ANCOVA coupled with Bonferonni and Scheffe´ mean comparison tests (P , 0.05). Source: Data from Audet and Charest (2010a); refer to this study for experimental details.


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uptake for host plants across the entire range of soilmetal exposure (from deficiency to toxicity conditions). That is to say, host plants that did not otherwise have direct access to these soil resources via the roots still accessed soil resources via fungal hyphae. These basic findings support the widely held view that mycorrhizal symbiosis should play a dynamic role in plant resource acquisition depending on environmental conditions, and that a fundamental understanding of the complexity of these relationships has yet to be fully characterized. Overall, within the context of phytoremediation, the effects of AM-enhanced metal biosorption often predominate treatment comparisons, whereas benefits of AM-enhanced uptake under “deficiency” conditions often appear negligible. Admittedly, this is often due to experimental design approaches that overemphasize metal toxicity outcomes (e.g., greater treatment range approaching toxicity conditions) while providing insufficient analysis of veritable deficiency (i.e., the soils and fertilizers used under experimental conditions typically contain sufficient essential nutrients to overcome any plant deficiency symptoms). Doubtlessly, more careful assessment of limiting metal/ nutrient availability ranges would permit a better depiction of AM-enhanced nutrient uptake across the entire range of metal exposure from deficiency to toxicity conditions. Nevertheless, available greenhouse study outcomes still indicate the dual mycorrhizal effects of enhanced uptake and metal biosorption mechanisms, and support the notion that these should occur simultaneously and/or independently from one another to then shape AM versus non-AM plantmetal uptake profiles. Likewise, and as alluded to in previous sections, mycorrhizospheric and hyphospheric effects are not limited to the physiology of plants. As for the soil conditions, increasing metals (Figure 6.8) can cause soil pH (Figure 6.9) to decrease, depending on the form of metal amendment; in this case, this is likely due to the proportional increase of conjugate acid bases in the soil solution. In the context of greenhouse pot studies in which plants are regularly watered and amended with mild fertilizers, the influx of SO422 (i.e., Zn is often applied in the form of ZnSO4 in fertilizers) and H1/H3O1over time alters the soil’s redox equilibrium and inevitably impacts the solubility of metal nutrients (Li and Christie, 2000)—referring to the process of “metal ageing” (Lock and Janssen, 2003)—and thereby altering the soil’s metal-binding properties (Ross, 1994; Chuan et al., 1996; Tack et al., 1996; Martinez and Motto, 2000). Evidently, under greenhouse experimental conditions, differences in the patterns and profiles of edaphic properties for rhizosphere, mycorrhizosphere, and hyphosphere environments are mostly attributable to the different rates of metal uptake and the subsequently different soilmetal depletion zones between roots and/or hyphae that can be found in the relatively small volume of homogeneous soils available in pots. However, once these conditions/patterns are accounted for, the presence of roots and/or hyphae has been shown to clearly alter the soilpH and soilmetal bioavailability profiles, presumably due to the multilateral effects discussed previously of root/hyphal exudation, metal-complexation, uptake, and so on. These effects have been closely correlated with high incidences of root colonization as indicated by the abundance of fungal hyphae, arbuscules, and vesicles (Audet and Charest, 2013) and this was found particularly in the foremost layers of soil (i.e., top 10 cm) that often represent the most bioactive soil strata for mycorrhizal symbioses. As in the case of phosphorus and nitrogen acquisition by mycorrhizae (Gahoonia and Nielsen, 1992; Eckhard et al., 1995; George et al., 1995; Bago et al., 1996), it has been suggested that hyphal exudates can induce the moderate alkalinization of the soil environment, whereas roots tend to acidify it. This may be relevant since microalterations caused by hyphal exudates that could promote alkalinization of the proximal soil environment may further favor metal biosorption, unlike

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FIGURE 6.8 Soilmetal (Zn) concentrations measured in compartmental pots used for the growth of “dwarf” sunflower (Helianthus annuus): soils found in the (a) peripheral and (b) central compartments are shown. Mean (n 5 4) and standard errors for the preexperimental unseeded (black diamond), postexperimental unseeded (black square), hyphosphere (white square), mycorrhizosphere (white triangle), and rhizosphere (white circle) treatments are shown. Shared letters designate regression equations having slopes that are not significantly different according to ANCOVA (P , 0.05). Source: Data from Audet and Charest (2010a); refer to this study for experimental details.

root acidification that would increase solubility. Of course, careful experimental design is necessary to isolate these small-scale biogeochemical outcomes while still within the investigative context of whole ecosystems, but it is more than likely that proliferation of roots and hyphae should play a significant role in shaping soil profiles. As such, plant investment in the mycorrhizosphere should play a key role in enhancing plant and soil resiliency in relation to metal stress conditions.

6.3.2 The burden of metal stress and the dilemma of resource allocation Despite the promising conceptual foundation and greenhouse experimental outcomes described earlier, and the cellular and molecular findings that support these processes, upscaling of mycorrhizae to fieldlevel application (as suggested by Miransari, 2011; Audet, 2012; Meier et al., 2012a,b; Rajkumar et al., 2012; Anastasi et al., 2013; Danesh et al., 2013; Jafari et al., 2013; Sepehri et al., 2013) should


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FIGURE 6.9 Soil-pH measured in the (a) peripheral and (b) central compartments pots used for the growth of “dwarf” sunflower (Helianthus annuus). Mean (n 5 4) and standard errors for the preexperimental unseeded (black diamond), postexperimental unseeded (black square), hyphosphere (white square), mycorrhizosphere (white triangle), and rhizosphere (white circle) treatments are shown. Shared letters designate regression equations having slopes that are not significantly different according to ANCOVA (P , 0.05). Source: Data from Audet and Charest (2010a); refer to this study for experimental details.

ultimately be addressed with cautious optimism. This is true particularly in light of potential ecological and evolutionary boundaries for both plants and AM fungi as subjected to the extremes of metal stress (Audet, 2013). Variations in plant resource allocation (i.e., trade-offs) define plant life-history strategies, especially in relation to stress; this often underlies relative investment and allocation of energy toward either intrinsic (e.g., metabolic) or extrinsic (e.g., symbiotic) systems (Aerts and Honnay, 2011; Klironomos et al., 2011; Audet, 2012). Based on the notion that plant stress tolerance is fluid (i.e., both flexible and fluctuating) in relation to the intensity of the given environmental stressor, environmental conditions can determine the extent to which plants would then invest in mycorrhizal infrastructure versus, for example, internalization and sequestration of metal nutrients. Within the context of metal phytoremediation, the burden of metal stress implies a dilemma of resource allocation (Foy et al., 1978) that may prevent suitable development of the mycorrhizospheric network in spite of beneficial mycorrhizal attributes (i.e., enhanced metal/nutrient uptake and metal biosorption). The “dilemma” is exemplified by the AM fungi being obligated

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biotrophs and requiring a suitably resistant plant host (i.e., having adequate intrinsic tolerance) to provide a sufficient extrinsic investment for the development of the mycorrhizosphere. Thus, the impending challenge of metal toxicity may prevent any sustainable root colonization due to the host plant being metabolically “overdrawn.” Fundamental attitudes regarding ecological rehabilitation and restoration have necessarily shifted toward whole-ecosystem rehabilitation by regaining appropriate levels of ecological function rather than simply alleviating or circumventing a given environmental stress factor. Any such efforts now seek to incorporate native biodiversity and components of the broader “natural” landscape. The field of metal phytoremediation has yielded significant advances covering a broad range of mechanisms and life-history strategies enabling plants to overcome the burden of metal pollution. However, representing a major oversight in the adaptation of such mechanisms to field-level application, much less emphasis is given to whether these factors should necessarily be ecologically compatible. In other words, plants more “invested” in intrinsic processes may be less invested in extrinsic ones (and vice versa) when subjected to environmental stress due to the balance of trade associated with their given resource allocation “budget” (Schwartz and Hoeksema, 1998), as first proposed by the considerations of mycorrhizal “cost efficiency” by Koide and Elliott (1989) and later Koide (1991). Under experimental conditions, it has often been demonstrated how AM symbiosis enhances plant growth particularly when subjected to extreme growth conditions. Yet, since experimental conditions are mostly optimized to exaggerate and thereby better understand the mechanisms of interaction, much less investigative attention has been given to the likelihood that root colonization could even be achieved (or, likewise, developed to the same extent as under optimal investigative parameters) when subjected to similar stressful conditions in situ. Although such conceptual reasoning should not supersede or prevent attempts to adapt AM fungi as an emerging technology for metal phytoremediation, these aspects certainly represent a considerable gap in our understanding and, as such, an area of particular consideration for future research.

6.4 Conclusion and future prospects In this chapter, we examined potential mechanisms of the AM fungi and their widespread symbiosis with the majority of herbaceous plants as beneficial components in the phytoremediation of metal-polluted environments. By then assessing these processes from a combined and multilateral perspective, we established a conceptual foundation for the dynamic functioning of the mycorrhizal symbiosis across a range of metal exposure conditions from deficiency to toxicity. This is punctuated by the processes of enhanced metal/nutrient uptake, metal/nutrient biosorption and precipitation, and soil particulate micro- and macroaggregation. Indeed, there is consensus in the wider literature pool that these attributes could be highly favorable for improving the efficiency of metal phytoremediation. However, it may arise that the integration and application of AM fungi as a field-scale biotechnology in the phytoremediation of metal-contaminated environments may not be as fluid and/or directly achievable as once believed, that is, unless the ecological context for plant stress tolerance is carefully taken into consideration, as experienced when seeking to apply mycorrhizal technologies within agricultural systems (Fester and Sawers, 2011). In all likelihood, these processes may have beneficial implications for environmental remediation practices.

References

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Yet, as stipulated throughout, the successful integration of any such processes into field-level applications hinges on identifying and then accounting for boundaries set by biogeochemical conditions of metal-contaminated environments and the ecophysiological factors underpinning plantsoil interactions. According to Cahill and McNickle (2011), Smith and Smith (2011), and later Willis et al. (2013), this fundamental questioning should include (to name just a few): • • •

How do combined and multilateral processes affect ecosystem function and resilience across a range of environmental conditions? How is the AM symbiosis regulated (i.e., does mycorrhizal investment fluctuate) in relation to these conditions? How prolific is the mycorrhizosphere compared to the rhizosphere?

In turn, it would be possible to optimize upscaling of biotechnologies to field-level application and expand our knowledge and understanding of terrestrial systems, particularly in an era of environmental change, challenge, and opportunity.

Acknowledgments This critical review was made possible by financial support awarded to the author from the Centre for Mined Land Rehabilitation at the University of Queensland (Australia) and the Natural Sciences and Engineering Research Council (Canada) while he was then affiliated with the Centre for Mined Land Rehabilitation within the Sustainable Minerals Institute.

References Aerts, R., Honnay, O., 2011. Forest restoration, biodiversity and ecosystem functioning. BMC Ecol. 11, 29. Ali, H., Khan, E., Sajad, M.A., 2013. Phytoremediation of heavy metals—concepts and applications. Chemosphere 91, 869881. Alkorta, I., Hernandez-Allica, J., Becerril, J.M., Amezaga, I., Albizu, I., Garbisu, C., 2004. Recent findings on the phytoremediation of soils contaminated with environmentally toxic heavy metals and metalloids such as zinc, cadmium, lead and arsenic. Rev. Environ. Sci. Biotech. 3, 7190. Aloui, A., Recorbet, G., Robert, F., Schoefs, B., Bertrand, M., Henry, C., et al., 2011. Arbuscular mycorrhizal symbiosis elicits shoot proteome changes that are modified during cadmium stress alleviation in Medicago truncatula. BMC Plant. Biol. 11, 75. Anastasi, A., Tigini, V., Varese, G.C., 2013. The bioremediation potential of different ecophysiological groups of fungi. In: Goltapeh, E.M., Danesh, Y.R., Varma, A. (Eds.), Fungi as Bioremediators. Springer, Berlin, pp. 2949. Andrade, G., Mihara, K.L., Linderman, R.G., Bethlenfalvay, G.J., 1997. Bacteria from rhizosphere and hyphosphere soils of different arbuscular-mycorrhizal fungi. Plant Soil 192, 7179. Audet, P., 2012. AM symbiosis and other plant-soil interactions in relation to environmental stress. In: Ahmad, P., Prasad, M.N.V. (Eds.), Environmental Adaptations and Stress Tolerance of Plants in the Era of Climate Change. Springer, New York, pp. 233264. Audet, P., 2013. Examining the ecological paradox of the “mycorrhizal-metal-hyperaccumulators”. Arch. Agron. Soil Sci. 59, 549558.

154


Audet, P., Charest, C., 2006. Effects of AM colonization on “wild tobacco” plants grown in zinc contaminated soil. Mycorrhiza 16, 277283. Audet, P., Charest, C., 2007a. Dynamics of AM symbiosis in heavy metal phytoremediation: meta analytical and conceptual perspectives. Environ. Pollut. 147, 609614. Audet, P., Charest, C., 2007b. Heavy metal phytoremediation from a meta analytical perspective. Environ. Pollut. 147, 231237. Audet, P., Charest, C., 2008. Allocation plasticity & metal partitioning: meta analytical perspectives in phytoremediation. Environ. Pollut. 156, 290296. Audet, P., Charest, C., 2009. Contribution of AM symbiosis to in vitro root metal uptake: from trace to toxic metal conditions. Botany 87, 913921. Audet, P., Charest, C., 2010a. Determining the impact of the AM mycorrhizosphere on “dwarf” sunflower Zn uptake and soil Zn bioavailability in a compartmental growth environment. J. Bot. 2010, Article ID 268540, 11 pages. Audet, P., Charest, C., 2010b. Identification of constraining experimental design factors in mycorrhizal pot growth studies. J. Bot. 2010, Article ID 718013, 6 pages. Audet, P., Charest, C., 2013. Assessing the AM mycorrhizosphere’s stratum of influence: plant metal uptake and soil metal bioavailability in a compartmental growth environment. Arch. Agron. Soil Sci. 59, 533548. Augé, R.M., 2004. Arbuscular mycorrhizae and soil/plant water relations. Can. J. Soil Sci. 84, 373381. Bago, B., Vierheilig, H., Piche, Y., Azcoń-Aguilar, C., 1996. Nitrate depletion and pH changes induced by the extraradical mycelium of the arbuscular mycorrhizal fungus Glomus intraradices grown in monoxenic culture. New Phytol. 133, 273280. Baker, A.J.M., Walker, P.L., 1990. Ecophysiology of metal uptake by tolerant plants. In: Shaw, A.J. (Ed.), Heavy Metal Tolerance in Plants: Evolutionary Aspects. CRC Press, Boca Raton, pp. 155177. Barceloux, D.G., 1999. Zinc. J. Toxicol. Clin. Tox. 37, 279280. Barea, J.M., Pozo, M.J., Azcoń, R., Azcoń-Aguilar, C., 2005. Microbial co-operation in the rhizosphere. J. Exp. Bot. 56, 17611778. Beare, M.H., Coleman, D.C., Crossley, D.A., Hendrix, P.F., Odum, E.P., 1995. A hierarchical approach to evaluating the significance of soil biodiversity and no-tillage ultisols. Plant Soil 170, 522. Bever, J.D., 1999. Dynamics within mutualism and the maintenance of diversity: inference from a model of interguild frequency dependence. Ecol. Lett. 2, 5261. Bever, J.D., 2003. Soil community feedback and the coexistence of competitors: conceptual frameworks and empirical tests. New Phytol. 157, 465473. Bever, J.D., Westover, K.M., Antonovics, J., 1997. Incorporating the soil community into plant population dynamics: the utility of the feedback approach. J. Ecol. 85, 561573. Bhargava, A., Carmona, F.F., Bhargava, M., Srivastava, S., 2012. Approaches for enhanced phytoextraction of heavy metals. J. Environ. Manage. 30, 103120. Bianciotto, V., Bonfante, P., 2002. Arbuscular mycorrhizal fungi: a specialised niche for rhizospheric endocellular bacteria. Antonie van Leewenhoek 81, 365371. Blinkley, D., Vitousek, P.M., 1989. Soil nutrient availability. In: Peracy, R.W., Ehleringer, J.R., Mooney, H.A., Rundel, P.W. (Eds.), Plant Physiological Ecology. Springer, Dordrecht, pp. 7596. Bonfante, P., Anca, I.A., 2011. Plants, mycorrhizal fungi, and bateria: a network of interactions. Ann. Rev. Microbiol. 63, 363386. Boucher, D.H., James, S., Keeler, K.H., 1982. The ecology of mutualism. Ann. Rev. Ecol. Sys. 13, 315347. Bradl, H.B., 2004. Adsorption of heavy metal ions on soils and soils constituents. J. Colloid Interf. Sci. 277, 118.

References

155

Brussaard, L., Behan-Pelletier, V., Bignell, D., Brown, V., Didden, W., Folgarait, P., et al., 1997. Biodiversity and ecosystem function in soil. Ambio 26, 563570. Brussaard, L., de Ruiter, P.C., Brown, G.G., 2007. Soil biodiversity for agriculture sustainability. Agric. Ecosys. Environ. 121, 233244. Burleigh, S.H., Kristensen, B.K., Bechmann, I.B., 2003. A plasma membrane zinc transporter from Medicago truncatula up-regulated in roots by Zn fertilization, yet down-regulated by arbuscular mycorrhizal colonization. Plant Mol. Biol. 52, 10771088. Cahill, J.F., McNickle, G.G., 2011. The behavioral ecology of nutrient foraging in plants. Ann. Rev. Ecol. Evol. Syst. 42, 289311. Cavagnaro, T.R., 2008. The role of arbuscular mycorrhizas in improving zinc nutrition under low soil zinc concentrations: a review. Plant Soil 304, 315325. Cavagnaro, T.R., Dickson, R.S., Smith, F.A., 2010. Arbuscular mycorrhizas modify plant responses to soil zinc addition. Plant Soil 329, 307313. Chalot, M., Blaudez, D., Brun, A., 2006. Ammonia: a candidate for nitrogen transfer at the mycorrhizal interface. Trends Plant Sci. 11, 263266. Christie, P., Li, X.L., Chen, B.D., 2004. Arbuscular mycorrhiza can depress translocation of zinc to shoots of host plants in soils moderately polluted with zinc. Plant Soil 261, 209217. Chuan, M.C., Shu, G.Y., Liu, J.C., 1996. Solubility of heavy metals in contaminated soil: effects of redox potential and pH. Water Air Soil Pollut. 90, 543556. Cleveland, C.C., Townsend, A.R., Schmidt, S.K., 2002. Phosphorus limitation of microbial processes in moist tropical forests: evidence from short-term laboratory incubations and field studies. Ecosystems 5, 680691. Cobbett, C.S., 2000. Phytochelatins and their roles in heavy metal detoxification. Plant Physiol. 123, 825832. Cobbett, C.S., Goldsbrough, P., 2002. Phytochelatins and metallothioneins: role in heavy metal detoxification and homeostasis. Ann. Rev. Plant Biol. 53, 159182. Corradi, N., Charest, C., 2011. Some like it toxic. Mol. Ecol. 20, 32893290. Danesh, Y.R., Tajbakhsh, M., Goltapeh, E.M., Varma, A., 2013. Mycoremediation of heavy metals. In: Goltapeh, E.M., Danesh, Y.R., Varma, A. (Eds.), Fungi as Bioremediators. Springer, Berlin, pp. 245267. Dickinson, N.N., Baker, A.J.M., Doronila, A., Laidlaw, S., Reeves, R.D., 2009. Phytoremediation of inorganics: realism and synergies. Int. J. Phytorem. 11, 97114. Douds, D.D., Pfeffer, P.E., Shachar-Hill, Y., 2000. Carbon partitioning, cost and metabolism of arbuscular mycorrhizae in arbuscular mycorrhizas: physiology and function. In: Kapulnick, Y., Douds, D.D. (Eds.), Arbuscular Mycorrhizas: Molecular Biology and Physiology. Kluwer Academic, Dordrecht, pp. 107129. Duponnois, R., Galiana, A., Prin, Y., 2008. The mycorrhizosphere effect: a multitrophic interaction complex improves mycorrhizal symbiosis and plant growth. In: Anwar, S.Z., Sayeed, A.M., Kazuyoshi, F. (Eds.), Mycorrhizae: Sustainable Agriculture and Forestry. Springer, Berlin, pp. 227240. Eckhard, G., Ro¨mheld, V., Marschner, H., 1994. Contribution of mycorrhizal fungi to micronutrient uptake by plants. In: Manthey, J., Crowley, D.E., Luster, G.L. (Eds.), Biochemistry of Metal Micronutrients in the Rhizosphere. CRC Press, Boca Raton, pp. 93110. Eckhard, G., Marschner, H., Jakobsen, I., 1995. The role of arbuscular mycorrhizal fungi in uptake of phosphorus and nitrogen from soil. Crit. Rev. Biotech. 15, 257270. Epstein, E., 1972. Mineral Nutrition of Plants: Principles and Perspectives. Wiley, New York. Evangelou, M.W.H., Ebel, M., Schaeffer, A., 2007. Chelate assisted phytoextraction of heavy metals soil. Effect, mechanism, toxicity, and fate of chelating agents. Chemosphere 68, 9891003. Fester, T., Sawers, R., 2011. Progress and challenges in agricultural applications of arbuscular mycorrhizal fungi. Plant Sci. 30, 459470.

156


Fitter, A.H., Garbaye, J., 1994. Interactions between mycorrhizal fungi and other soil organisms. Plant Soil 159, 123132. Fitter, A.H., Helfason, T., Hodge, A., 2011. Nutritional exchanges in the arbuscular mycorrhizal symbiosis: implications for sustainable agriculture. Fungal Biol. Rev. 25, 6872. Fogarty, R.V., Tobin, J.M., 1996. Fungal melanins and their interactions with metals. Enz. Microb. Technol. 19, 311317. Fourest, E., Roux, J.C., 1992. Heavy metal biosorption by fungal mycelial by-products: mechanism and influence of pH. Appl. Microbiol. Biotech. 37, 399403. Foy, C.D., Chaney, R.L., White, M.C., 1978. The physiology of metal toxicity in plants. Ann. Rev. Plant Physiol. 29, 511566. Frey-Klett, P., Garbaye, J., Tarkka, M., 2007. The mycorrhiza helper bacteria revisited. New Phytol. 176, 2236. Gadd, G.M., 1993. Interactions of fungi with toxic metals. New Phytol. 124, 2560. Gahoonia, T.S., Nielsen, N.E., 1992. The effects of rootinduced pH changes on the depletion of inorganic and organic phosphorus in the rhizosphere. Plant Soil 143, 185191. Galli, U., Schuëpp, H., Brunold, C., 1994. Heavy metal binding by mycorrhizal fungi. Physiol. Plant 92, 364368. Garbaye, J., 1991. Biological interactions in the mycorrhizosphere. Cell. Mol. Life. Sci. 47, 370375. Garbaye, J., 1994. Helper bacteria: a new dimension to the mycorrhizal symbiosis. New Phytol. 128, 197210. Garg, N., Aggarwal, N., 2012. Effect of mycorrhizal inoculations on heavy metal uptake and stress alleviation of Cajanus cajan (L.) Millsp. genotypes grown in cadmium and lead contaminated soils. Plant Growth Reg. 66, 926. George, E., Marschner, H., Jakobsen, I., 1995. Role of arbuscular-mycorrhizal fungi in uptake of phosphorus and nitrogen from soil. Crit. Rev. Biotech. 15, 257270. Giller, K.E., Witter, E., McGrath, S.P., 1998. Toxicity of heavy metals to microorganisms and microbial processes in agricultural soils: a review. Soil Biol. Biochem. 30, 13891414. González-Chavez, C., d’Haen, J., Vangronsveld, J., Dodd, J.C., 2002. Copper sorption & accumulation by the extraradical mycelium of different Glomus spp. (arbuscular mycorrhizal fungi) isolated from the same polluted soil. Plant Soil 240, 287297. González-Guerrero, M., Azcoń-Aguilar, C., Mooney, M., Valderas, A., MacDiarmid, C.W., Eide, D.J., et al., 2005. Characterization of a Glomus intraradices gene encoding a putative Zn transporter of the cation diffusion facilitator family. Fungal Genet. Biol. 42, 130140. González-Guerrero, M., Cano, C., Azcoń-Aguilar, C., Ferrol, N., 2007. GintMT1 encodes a functional metallothionein in Glomus intraradices that responds to oxidative stress. Mycorrhiza 17, 327335. González-Guerrero, M., Melville, L.H., Ferrol, N., Lott, J.N.A., Azcoń-Aguilar, C., Peterson, R.L., 2008. Ultrastructural localization of heavy metals in the extraradical mycelium and spores of the arbuscular mycorrhizal fungus Glomus intraradices. Can. J. Microbiol. 54, 103110. González-Guerrero, M., Benabdellah, K., Ferrol, N., Azcoń-Aguilar, C., 2009. Mechanisms underlying heavy metal tolerance in arbuscular mycorrhizas. In: Azcoń-Aguilar, C., Barea, J.M., Gianinazzi, S., Gianinazzi-Pearson, V. (Eds.), Mycorrhizas: Functional Processes and Ecological Impact. Springer, Berlin, pp. 116. González-Guerrero, M., Raimunda, D., Cheng, X., Arguëllo, J.M., 2010a. Distinct functional role of homologous Cu1 efflux ATPases in Pseudomonas aeruginosa. Mol. Microbiol. 78, 12461258. González-Guerrero, M., Benabdellah, K., Valderas, A., Azcoń-Aguilar, C., Ferrol, N., 2010b. GintABC1 encodes a putative ABC transporter of the MRP subfamily induced by Cu, Cd and oxidative stress in Glomus intraradices. Mycorrhiza 20, 137146.

References

157

Govindarajulu, M., Pfeffer, P.E., Jin, H., Douds, D.D., Allen, J.W., Bucking, H., et al., 2005. Nitrogen transfer in the arbuscular mycorrhizal symbiosis. Nature 435, 819823. Gu¨hre, V., Pazkowski, U., 2006. Contribution of the arbuscular mycorrhizal symbiosis to heavy metal phytoremediation. Plant 223, 11151122. Harrison, M.J., 1999. Signaling in the arbuscular mycorrhizal symbiosis. Ann. Rev. Microbiol. 59, 1942. Harrison, M.J., 2005. Molecular and cellular aspects of the arbuscular mycorrhizal symbiosis. Ann. Rev. Plant Phys. Plant Mol. Biol. 50, 361389. Hassan, S.E.D., Boon, E., St-Arnaud, M., Hijri, M., 2011. Molecular biodiversity of arbuscular mycorrhizal fungi in trace metal-polluted soils. Mol. Ecol. 20, 34693483. Hassan, S.E.D., Hijri, M., St-Arnaud, M., 2013. Effect of arbuscular mycorrhizal fungi on trace metal uptake by sunflower plants grown on cadmium contaminated soil. New Biotechnol. 30, 780787. Hassan, Z., Aarts, M.G.M., 2011. Opportunities and feasibilities for biotechnological improvement of Zn, Cd or Ni tolerance and accumulation in plants. Environ. Exp. Bot. 72, 5363. Hildebrandt, U., Regvar, M., Bothe, H., 2007. Arbuscular mycorrhiza and heavy metal tolerance. Phytochemistry 68, 139146. Jafari, M., Danesh, Y.R., Ghoosta, Y., 2013. Molecular techniques in fungal bioremediation. In: Goltapeh, E.M., Danesh, Y.R., Varma, A. (Eds.), Fungi as Bioremediators. Springer, Berlin, pp. 453465. Janos, D.P., 2007. Plant responsiveness to mycorrhizas differs from dependence upon mycorrhizas. Mycorrhiza 17, 7591. Javot, H., Pumplin, N., Harrison, M.J., 2007. Phosphate in the arbuscular mycorrhizal symbiosis: transport properties and regulatory roles. Plant Cell Environ. 30, 310322. Jin, H., Pfeffer, P.E., Douds, D.D., Piotrowski, E., Lammers, P.J., Shachar-Hill, Y., 2005. The uptake, metabolism, transport and transfer of nitrogen in an arbuscular mycorrhizal symbiosis. New Phytol. 168, 687696. Johnson, N.C., Graham, J.H., Smith, F.A., 1997. Functioning of mycorrhizal associations along the mutualismparasitism continuum. New Phytol. 135, 575586. Joner, E.J., Briones, R., Leyval, C., 2000. Metal-binding capacity of arbuscular mycorrhizal mycelium. Plant Soil 226, 227234. Jones, M.D., Smith, S.E., 2004. Exploring functional definitions of mycorrhizas: are mycorrhizas always mutualisms? Can. J. Bot. 82, 10891109. Kahn, A.G., Kuek, C., Chaudhry, T.M., Khoo, C.S., Hayes, W.J., 2000. Role of plants, mycorrhizae and phytochelators in heavy metal contaminated land remediation. Chemosphere 41, 197207. Klironomos, J.N., 2002. Feedback with soil biota contributes to plant rarity and invasiveness in communities. Nature 417, 6770. Klironomos, J.N., Zobel, M., Tibbett, M., Stock, W.D., Rillig, M.C., Parrent, J.L., et al., 2011. Forces that structure plant communities: quantifying the importance of the mycorrhizal symbiosis. New Phytol. 189, 366370. Koide, R.T., 1991. Nutrient supply, nutrient demand and plant response to mycorrhizal infection. New Phytol. 117, 365386. Koide, R.T., 1993. Physiology of the mycorrhizal plant. Adv. Plant Pathol. 9, 3354. Koide, R.T., 2000. Mycorrhizal symbiosis and plant reproduction. In: Kapulnik, Y., Douds, D.D. (Eds.), Arbuscular Mycorrhizas: Physiology and Function. Kluwer, Dordrecht, pp. 1946. Koide, R.T., Elliott, G., 1989. Cost, benefit and efficiency of the vesicular-arbuscular mycorrhizal symbiosis. Funct. Ecol. 3, 252255. Lasat, M.M., 2002. Phytoextraction of toxic metals: a review of biological mechanisms. J. Environ. Qual. 31, 109120.

158


Lebeau, T., Braud, A., Jezequel, K., 2008. Performance of bioaugmentation-assisted phytoextraction applied to metal contaminated soils: a review. Environ. Pollut. 153, 497522. Lestan, D., Luo, C.L., Li, X.D., 2008. The use of chelating agents in the remediation of metal-contaminated soils: a review. Environ. Pollut. 153, 313. Leung, T.L.F., Poulin, R., 2008. Parasitism, commensalism and mutualism: exploring the many shades of symbiosis. Vie Milieu 58, 107115. Leyval, C., Turnau, K., Haselwandter, K., 1997. Effect of heavy metal pollution on mycorrhizal colonization and function: physiological, ecological, and applied aspects. Mycorrhiza 7, 139153. Li, X., Christie, P., 2001. Changes in soil solution Zn and pH and uptake of Zn by arbuscular mycorrhizal red clover in Zn-contaminated soil. Chemosphere 42, 201207. Liu, A., Hamel, C., Hamilton, R.I., Ma, B.L., Smith, D.L., 2000. Acquisition of Cu, Zn, Mn and Fe by mycorrhizal maize (Zea mays L.) grown in soil at different P and micronutrient levels. Mycorrhiza 9, 331336. Lock, K., Janssen, C.R., 2003. Influence of aging on metal availability in soils. Rev. Environ. Contam. Tox. 178, 121. Lo´pez-Millán, A.F., Ellis, D.R., Grusak, M.A., 2004. Identification and characterization of several new members of the ZIP family of metal ion transporters in Medicago truncatula. Plant Mol. Biol. 54, 583596. Lo´pez-Pedrosa, A., Gonález-Guerrero, M., Valderas, A., Azcoń-Aguilar, C., Ferrol, N., 2006. GintAMT1 encodes a functional high-affinity ammonium transporter that is expressed in the extraradical mycelium of Glomus intraradices. Fungal Genet. Biol. 43, 102110. Marschner, H., 1995. Mineral Nutrition of Higher Plants. second ed. Springer, Berlin. Martinez, C.E., Motto, H.L., 2000. Solubility of lead, zinc and copper added to mineral soils. Environ. Pollut. 107, 153158. McBride, M.B., 1994. Environmental Chemistry of Soils. Oxford University Press, Oxford. McGrath, S.P., Zhao, F.J., 2003. Phytoextraction of metals and metalloids from contaminated soils. Curr. Opin. Biotech. 14, 277282. Meharg, A.A., 2003. The mechanistic basis of interactions between mycorrhizal associations and toxic metal cations. Mycol. Res. 107, 12531265. Meier, S., Borie, F., Bolan, N., Cornejo, P., 2012a. Phytoremediation of metal-polluted soils by arbuscular mycorrhizal fungi. Crit. Rev. Environ. Sci. Tech. 42, 741775. Meier, S., Borie, F., Curaqueo, G., Bolan, N., Cornejo, P., 2012b. Effects of arbuscular mycorrhizal inoculation on metallophyte and agricultural plants growing at increasing copper levels. Appl. Soil Ecol. 61, 280287. Mendgen, K., Hahn, M., 2002. Plant infection and the establishment of fungal biotrophy. Trends Plant Sci. 7, 352356. Mengel, K., Kosegarten, H., Kirkby, E.A., Appel, T., 2001. Principles of Plant Nutrition. Springer, Berlin. Miller, R.M., Jastrow, J.D., 1990. Hierarchy of root and mycorrhizal fungal interactions with soil aggregation. Soil Biol. Biochem. 22, 579584. Miransari, M., 2011. Hyperaccumulators, arbuscular mycorrhizal fungi and stress of heavy metals. Biotech. Adv. 29, 645653. Neagoe, A., Iordache, V., Kothe, E., 2013. Upscaling the biogeochemical role of arbuscular mycorrhizal fungi in metal mobility. In: Goltapeh, E.M., Danesh, Y.R., Varma, A. (Eds.), Fungi as Bioremediators. Springer, Berlin, pp. 285311. Newsham, K.K., Fitter, A.H., Watkinson, A.R., 1995. Multi-functionality and biodiversity in arbuscular mycorrhizas. Trends Ecol. Evol. 10, 407411. Peterson, L.R., Massicotte, H.B., Melville, L.H., 2004. Mycorrhizas: Anatomy and Cell Biology. NRC Research Press, Ottawa. Pilon-Smits, E., 2005. Phytoremediation. Ann. Rev. Plant Biol. 56, 1539.

References

159

Piotrowski, J.S., Denich, T., Klironomos, J.N., Graham, J.M., Rillig, M.C., 2004. The effects of arbuscular mycorrhizae on soil aggregation depend on the interaction between plant and fungal species. New Phytol. 164, 365373. Pongrac, P., Vogel-Mikus, K., Poschenrieder, C., Barcelo, J., Tolra, R., Regvar, M., 2013. Arbuscular mycorrhiza in glucosinolate-containing plants: the story of the metal hyperaccumulator Noccaea (Thalspi) praecox (Brassicaceae). In: de Bruijn, F.J. (Ed.), Molecular Microbial Ecology of the Rhizosphere, vol. 2. Wiley and Sons, New York, pp. 10231032. Purin, S., Rillig, M.C., 2008. Parasitism of arbuscular mycorrhizal fungi: reviewing the evidence. FEMS Microbiol. Lett. 279, 814. Rajkumar, M., Sandhya, S., Prasad, M.N.V., Freitas, H., 2012. Perspectives of plant-associated microbes in heavy metal phytoremediation. Biotech. Adv. 30, 15621574. Rangel, W.d.M., Schneider, J., Costa, E.T.d.S., Soares, C.R.F.S., Guilherme, L.R.G., Moreira, F.M.D.S., 2013. Phytoprotective effect of arbuscular mycorrhizal fungi species against arsenic toxicity in tropical leguminous species. Int. J. Phytorem. 16, 840858. Rascio, N., Navari-Izzo, F., 2011. Heavy metal hyperaccumulating plants: how and why they do it? And what makes them so interesting? Plant Sci. 180, 169181. Redecker, D., Kodner, R., Graham, L.E., 2000. Glomalean fungi from the Ordovician. Science 289, 19201921. Remy, W., Taylor, T.N., Hass, H., Kerp, H., 1994. Four hundred-million-year-old vesicular arbuscular mycorrhizae. Proc. Natl. Acad. Sci. U.S.A. 91, 1184111843. Rillig, M.C., Mummey, D.L., 2006. Mycorrhizas and soil structure. New Phytol. 171, 4153. Rillig, M.C., Mardatin, N.F., Leifheit, E.F., Antunes, P.M., 2010. Mycelium of arbuscular mycorrhizal fungi increases soil water repellency and is sufficient to maintain water-stable soil aggregates. Soil Biol. Biochem. 42, 11891191. Ross, S.M., 1994. Retention, transformation and mobility of toxic metals in soils. In: Ross, S.M. (Ed.), Toxic Metals in Soil-Plant Systems. Wiley and Sons, New York, pp. 63152. Schachtman, D.P., Reid, R.J., Ayling, S.M., 1998. Phosphorus uptake by plants: from soil to cell. Plant Physiol. 116, 447453. Schu¨tzendu¨bel, A., Polle, A., 2002. Plant responses to abiotic stresses: heavy metal-induced oxidative stress and protection by mycorrhization. J. Exp. Bot. 372, 13511365. Schwab, S.M., Menge, J.A., Tinker, P.B., 1991. Regulation of nutrient transfer between host and fungus in vesicular-arbuscular mycorrhizas. New Phytol. 117, 387398. Schwartz, M.W., Hoeksema, J.D., 1998. Specialization and resource trade: biological markets as a model of mutualisms. Ecology 79, 10291038. Schu¨ßler, A., Schwarzott, D., Walker, C., 2001. A new fungal phylum, the Glomeromycota: phylogeny and evolution. Mycol. Res. 105, 14131421. Sepehri, M., Khodaverdiloo, H., Zarei, M., 2013. Fungi and their role in phytoremediation of heavy metal contaminated soils. In: Goltapeh, E.M., Danesh, Y.R., Varma, A. (Eds.), Fungi as Bioremediators. Springer, Berlin, pp. 313345. Smith, S.E., Smith, F.A., 2011. Roles of arbuscular mycorrhizas in plant nutrition and growth: new paradigms from cellular to ecosystem scales. Ann. Rev. Plant Biol. 62, 227250. Tack, F.M., Callewaert, O.W.J.J., Verloo, M.G., 1996. Metal solubility as a function of pH in a contaminated, dredged sediment affected by oxidation. Environ. Pollut. 91, 199208. Tinker, P.B., Durall, D.M., Jones, M.D., 1994. Carbon use efficiency in mycorrhizas: theory and sample calculations. New Phytol. 128, 115122. van der Heijden, M.G.A., Klironomos, J.N., Ursic, M., Moutoglis, P., Streitwolf-Engel, R., Boller, T., et al., 1998. Mycorrhizal fungal diversity determines plant biodiversity, ecosystem variability and productivity. Nature 396, 6972.

160


van der Heijden, M.G.A., Wiemken, A., Sanders, I.R., 2003. Different arbuscular mycorrhizal fungi alter coexistence and resource distribution between co-occurring plants. New Phytol. 157, 569578. Vierheilig, H., Piché, Y., 2002. Signaling in arbuscular mycorrhiza: facts and hypotheses. In: Buslig, B.S., Manthey, J.A. (Eds.), Flavonoids in Cell Function. Kluwer Academic, Dordrecht, pp. 2340. Vilousek, P.M., Howarth, R.W., 1991. Nitrogen limitation on land and in the sea: how can it occur. Biogeochemistry 13, 87115. Wardle, D.A., Barker, G.M., Bonner, K.I., Nicholson, K.S., 1998. Can comparative approaches based on plant ecophysiological traits predict the nature of biotic interactions and individual plant species effects in ecosystems? J. Ecol. 86, 405420. Wardle, D.A., Bardgett, R.D., Klironomos, J.N., Seta¨la¨, H., van der Putten, W.H., Wall, D.H., 2004. Ecological linkages between above- and belowground biota. Science 304, 16291633. Willis, A., Rodrigues, B.F., Harris, P.J.C., 2013. The ecology of arbuscular mycorrhizal fungi. Crit. Rev. Plant Sci. 32, 120. Wuana, R.A., Okieimen, F.E., 2011. Heavy metals in contaminated soils: a review of sources, chemistry, risks and best available strategies for remediation. ISRN Ecol. 2011, Article ID 402647, 20 pages. Zare-Maivan, H., 2013. Mycorrhizae adsorb and bioaccumulate heavy and radioactive metals. In: Goltapeh, E.M., Danesh, Y.R., Varma, A. (Eds.), Fungi as Bioremediators. Springer, Berlin, pp. 269281. Zitka, O., Merlos, M.A., Adam, V., Ferrol, N., Phanka, M., Hubalek, J., et al., 2012. Electrochemistry of copper(II) induced complexes in mycorrhizal maize plant tissues. J. Hazard Mat. 203/204, 257263.

CHAPTER

Biological Control of Fungal Disease by Rhizobacteria under Saline Soil Conditions

7

Dilfuza Egamberdieva, Abeer Hashem and Elsayed Fathi Abd-Allah

7.1 Introduction The urgency of feeding the world’s growing population requires intensification of crop production and enlargement of agricultural land. The increase in abiotic stresses, such as drought and salinity, is one of the main consequences of climate change and will impede the development of the agricultural system (Ahmad and Sharma, 2008; Ahmad et al., 2012). The total global area of salt-affected soils has recently been estimated to be approximately 830 million hectares (Martinez-Beltran and Manzur, 2005). Extensive research attempts are underway to improve plants’ salt tolerance and disease resistance. However, when soil salinity is high, pathogen-resistant varieties are attacked by Fusarium, Vertcillium, and other pathogens and show severe symptoms (Besri, 1993). Previous reports also indicated that salt stress inhibits root initiation, plant growth, and increases susceptibility of plants to various phytopathogens (Rasmussen and Stanghellini, 1988; Triky-Dotan et al., 2005; Egamberdieva et al., 2011; Egamberdieva and Jabborova, 2013). According to Esechie et al. (2002) and Ma et al. (2001), young salt-stressed seedlings are more susceptible to hypocotyl and cotyledon injury or attack by pathogens. According to Triky-Dotan et al. (2005), the effects of salt on plant disease may result from its affect on the pathogen, the host, or the soil’s abiotic components. Salinity also disturbs plantmicrobe interaction, which is a critical ecological factor to help further plant growth in degraded ecosystems (Requena et al., 2001; Egamberdiyeva and Kucharova, 2007). To control these pathogens is extremely difficult and a very small percentage (0.1%) of applied fungicides used for crop protection reaches the target pathogen (Pimentel and Levitan, 1986). On the other hand, chemical control of diseases has negative effects on the environment such as a decrease in the biodiversity of soil microbiota, development of fungicide-resistant pathogens, and contamination of fruits and vegetables with chemicals that endanger the health of consumers (Pimentel et al., 1993; Bernard et al., 2012; Luduenã et al., 2012). It is well documented that biological control agents based on plant growth-promoting rhizobacteria (PGPR) are able to control plant diseases, increase plant growth, and improve resistance to environmental stresses, including drought and salt (Yildirim et al., 2008; Lugtenberg and Kamilova, 2009; Ramette et al., 2011; Crépin et al., 2012; Dodd and Pérez-Alfocea, 2012; Egamberdieva et al., 2013).


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CHAPTER 7 Biological Control of Fungal Disease by Rhizobacteria

Biological control of plant disease by rhizobacteria involves several mechanisms such as production of antifungal metabolites, cell wall degrading enzymes, induced host resistance, and competition for nutrition and niches (Zhang et al., 2010; Li et al., 2011). Abiotic and biotic factors (e.g., pH, moisture, salinity, drought, temperature, and soil inorganic and organic constituents) may influence the interactions between plant pathogens and biological control agents (Landa et al., 2004). Most studies on growth promotion and biological control of plant disease by rhizobacteria have been directed toward normal environmental conditions. There is still little direct evidence of how abiotic factors affect the interactions among PGPR and plant, soil-borne plant pathogens, and their action mechanisms. In this review, we attempt to discuss some of the scientific challenges that still exist in biocontrol research under harsh environmental conditions. This chapter also provides an overview of the modes of action of the PGPR that act as biological control agents affected by salinity.

7.2 Salinity and plant pathogens Previous studies showed the differential effects of salinity on pathogen growth, reproduction, the virulence of the pathogen, and on the susceptibility of the plant (Blaker and MacDonald, 1985; Rasmussen and Stanghellini, 1988), whereas higher salinity conditions were found to increase fungal disease (Sanogo, 2004; Triky-Dotan et al., 2005). El-Abyed et al. (1988) and Ragazzi et al. (1994) reported that mycelial growth of different Fusarium species were increased under salt-stress conditions. Daami-Remadi and others (2009) observed that soil salinity (210 g of NaCl/L) increases the population of Fusarium oxysporum f. sp. lycopersici in the soil. The sporulation of the fungus in the plant vessels resulted in a significant increase in the leaf damage index (LDI). Tomato plants irrigated with saline water were more susceptible to the pathogen than the tomato irrigated with nonsaline water. Similar observations were reported by Swiecki and MacDonald (1988) and Blaker and MacDonald (1986) in citrus plants where salinity stress has shown to increase the susceptibility of citrus and chrysanthemum to Phytophthora root rots. They found that the Phytophthora isolates have a greater tolerance of soil salinity than crop plants. Goudarzi et al. (2011) reported that shoot and root colonization by Macrophomina phaseolina significantly increased by raising soil salinity levels up to 1400 mg of NaCl kg21. Consequently, more infected crown and root were observed with increasing NaCl levels. In our study, we isolated and identified cucumber and the tomato root rot pathogen Fusarium solani. This is the first report that demonstrates the occurrence of F. solani pathogen in salinated soil that causes cucumber and tomato foot and root rot disease. The F. solani isolates were salt tolerant up to 4% NaCl (Figure 7.1). In earlier studies, Swieckil and MacDonald (1991) found that salinity stress increased Phytophthora root and crown rot severity in tomato. Similar results were observed in our studies with tomato and cucumber, where higher levels of soil salinity increased root rot caused by Fusarium solani (Egamberdieva et al., 2011, 2012). Sanogo (2004) studied the response of chile pepper to salinity and infection by Phytophthora capsici under greenhouse conditions in plants susceptible or resistant to P. capsici. They found that disease severity increased in plants susceptible to P. capsici by approximately 1.3- to 2.7-fold with increasing salinity levels, whereas no such effect was observed in plants resistant to P. capsici. Blodgett et al. (1997) noted that water-stressed plants’ defense mechanisms may be slowed down more than in nonstressed plants.

7.3 Plant growth-promoting rhizobacteria

163

Fusarium solani, tomato

1%

2%

3%

4%

Fusarium solani, cucumber

1%

2%

3%

4%

FIGURE 7.1 Salt tolerance of F. solani isolated from cucumber and tomato.

7.3 Plant growth-promoting rhizobacteria In plant rhizosphere, the interactions of microorganisms with each other may be associative, competitive, mutualistic, or antagonistic. Some bacteria promote plant growth and increase the availability of essential nutrients through nutrient cycling activities; others induce resistance in the plants against plant pathogens (Adesemoye et al., 2008; Cummings, 2009; Wahyudi et al., 2011). The extracellular products present in the rhizosphere and root-associated bacteria play an important role in inhibiting plant pathogens (Hinsinger et al., 2006; Lugtenberg and Kamilova, 2009). PGPR may colonize the rhizosphere and root surface and protect plants from various stresses. Root colonization by microbes is influenced by biotic and abiotic factors such as indigenous microorganisms, temperature, soil type, rhizosphere exudates, humidity and others; thus, PGPR have to be highly competitive to colonize the rhizosphere (Compant et al., 2010). The rhizosphere protects a large and diverse community of microbes that interact with each other, but low taxonomic diversity was found in saline environments (Nannipieri et al., 2003; Trabelsi et al., 2009). Soil salinity not only inhibits plant growth and development but also negatively affects soil microbial population and activities. The salt-tolerant bacteria, with their physiological adaptation for increased tolerance to drought, increasing salt concentration, and high temperatures, could survive in such harsh environments and help plants tolerate salt stress (Mayak et al., 2004; Yasmin et al., 2013). A range of salt-tolerant rhizobacteria (e.g., Rhizobium, Azospirillum, Pseudomonas, Flavobacterium, Arthrobacter, and Bacillus) so far has shown beneficial interactions with plants in stressed environments (Adesemoye et al., 2008; Egamberdieva and Islam, 2008; Egamberdieva et al., 2013). Root-associated bacteria are more tolerant to salt stress than soil bacteria because salinity stress alleviated in the rhizosphere is due to depletion of water and exclusion of toxic solutes by plant roots and thus elevate both its ionic strength and its osmolality (Tripathi et al., 2002). They colonize rhizosphere, so root tissue may respond to plant

164


signals, exchange nutrients with plant cells, and synthesize and release auxin as secondary metabolites because of the rich supplies of substrates exuded from the roots (Lugtenberg et al., 2001; Compant et al., 2005; Arora et al., 2008). According to Rangarajan et al. (2003), fluorescent pseudomonads dominate in nonsaline soils and species, such as Pseudomonas alcaligenes and P. pseudoalcaligenes, found in saline soils. We previously reported the occurrence of P. aeruginosa in the rhizosphere of wheat plants growing in irrigated salinated Uzbek soil (Egamberdieva et al., 2008). The physiological and biochemical mechanisms of adaptation to saline environments by plant growth-promoting bacteria (e.g., Rhizobium, Azospirillum, Pseudomonas, Arthrobacter, and Bacillus) has been reported (Egamberdieva and Kucharova, 2009; Ilyas et al., 2012; Yasmin et al., 2013).

7.4 Biological control In the last decade, studies on the use of beneficial microorganisms as biocontrol agents for protecting plants from various diseases have increased greatly. Several strains have been reported to show good performance in vitro and in specific trials, greenhouse, and field experiments (Rangarajan et al., 2003; Gasoni and Gurfinkel, 2009; Berendsen et al., 2012). To screen root-associated microbes for their biological control activities is a difficult and timeconsuming process. Kamilova and colleagues (2005) described an enrichment method for enhanced competitive plant root tip colonizers that are able to reduce the tomato foot and root rot disease caused by the fungus Fusarium oxysporum f. sp. radicis-lycopersici (Forl). In this method, a mixture of bacteria isolated from the rhizosphere is applied on a sterile seedling and the best colonizer is collected from the plant root tip grown for 4 to 5 weeks in a gnotobiotic sand system (Kuiper et al., 2001). This cycle is repeated to get the best competitive root tip colonizers. We used this method to select enhanced salt-tolerant wheat root tip colonizers and those strains were able to protect cucumber and tomato against foot and root rot disease in salinated soil conditions (Egamberdieva et al., 2011, 2012). In this study, we observed that 17% of the cucumber plants grown in soil to which no Fusarium solani spores had been added were diseased, whereas in the presence of the pathogenic fungus 54% of the plants had disease symptoms (Figure 7.2). The bacterial strains also increased the dry weight of whole cucumber plants and fruit yield in a statistically significant way in comparison to the control. In another study, we observed that salttolerant selected bacterial strains (e.g., P. alcaligenes PsA15, B. amyloliquefaciens BcA12, P. chlororaphis TSAU13, and P. extremorientalis TSAU20) significantly (P , 0.05) reduced the damping-off of cotton caused by R. solani and F. oxysporum in salinated soil (Egamberdieva and Jabborova, 2013). The bacterial strains P. alcaligenes PsA15 and B. amyloliquefaciens BcA12 were also able to reduce Verticillium wilt of cotton plants under saline soil conditions. In addition, we evaluated the potential of selected root-colonizing bacterial strains for biological control of wheat root rot caused by F. culmorum. The presence of the pathogenic fungus caused disease symptoms in 47.9% of the plants (Figure 7.3). Disease severity in plants inoculated with the pathogen and bacterial strains was significantly less than the pathogen control. Results from the greenhouse pot experiment demonstrated that P. chlororaphis TSAU13, P. putida 1T1, S. rhizophila ep17, P. extremorientalis TSAU20, and

7.4 Biological control

Diseased seedling with Fusarium solani

165

P. extremorientalis TSAU20

FIGURE 7.2 Biological control of cucumber root rot caused by F. solani by P. extremorientalis TSAU20.

60

Diseased plants, %

50 40

*

30

*

*

*

*

20 10 0 F

TSAU13 TSAU1 TSAU6 TSAU20 TSAU22

1T1

3Re27

ep17

FIGURE 7.3 Control of wheat root rot in saline soil by selected bacterial isolates. Plants were grown in soil infested with F. culmorum; treatments were: F, control plants not treated with bacteria and seeds treated with bacterial inoculants; P. chlororaphis TSAU 13; P. putida TSAU 1, P. extremorientalis TSAU 6; P. extremorientalis TSAU 20; P. aureantiaca TSAU 22; P. putida 1T1; P. trivialis 3re27; and S. rhizophila ep17.

Significantly different from the control at P , 0.05.

166


P. aurantiaca TSAU22 isolates significantly inhibited wheat root rot caused by F. culmorum. In another study, Safiyazov et al. (1995) observed that three antagonistic bacteria, Pseudomonas fluorescens 41, Bacillus subtilis 23, and Bacillus megatherium 26, were able to control cotton diseases caused by Xanthomonas malvacearum, Rhizoctonia solani, Fusarium vasinfectum, and Verticillium dahlia under saline soil conditions. Several authors suggested that tolerance to high NaCl concentrations is an important bacterial property for successful colonization of the rhizosphere of plants grown in saline soil conditions (McInnes et al., 1994). Yao et al. (2010) reported that the Pseudomonas putida strain isolated from alkaline soil could increase the salt tolerance of cotton and improve growth in salinated soil. We also observed plant growth stimulation and biological control of cotton by salt-tolerant Pseudomonas strains in salinated soil (Egamberdieva and Jabborova, 2013). However, our followup investigations showed that tested strains, which were isolated from different plants grown in nonsaline soil and showed the best biocontrol abilities in saline soil, could also grow at a normal rate in the presence of up to 3% added NaCl (Egamberdieva et al., 2011). This result showed that for the application of bacteria in salinated soils there is no strict need to isolate the bacteria from plants grown in salinated soil. These findings are consistent with observations showing that the rhizosphere is characterized by changing osmotic conditions, and its microbial inhabitants can adapt to increased osmolarity—that is, by producing osmoprotective substances (Miller and Wood, 1996). The Stenotrophomonas strain is known for the production of osmoprotective substances in extraordinarily high amounts, which can contribute to its rhizosphere competence under salinated conditions (Berg et al., 2010). Altogether, the results showed that salt has no severe influence on bacterial plant-growth stimulation and biocontrol traits (Egamberdieva et al., 2011). Saleena et al. (2003) reported that Pseudomonas strains exhibiting antibiosis suppressed both bacterial leaf blight and sheath blight diseases in rice under both natural and saline soil conditions.

7.5 Mechanisms of action of plant growth-promoting rhizobacteria Plant growth-promoting rhizobacteria (PGPR) may protect plants from fungal pathogens using several mechanisms such as competition for niches or nutrients, parasitism that may involve production of hydrolytic enzymes, antibiosis, production of phytohormones, and induction of systemic resistance in host plants (Lugtenberg and Kamilova, 2009; Raaijmakers et al., 2009; Martıńez-Viveros et al., 2010). Several authors reported on the involvement of antibiosis in the biocontrol of plant pathogens (Aliye et al., 2008; Spaepen et al., 2009; Park et al., 2013). Every soil has a natural potential to suppress the activity of plant pathogens to some degree due to the presence and activity of soil microorganisms. These suppressive soils provide examples of biotic and abiotic factors affecting the pathogen, the plant, or the interaction between plant and pathogen (Alabouvette and Steinberg, 2006). We observed that 4.5% of bacterial strains isolated from the rhizosphere of wheat grown in nonsalinated soil were antagonistic against F. culmorum and F. oxysporum. Wheat-associated bacteria from salinated soil showed higher antagonistic activity, up to 15.5%. These results indicate that salinated soil may support high levels of antagonists, but disease incidence is also high in salinated soil compared to nonsaline soil. This indicates that a higher population of antagonists in

7.5 Mechanisms of action of plant growth-promoting rhizobacteria

1% NaCl

2% NaCl

167

3% NaCl

FIGURE 7.4 Antagonistic activity of P. chlororaphis TSAU13 affected by salinity (13% NaCl).

rhizosphere is not so important in disease suppression but their specific activities (e.g., antibiotic production, induction of host defense responses) are essential (Lewis and Papavizas, 1985). In our previous work, we also observed that the antagonistic activity of the salt-tolerant strain P. chlororaphis TSAU13 was not affected by salinity up to 3% NaCl (Figure 7.4). The strain was also able to produce cell wall-degrading enzymes (e.g., as cellulase, extracellular protease, glucanase, and chitinase) under saline conditions. The same results were shown by Martin (1995), who stated that the production of pectolytic enzymes by Pythium is decreased but not prevented at high salinity levels. According Sharaf and Farrag (2004), indole acetic acid (IAA) is able to reduce the infection rate of tomato wilt caused by Fusarium oxysporum lycopersici. In their study, disease suppression exerted by the application of IAA was achieved through either increasing plant growth by exerting a direct harmful affect on the target pathogen and/or by inducing resistance in host tissue. We also investigated whether IAA is one of the biological control mechanisms by using various indole acetic acid concentrations and IAA-producing bacteria for control of cucumber root rot caused by Fusarium solani in the gnotobiotic condition. The results showed that P. extremorientalis TSAU 20 and P. aureantiaca TSAU 22, which produce IAA, were able to reduce the infection rate of cucumber root rot (17%) caused by F. solani (Figure 7.5). Higher concentrations of IAA (0.01; 0.001 μg/ml) did not reduce disease incidence, whereas only a low concentration of IAA (0.0001 μg/ml) reduced diseased plants to 18%. Similar results were obtained by Fernández-Falcoń et al. (2003), where the exogenous application of indole acetic acid to banana plants induces resistance to Panama disease, and the resistance induction is more effective when performed using low doses and frequent applications. Rhizobacteria, which is able to protect plants from various diseases, result in significant effects when their survival in the rhizosphere is supported. Competition for the nutrients and niches in the rhizosphere is a fundamental mechanism by which PGPB protects plants from phytopathogens (Compant et al., 2005). There are several reports on potential root-colonizing bacteria, which may compete with fungal pathogens by competition for carbon and energy sources, that would provide a basis for biological control (Rekha et al., 2007; Egamberdieva and Kucharova, 2009; Lugtenberg and Kamilova, 2009). Paul and Nair (2008) also reported that the root-colonization potential of the salt-tolerant Pseudomonas strain was not hampered with higher salinity in soil. We observed that PGPR strains were able to colonize and survive on the roots of tomato and cucumber plants grown in salinated soil under greenhouse conditions. Increasing the salinity level did not negatively affect root colonization by Pseudomonas strains. Only the highest NaCl (10.0 dSm21) concentration decreased the number of bacteria colonizing cucumber and tomato roots.

168


60

Diseased plants, %

50

40

*

30

*

*

IAA(0,0001)

TSAU20

20

10

0 F

IAA(0,01)

IAA(0,001)

TSAU22

FIGURE 7.5 Control of cucumber root rot caused by F. solani in gnotobiotic condition by IAA-producing bacteria P. extremorientalis TSAU 20, P. aureantiaca TSAU 22, and IAA. Plants were grown in soil infested with F. solani; treatments were: F, control plants not treated with bacteria and IAA; seeds treated with 0.01, 0.001, and 0.0001 μg/ml IAA and bacterial inoculants; P. extremorientalis TSAU 20; and P. aureantiaca TSAU 22.

Significantly different from the control at P , 0.05.

7.6 Conclusion and future prospects This review has shown that there is potential for the use of PGPR as biocontrol agents for a wide variety of crop plants under extreme climatic conditions. They are able to increase plant growth tolerance to salt stress and protect plants from various soil-borne pathogens. However, there are few scientific challenges for research in the field of biocontrol under salinated soil conditions. There is also good evidence for the involvement of phytohormone auxin, antibiotics, and HCN in the biocontrol of plant root diseases by PGPR. Knowledge of the mechanisms contributing to plant protection by plant growth-promoting rhizobacteria, as well as the constraints to their activity under several conditions, can facilitate more effective use of biological control agents. Thus, further research should be directed to optimizing biocontrol methods for soil-borne diseases and determining the feasibility of using such agents under severe environmental conditions. In addition, it will be important to exploit molecular techniques to study the mechanisms of action used by plantbeneficial rhizobacteria to protect plants from various diseases in saline soil. More detailed studies are needed on the survival of biological control agents under harsh conditions, the role of abiotic factors in altering the activity of rhizobacteria, and managing plant microbe interactions with respect to their adaptability to conditions under extreme environments. Our understanding of the plantmicrobe interaction in the rhizosphere of plants grown in stressed environments must increase before we can use PGPR as biofertilizer for sustainable production of crops under severe conditions. This could contribute greater evidence indicating that biocontrol agents based on PGPR may reduce improper use of chemical pesticides under stressed soil conditions.

References

169

References Adesemoye, A.O., Torbert, H.A., Kloepper, J.W., 2008. Enhanced plant nutrient use efficiency with PGPR and AMF in an integrated nutrient management system. Can. J. Microbiol. 54, 876886. Ahmad, P., Sharma, S., 2008. Salt stress and phytobiochemical responses of plants. Plant Soil J. 54 (3), 8999. Ahmad, P., Hakeem, K.R., Kumar, A., Ashraf, M., Akram, N.A., 2012. Salt-induced changes in photosynthetic activity and oxidative defense system of three cultivars of mustard (Brassica juncea L.). Afr. J. Biotech. 11, 26942703. Alabouvette, C., Steinberg, C., 2006. An ecological and societal approach to biological control. Prog. Biol. Cont. 2, 123144. Aliye, N., Fininsa, C., Hiskias, Y., 2008. Evaluation of rhizosphere bacterial antagonists for their potential to bioprotect potato (Solanum tuberosum) against bacterial wilt (Ralstonia solanacearum). Biol. Cont. 47 (3), 282288. Arora, N.K., Khare, E., Oh, J.H., Kang, S.K., Maheshwari, D.K., 2008. Diverse mechanisms adopted by fluorescent Pseudomonas PGC2 during the inhibition of Rhizoctonia solani and Phytophtora capsici. World J. Microb. Biotech. 24, 581585. Berendsen, R.L., Pieterse, C.M.J., Bakker, P.A.H.M., 2012. The rhizosphere microbiome and plant health. Trends Plant Sci. 17 (8), 478486. Berg, G., Egamberdieva, D., Lugtenberg, B., Hagemann, M., 2010. Symbiotic plant-microbe interactions: stress protection, plant growth promotion and biocontrol by Stenotrophomonas. In: Seckbach, J.J., Grube, M. (Eds.), Symbioses and Stress, Cellular Origin, Life in Extreme Habitats and Astrobiology. Springer-Verlag, Dordrecht, 17(4), pp. 445460. Bernard, E., Larkin, R.P., Tavantzis, S., Erich, M.S., Alyokhin, A., Sewell, G., et al., 2012. Compost, rapeseed rotation, and biocontrol agents significantly impact soil microbial communities in organic and conventional potato production systems. Appl. Soil Ecol. 52, 2941. Besri, M., 1993. Effects of salinity on plant diseases development. In: Towards the Rational Use of High Salinity Tolerant Plants. Lieth, H., Al Masoom, A. (Eds.), vol. 28. Springer, Netherlands, pp. 6774. Blaker, N.S., MacDonald, J.D., 1985. The effect of soil salinity on formation of sporangia and zoospores by three isolates of Phytophthora. Phytopathology 75, 270274. Blaker, N.S., MacDonald, J.D., 1986. The role of salinity in the development of Phytophthora root rot of citrus. Phytopathology 6, 970975. Blodgett, J.T., Kruger, E.L., Stanosz, G.R., 1997. Effects of moderate water stress on disease development by Sphaeropsis sapinea on red pine. Phytopathology 87, 422428. Compant, S., Duffy, B., Nowak, J., Clément, C., Barka, E.A., 2005. Use of plant growth-promoting bacteria for biocontrol of plant diseases: principles, mechanisms of action, and future prospects. Appl. Environ. Microbiol. 49514959. Compant, S., Clément, C., Sessitsch, A., 2010. Plant growth-promoting bacteria in the rhizo- and endosphere of plants: their role, colonization, mechanisms involved and prospects for utilization. Soil Biol. Biochem. 42, 669678. Crépin, A., Barbey, C., Cirou, A., Tannie`res, M., Orange, N., Feuilloley, M., et al., 2012. Biological control of pathogen communication in the rhizosphere: a novel approach applied to potato soft rot due to Pectobacterium atrosepticum. Plant Soil 358, 2737. Cummings, S.P., 2009. The application of plant growth promoting rhizobacteria (PGPR) in low input and organic cultivation of graminaceous crops; potential and problems. Env. Biotech. 5 (2), 4350. Daami-Remadi, M., Sayes, S., Horrigue-Raouani, N., Hassine, H.W., 2009. Effects of Verticillium dahliae Kleb., Fusarium oxysporum Schlecht. f. sp. tuberosi Snyder, Hansen and Meloidogyne javanica (Treub.)

170


chitwood inoculated individually or in combination on potato growth, wilt severity and nematode development. Afr. J. Microb. Res. 3, 595604. Dodd, I.C., Perez-Alfocea, F., 2012. Microbial alleviation of crop salinity. J. Exp. Bot. 63, 34153428. Egamberdieva, D., Jabborova, D., 2013. Biocontrol of cotton damping-off caused by Rhizoctonia solani in salinated soil with rhizosphere bacteria. Asian Austral. J. Plant Sci. Biotech. 7 (2), 3138. Egamberdieva, D., Kucharova, Z., 2009. Selection for root colonizing bacteria stimulating wheat growth in saline soils. Biol. Fertil. Soil 45, 563571. Egamberdieva, D., Kamilova, F., Validov, S., Gafurova, L., Kucharova, Z., Lugtenberg, B., 2008. High incidence of plant growth-stimulating bacteria associated with the Rhizosphere of wheat grown in salinated soil in Uzbekistan. Env. Microb. 19, 119. Egamberdieva, D., Kucharova, Z., Davranov, K., Berg, G., Makarova, N., Azarova, T., et al., 2011. Bacteria able to control foot and root rot and to promote growth of cucumber in salinated soils. Biol. Fertil. Soil 47, 197205. Egamberdieva, D., Berg, G., Chebotar, V., Tikhonovich, I., Kamilova, F., Validov S., et al., 2012. Bacteria controlling foot and root rot and promoting growth of cucumber and tomato in salinated soil. In: Biological control of fungal and plant pathogens. Pertot, I., Elad, Y., Gessler, C. (Eds.), vol. 78. IOBC/ WPRS, 107112. Egamberdieva, D., Berg, G., Lindstro¨m, K., Ra¨sa¨nen, L.A., 2013. Alleviation of salt stress of symbiotic Galega officinalis L. (Goat’s Rue) by co-inoculation of rhizobium with root colonising Pseudomonas. Plant Soil 369 (1), 453465. Egamberdiyeva, D., Islam, K.R., 2008. Salt tolerant rhizobacteria: plant growth promoting traits and physiological characterization within ecologically stressed environment. In: Ahmad, I., Pichtel, J., Hayat, S. (Eds.), Plant-Bacteria Interactions: Strategies and Techniques to Promote Plant Growth. Wiley-VCH Verlag GmbH & Co., KGaA, Weinheim, Germany, pp. 257281. Egamberdiyeva, D., Kucharova, Z., 2007. Managing fungal diseases of tomato and wheat by potential biocontrol agents in salinated soils of Uzbekistan. In: Best Practice in Disease, Pest and Weed Management: The State of the Art. Alford, D.V., Feldmann, F., Hasler, J., Von Tiedemann, A., (Eds.), British Crop Protection Council, pp. 6465. El-Abyad, M.S., Hindorf, H., Rizk, M.A., 1988. Impact of salinity stress on soil-borne fungi of sugar beet. II. Growth activities in vitro. Plant Soil 110, 3337. Esechie, H.A., Al-Saidi, A., Al-Khanjari, A., 2002. Effect of sodium chloride salinity on seedling emergence in chickpea. J. Agron. Crop Sci. 188, 155160. Fernández-Falcoń, M., Borges, A.A., Borges-Pérez, B., 2003. Induced resistance to Fusarium wilt of banana by exogenous applications of indoleacetic acid. Phytoprotection 84, 149153. Gasoni, L., de Gurfinkel, B.S., 2009. Biocontrol of Rhizoctonia solani by the endophytic fungus Cladorrhinum foecundissimum in cotton plants. Aust. Plant Path. 38, 389391. Goudarzi, S., Banihashemi, Z., Maftoun, M., 2011. Effect of salt and water stress on root infection by Macrophomina phaseolina and ion composition in shoot in sorghum. Iran J. Plant Path. 47 (3), 6983. Hinsinger, P., Plassard, C., Jaillard, B., 2006. Rhizosphere: a new frontier for soil biogeochemistry. Geochem. J. Explor. 88, 210213. Ilyas, N., Bano, A., Iqbal, S., Raja, N.J., 2012. Physiological, biochemical and molecular characterization of Azospirillum spp., isolated from maize under water stress. Pak. J. Bot. 44 (1), 7180. Kamilova, F., Validov, S., Azarova, T., Mulders, I., Lugtenberg, B., 2005. Enrichment for enhanced competitive plant root tip colonizers selects for a new class of biocontrol bacteria. Environ. Microbiol. 7, 18091817. Kuiper, I., Bloemberg, G.V., Lugtenberg, B.J., 2001. Selection of a plant-bacterium pair as a novel tool for rhizostimulation of polycyclic aromatic hydrocarbon-(PAH)-degrading bacteria. Mol. Plant-Microbe Inter. 14, 11971205.

References

171

Landa, B.B., Navas-Cortés, J.A., Jiménez-Dıáza, R.M., 2004. Influence of temperature on plantrhizobacteria interactions related to biocontrol potential for suppression of Fusarium wilt of chickpea. Plant Pathol. 53, 341352. Lewis, J.A., Papavizas, G.C., 1985. Effect of mycelial preparation of Trichoderma and Gliocladium on population of Rhizoctonia solani and the incidence of damping-off. Phytopathology 75, 812817. Li, R., Zhang, H., Liu, W., Zheng, X., 2011. Biocontrol of postharvest gray and blue mold decay of apples with Rhodotorula mucilaginosa and possible mechanisms of action. Int. J. Food Microbiol. 146 (2), 151156. Luduenã, L.M., Taurian, T., Tonelli, M.L., Angelini, J.G., Anzuay, M.S., Valetti, L., et al., 2012. Biocontrol bacterial communities associated with diseased peanut (Arachis hypogaea L.) plants. Eur. J. Soil Biol. 53, 4855. Lugtenberg, B., Kamilova, F., 2009. Plant-growth-promoting rhizobacteria. Annu. Rev. Microbiol. 63, 541556. Lugtenberg, B.J.J., Dekkers, L., Bloemberg, G.V., 2001. Molecular determinants of rhizosphere colonization by Pseudomanas. Annu. Rev. Phytopathol. 39, 461490. Ma, Z., Morgan, D.P., Michlailides, T.J., 2001. Effects of water stress on Botryosphaeria blight of pistachio caused by Botryosphaeria dothidea. Plant Dis. 85, 745749. Martin, F.N., 1995. Pythium. In: Kohmoto, K., Singh, U.S., Singh, R.P. (Eds.), Pathogenesis and Host Specificity in Plant Diseases; Histopathological, Biochemical, Genetic and Molecular Bases. Elsevier, Oxford, pp. 1736. Martinez-Beltran J., Manzur C.L., 2005. Overview of salinity problems in the world and FAO strategies to address the problem. In: Proceedings of the International Salinity Forum. Riverside, California, pp. 311313. Martıńez-Viveros, O., Jorquera, M.A., Crowley, D.E., Gajardo, G., Mora, M., 2010. Mechanisms and practical considerations involved in plant growth promotion by rhizobacteria. J. Soil Sci. Plant Nutr. 10, 293319. Mayak, S., Tirosh, T., Glick, B.R., 2004. Plant growth-promoting bacteria that confer resistance to water stress in tomatoes and peppers. Plant Sci. 166, 525530. McInnes, K.J., Weaver, R.W., Savage, M.J., 1994. Soil water potential. In: Weaver, R.W., Angle, S., Bottomley, P., Bezdicek, D., Smith, S., Tabatabai, A., Wollum, A. (Eds.), Methods of Soil Analysis. Microbiological and Biochemical Properties. Soil Science Society of America, Inc., Madison, WI, pp. 5358. Miller, K.J., Wood, J.M., 1996. Osmoadaptation by rhizosphere bacteria. Annu. Rev. Microbiol. 50, 101136. Nannipieri, P., Ascher, J., Ceccherini, M.T., Landi, L., Pietramellara, G., Renella, G., 2003. Microbial diversity and soil functions. Eur. J. Soil Sci. 54, 655667. Park, J.W., Balaraju, K., Kim, I.W., Lee, S.W., Park, K., 2013. Systemic resistance and growth promotion of chili pepper induced by an antibiotic producing Bacillus vallismortis strain BS07. Biol. Cont. 65 (2), 246257. Paul, D., Nair, S., 2008. Stress adaptations in a plant growth promoting rhizobacterium (PGPR) with increasing salinity in the coastal agricultural soils. J. Basic Microbiol. 48 (5), 378384. Pimentel, D., Levitan, L., 1986. Pesticides: amounts applied and amounts reaching pests. BioScience 36, 8691. Pimentel, D., McLaughlin, L., Zepp, A., Lakitan, B., Kraus, T., Kleinman, P., et al., 1993. Environmental and economic effects of reducing pesticide use in agriculture. Agr. Ecos. Env. 46, 273288. Raaijmakers, J.M., Paulitz, T.C., Steinberg, C., Alabouvette, C., Moe¨nne-Loccoz, Y., 2009. The rhizosphere: a playground and battlefield for soilborne pathogens and beneficial microorganisms. Plant Soil 321, 341361. Ragazzi, A., Vecchio, V., Dellavalle, I., Cucchi, A., Mancini, F., 1994. Variations in the pathogenicity Fusarium oxysporum f.sp. vasinfectum in relation to salinity of the nutrient medium. Z Pflanzenk. Pflanzenschutz 101, 263266.

172


Ramette, A., Frapolli, M., Saux, M.F., Gruffaz, C., Meyer, J.M., Défago, G., et al., 2011. Pseudomonas protegens sp. nov., widespread plant-protecting bacteria producing the biocontrol compounds 2,4-diacetylphloroglucinol and pyoluteorin. Syst. Appl. Microbiol. 34 (3), 180188. Rangarajan, S., Saleena, L.M., Vasudevan, P., Nair, S., 2003. Biological suppression of rice diseases by Pseudomonas spp. under saline soil conditions. Plant Soil 251, 7382. Rasmussen, S.L., Stanghellini, M.E., 1988. Effect of salt stress on development of Pythium blight in Agrostis palustris. Phytopathology 78, 14951497. Rekha, P.D., Lai, W.A., Arun, A.B., Young, C.C., 2007. Effect of free and encapsulated Pseudomonas putida CC-FR2-4 and Bacillus subtilis CC-pg104 on plant growth under gnotobiotic conditions. Bio. Res. Tech. 98, 447451. Requena, N., Pérez-Solis, E., Azcoń-Aguilar, C., Jeffries, P., Barea, J.M., 2001. Management of indigenous plant-microbe symbioses aids restoration of desertified ecosystems. Appl. Environ. Microbiol. 67, 495498. Safiyazov, J.S., Mannanov, R.N., Sattarova, R.K., 1995. The use of bacterial antagonists for the control of cotton diseases. Field Crops Res. 43, 5154. Saleena, L.M., Vasudevan, P., Nair, S., 2003. Biological suppression of rice diseases by Pseudomonas spp. under saline soil conditions. Plant Soil 251 (1), 7382. Sanogo, S., 2004. Response of chile pepper to Phytophthora capsici in relation to soil salinity. Plant Dis. 88, 205209. Sharaf, E.F., Farrag, A.A., 2004. Induced resistance in tomato plants by IAA against Fusarium oxysporum lycopersici. Pol. J. Microbiol. 53 (2), 111116. Spaepen, S., Vanderleyden, J., Okon, Y., 2009. Plant growth-promoting actions of Rhizobacteria. Adv. Bot. Res. 51, 283320. Swiecki, T.J., MacDonald, J.D., 1988. Histology of chrysanthemum roots exposed to salinity and Phytophthora cryptogea. Can. J. Bot. 66, 280288. Swieckil, T.J., MacDonald, J.D., 1991. Soil salinity enhances phytophthora root rot of tomato but hinders asexual reproduction by Phytophthora parasitic. J. Am. Soc. Hort. Sci. 116 (3), 471477. Trabelsi, D., Mengoni, A., Aouani, M.E., Mhamdi, R., Bazzicalupo, M., 2009. Genetic diversity and salt tolerance of bacterial communities from two Tunisian soils. Annu. Microbiol. 59 (1), 2532. Triky-Dotan, S., Yermiyahu, U., Katan, J., Gamliel, A., 2005. Development of crown and root rot disease of tomato under irrigation with saline water. Phytopathology 95, 14381444. Tripathi, A.K., Verma, S.C., Ron, E.Z., 2002. Molecular characterization of a salt-tolerant bacterial community in the rice rhizosphere. Res. Microbiol. 153, 579584. Wahyudi, A.T., Astuti, R.P., Widyawati, A., Meryandini, A., Nawangsih, A.A., 2011. Characterization of Bacillus sp. strains isolated from rhizosphere of soybean plants for their use as potential plant growth for promoting Rhizobacteria. J. Microbiol. Antimicrob. 3 (2), 3440. Yao, L., Wu, Z., Zheng, Y., Kaleem, I., Li, C., 2010. Growth promotion and protection against salt stress by Pseudomonas putida Rs-198 on cotton. Eur. J. Soil Biol. 46 (1), 4954. Yasmin, H., Bano, A., Samiullah, 2013. Screening of PGPR isolates from semi-arid region and their implication to alleviate drought stress. Pak. J. Bot. 45 (SI), 5158. Yildirim, E., Turan, M., Donmez, M.F., 2008. Mitigation of salt stress in radish (Raphanus Sativus l.) by plant growth promoting rhizobacteria. Roum. Biotechnol. Lett. 13 (5), 39333943. Zhang, H., Ma, L., Turner, M., Xu, H., Zheng, X., Dong, Y., et al., 2010. Salicylic acid enhances biocontrol efficacy of Rhodotorula glutinis against postharvest Rhizopus rot of strawberries and the possible mechanisms involved. Food Chem. 122 (3), 577583.

CHAPTER

Crop Plants under Saline-Adapted Fungal Pathogens: An Overview

8

Murat Dikilitas and Sema Karakas

8.1 Introduction In the past, researchers directed their attention to either the relationship between plants and abiotic stress or between plants and pathogens. There are also relationships between abiotic stresses, such as drought, salinity, and so on, and microorganisms that cannot be ignored. Therefore, the newer concept being addressed is the interactions between plants, pathogens, and abiotic stress. Although pathogen-induced diseases or abiotic stressors may have a detrimental effect on crop production and quality, new methods have been proposed to protect plants from biotic and abiotic stress factors. For example, virus, fungi, bacteria, and nematode-resistant plants and salt, heat, drought, and cold-tolerant plants have gained much attention in the presence of climatic change. These stresstolerant plants can be crucially important to increasing crop yield in salt-affected areas. However, the loss of salt tolerance or disease resistance of crop plants as well as an increase of the virulence of the plant pathogens should be taken into account. There are quite a few reports about crop plants’ loss of salt tolerance or the increase in the pathogenicity of fungal elements after time (Krokene and Solheim, 2001; Dikilitas, 2003; Dikilitas et al., 2011a). As a result of this, we may have to start to produce new stress-tolerant lines. Genetically engineered plants with increased disease resistance or stress tolerance may overcome the negative effects of stress for a period of time, although this is a major challenge for biotechnologists. Most attempts to develop crops resistant to fungal and bacterial diseases or abiotic stress factors through genetic engineering, however, have been unsuccessful in the long term due to the status of resistance (R) genes that are extremely vulnerable to a single loss-of-function mutation in the corresponding pathogen, Avr gene, which may eventually lead to loss of resistance in crop plants (Rougon-Cardoso and Zipfel, 2010). Increasing resistance to a particular plant pathogen or to a particular abiotic stress factor does not resolve the problem arising from the attack of multiple plant pathogens or multiple abiotic stressors as well as the problems that arise from the combined effect of pathogens and salt. Therefore, increasing resistance to a broad range of plant pathogens, or the negative effects of both salt and pathogens, are vitally important. The most important issue is to evaluate the pathological effects of fungi under saline stress conditions in which they may either evolve or adapt themselves. The fungi may be suppressed by the effects of salinity and lose their ability to produce enough


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conidia and mycelia to infect the host plant. However, if they do tolerate the negative effects of salinity as the crop plants do, the fungi may then easily pass the plants’ defense barriers without exerting remarkable force. In this chapter, we outline the possible behavior of fungal plant pathogens under saline conditions; in particular, the interactions between salinity and fungi and the pathological effects of fungi on crop plants under salinity stress were analyzed. Because it is well known that the response of plants to infection by disease can be modified by environmental factors, the behavior of plant pathogens on crop plants may also be affected by environmental factors such as salinity and drought. Under these circumstances, the potential interaction between salinity and the disease is a realistic possibility that must be seriously considered and tackled. The demand for food is increasing globally; therefore low-fertility agricultural areas, as well as polluted areas, need to be used for agricultural purposes to cope with hunger. However, marginal areas characterized by salinity and pollution bring major problems when stress-tolerant crop plants are cultivated in them. It is known that the behavior and characteristics of plant pathogens, as well as saprophytic or antagonistic agents of microorganisms, change due to adverse conditions. Any microbial population as pathogens in the vicinity of crop plants’ roots may have the capacity to adapt themselves to marginal conditions where highly virulent salt-tolerant races of pathogens may be able survive. The soil quality of such fields, therefore, needs to be determined and improved in order to make them usable for agricultural purposes. Apart from the preceding issues, there are many reasons for salinity problems. Instead of evaluating those issues, the effect of salinity on plant growth and metabolism is discussed and highlighted before we move on to an evaluation of salinity stress on fungi.

8.2 Effects of salinity on crop plants Salinity is a global problem for agriculturists, especially for crops being irrigated. The presence of even a small concentration of salt in good quality irrigation water results in salt accumulation in soils unless leached away. On the other hand, excess irrigation without drainage results in a rise in the groundwater level that eventually leads to salt accumulation on the surface of the soil (Bridges, 1997; Dikilitas and Karakas, 2010). Salinity may also result from the accumulation of compost in the form of potassium, nitrate, and chloride. Soil salinity inhibits plant growth and development with adverse effects such as osmotic stress, Na1 and Cl2 ion toxicity, ethylene production, nutrient imbalance, production of reactive oxygen species (ROS), and plasmolysis (Dikilitas, 2003; Sairam and Tyagi, 2004). When plants are exposed to a high level of salinity, a decrease in the growth rate is the plants’ first response along with symptoms of chlorosis, leaf drop, wilting, and root death (Johnson, 2000). Once salt is taken up, Na1 is easily translocated to shoots and leaves through the transpiration stream in the xylem. Although the return of Na1 to roots via phloem can occur, this flow is minimal. Therefore, the accumulation of Na1 is higher in leaves and shoots than in roots (Tester and Davenport, 2003). On the other hand, vegetative tissues are fed mainly through the xylem and thus tend to have higher Na1 levels. The metabolic toxicity of Na1 is generally atrributed to Na1 competition with K1 for binding sites because potassium ion is essential for cellular functioning (e.g., enzyme, chlorophyll synthesis, and stomatal). Competition of Na1 was also reported with Ca21 ions in the root medium (Flowers, 2004).

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Similar disorders also were observed with limited Ca21 translocation under salinity stress (Dajic, 2006). Under these conditions, the cell wall membrane becomes fragile and lysed, leading to continuous outflow of assimilates (e.g., sugars and amino acids) that possibly facilitate fungal growth. Salinity can also cause a reduction in photosynthesis with an increase of Cl2 toxicity. For example, Monirifar and Barghi (2009) stated that the reduction in chlorophyll content in lucerne plants was correlated with Cl2 accumulation; although, the Cl2 ion is essential as a micronutrient for plant growth and is involved in photosynthesis and maintaining electrical neutrality in membranes. The excess intake of Cl2 from soil or substrate to xylem vessel elements through the symplastic pathway results in electrolyte leakage and membrane instability as well as toxicity to photosynthetic organs. Salinity also alters the hormone balance in plants (Ruiz et al., 2013; Sugano et al., 2013). An increase in salinity stress causes a decrease in the transport of kinetin from roots to leaves and results in an increase in the content of abscisic acid in the leaf. These changes can cause a decrease in somatal aperture and leaf abscission (Nadeem et al., 2010). An increase in ethylene production also is associated with salinity in crop plants. For example, Shibli et al. (2007) stated that elevated salinity treatments (i.e., 0, 50, 100, 150, and 200 mM NaCl) significantly enhanced ethylene accumulation in tomato cultivars, and this was accompanied with increased leaf epinasty. In addition, salinity may affect germination of crop plants in two ways: (1) by either creating a low osmotic potential that reduces or prevents water uptake or (2) by providing conditions for the entry of ions that may be toxic to the embryo or developing seedlings (Sosa et al., 2005). Apart from the reduction in germination, salinity may also delay growth. Salinity may cause changes in plant metabolism too. Various metabolites (e.g., proline and betaine) and many antioxidant enzymes are activated by either increased or decreased metabolite levels. For example, several hypotheses have been put forward to explain the role of proline accumulation under stress conditions. It certainly regulates and reduces water loss from the cell during or after stress; it addition, it may act as a sink for the nitrogen from nitrogenous compounds. Proline may also act as a substrate for respiration that may provide the energy needed for recovery from the effect of stress (Hare and Cress, 1997; Arfan, 2009). Some researchers, although, suggested that proline accumulation was neither a sensitive indicator of salinity nor of protective measure, rather merely a symptom of injury (Hadson and Hitz, 1982). Most studies have shown that a positive correlation between proline accumulation and adaptation to salt and/or drought stress was evident (Aghaleh et al., 2009). With this finding, it has been shown that the addition of proline to a salt-supplemented medium enhances the growth and survival of unselected cells in a number of species (Chaudhary, 1996; Al-Rawahy, 2000; Namdjoyana and Kermanian, 2013). Proline application also increases the production of antioxidant enzymes (e.g., superoxide dismutase and peroxidase) as well as other metabolites in stressed plants (Hua and Guo, 2002; Ben Ahmed et al., 2011). Sorkheh et al. (2012) and Abdelhamid et al. (2013) reported that foliar application of proline not only increased the growth parameters but also decreased Na1 ion concentration. Similar achievements were made by using L-phenylalanine and laminarin on the growth of nonsalt-adapted plants (Meszka and Bielenin, 2011; Syklowska-Baranek et al., 2012). Several methods and approaches have been proposed for agricultural areas where salinity was the main problem; ones for salinity management have been evaluated in the work of Qadir et al. (2002). When salinity management involved crop plants, the common methods for enhanced

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salinity tolerance included genetic, physiological, and biochemical approaches. For example, salttolerant cell lines of lucerne were selected and maintained under in vitro conditions for several years and the plants were finally regenerated as salt tolerant (Al-Rawahy, 2000; Dikilitas, 2003). As reported from previous studies, biochemical or genetic approaches for salt tolerance have not always brought success for the crop plants exposed to saline conditions. Those plants either eventually lost their tolerance to salt or they did not show as high a salt tolerance as desired after regeneration (Dikilitas, 2003). When they brought some success and hope for the marginal areas, their resistance to disease stress was either neglected or did not get enough attention from the plant breeders.

8.3 Effects of salinity on fungi Environmental conditions, such as temperature, or conditions specific to the pathogen (e.g., the concentration of conidia, age of culture, or method of inoculation) may have effects on the virulence of the pathogen (Howell and Erwin, 1995; Dikilitas, 2003; Roos et al., 2011). These effects may increase or decrease the virulence of the pathogen in soil fauna. Because most semiarid and arid areas of the world are characterized by soil salinity, any changes in plant pathogens’ behavior to adverse conditions with respect to physiological and biochemical conditions are inevitable.

8.3.1 Negative effects of salinity on fungal growth Fungi, such as glycophytes, are negatively affected because they are not able to tolerate the adverse effect of salinity. Their salt-tolerance mechanism is similar to that of crop plants (Mahmoud et al., 2007). High salt concentrations lower the production of mycelia, conidial formation, and sporulation of fungi through the effects of negative osmotic potential as well as toxic and nutritional effects (Jones et al., 2011; Egamberdieva, 2012). Chandler et al. (1994) reported that the conidial germination and the mycelial growth of Verticillium species were declined under reduced osmotic potential. Similar findings were also made by McQuilken et al. (1992) and Goudarzi et al. (2008) on the sporulation of Pythium oligandrum and Macrophomina phaseolina. Through its negative effect, salinity may be used as a control agent to suppress the growth of fungi and the progress of disease. It has been reported that the individual application of sodium or calcium, or their combination with fungicides or biological control agents (Saccharomyces cerevisiae), effectively controlled diseases in vegetative growth periods as well as in postharvest stages through the suppressive effects of those compounds. For example, Amir et al. (1996) reported that salinity resulted in soil suppressiveness to Fusarium oxysporum, a fungal agent of vascular wilt disease, through reduced germination of conidia and mycelial growth. They suggested that the reduced number of propagules by soil salinity may prevent extensive pathogen distribution. They proposed that the roots of crop plants may be protected from infecting fungi in this way. Similar findings were made by Engel and Grey (1991) who stated that chloride fertilizers reduced the severity of root diseases of winter wheat caused by Fusarium culmorum. By using this, a remarkable increase in crop productivity was enabled. Toxicity of Na1 or Cl2 ions also encouraged the entomologs to control pests in crops. For example, Araya et al. (1991) stated that irrigating wheat and barley seedlings with saline Arnon and Hoagland solution (0700 mM NaCl) resulted in a decrease in the population and growth rate of the aphids Schizaphis graminum and Rhopalosiphum

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padi due to a high accumulation of Na1 and Cl2 ions in the leaves. Kostandi and Soliman (1998) also stated that the effect of saline irrigation containing NaCl or Na2SO4 reduced smut occurrence by 22.7% and 10.8%, respectively; and natural salt excretion was thought to be a possible defense mechanism. For example, salt excretion in leaves of some mangrove species served as an important defense against fungal attack in mangrove forests. Because the species is unsual in its ability to grow and tolerate high salinity, mangrove may also be unusual in its escape from intense disease pressures even when growing at high densities (Gilbert et al., 2002). The detrimental effects of salinity on fungi inspired some researchers to take the lead in offering alternative control strategies for pathogen fungi. For example, Mecteau et al. (2002) reported that potato dry rot caused by Fusarium sambucinum, which is a major postharvest disease of economic importance, was controlled by applying various sodium or potassium salts (0.2 M) onto the surface of potatoes following harvest. Application of sodium metabisulfite, sodium carbonate, sodium bicarbonate, and aluminum chloride caused a significant reduction in the development of dry rot in potato in vivo. Similar results were obtained with Fusarium solani var. coeruleum by Mecteau et al. (2008). El-Mougy and Abdel-Kader (2009) reported similar results for early potato blight disease caused by Alternaria solani. Recently, Hasan et al. (2012) reported that the application of sodium bicarbonate suppressed the mycelial growth and spore germination of Colletotrichum gloeosporioides, the postharvest anthracnose disease agent of papaya. In this way, disease severity was reduced to 60% compared to those of a group of plants to which it was not applied. A combination of salts and antifungal products was also used to enable efficient control of diseases. For example, application of potassium bicarbonate with Nerol, a commercial antifungal product of essential citrus oil fractions, significantly reduced the occurrence of the early blight disease of potato plants caused by Alternaria solani (Abd-El-Kareem, 2007). In some studies, even application of NaCl to fields was suggested. For example, Elmer (1992) reported that the limited distribution and development of Fusarium crown and root rot caused by Fusarium oxysporum and F. proliferatum was enabled with the application of NaCl. Similarly, Reid et al. (2001) tested the toxic effects of NaCl in Fusarium-contamined asparagus beds. Nevertheless, they did not recommend the use of NaCl on fungi in such productive fields. Recently, salt application was also used on papaya before harvest (Madani et al., 2014). They applied six preharvest calcium sprays to reduce the anthracnose disease caused by Colletotrichum gloeosporioides Penz. Madani et al. also managed to reduce the germination of conidia of Colletotrichum; possibly this was a result of its toxicity and reduced osmotic potential in fungal cells and the inhibiting cell wall degrading enzymes produced by the pathogen (Wisniewski et al., 1995). Although the negative effects of salt on fungi were generally through the fungistatic effect of NaCl, potential dangers and affects of NaCl on plants have been discussed and evaluated previously in many studies. For example, Bhai et al. (2009) reported that the mycelial growth, sporangial formation, and zoospore germination of Phytophthora capsici were inhibited in vitro at 1 M, 0.75 M, and 0.5 M NaCl concentrations, respectively. However, much higher concentrations of NaCl than those were needed to destroy the soil inoculum level in vivo which was quite phytotoxic. Their suggestion was to wash off the soils to nullify the phytotoxic effect of NaCl; however, this would not be practical in fields and can only be applied to the pots of contaminated soils. Similarly, Wenneker and Kanne (2010) suggested using a potassium bicarbonate formulation (Armicab) to control the powdery mildew (Sphaerotheca mors-uvae) of gooseberry in organic growing fields. Because sulfur is a fungicide against powdery mildew in gooseberry or table grape,

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it is not recommended due to its possible bleaching and scorching effects on berries and shoots. The weekly spraying of fruits reduced the disease significantly. Earlier, Nigro et al. (2006) stated that salts (e.g., calcium chloride, potassium carbonate, and sodium bicarbonate) showed an activity or similarity to that of conventional chemical treatments. However, the number of applications of spray to crops was reported to be high because long-lasting action of salts on crops cannot be expected—the salts are quickly converted into an ineffective compound and washed off by even a small amount of precipitation (Wenneker and Kanne, 2010). Generally, the conditions required for sporulation are more specific and narrower than the conditions required for mycelium development and the spread of fungus. For example, the conidial germination of Cryphonectria parasitica (Murr.), a fungal agent of chestnut blight, showed more susceptibility to NaCl at a 22.0 MPa osmotic potential than that of mycelial growth (Gao and Shain, 1995). In some studies, mycelial growth of fungi was not even affected although the production of metabolites was affected significantly. For example, the mycelial growth of F. oxysporum was either increased or not affected very much in differing NaCl concentrations (110% NaCl), although the synthesis of gibberellic acid (GA) and indole acetic acid (IAA) showed a drastic decline of more than 1% NaCl (Hasan, 2002). Similarly, the growth of wilt fungi, V. dahliae and V. albo-atrum, on potato dextrose agar (PDA) or Dox media containing 50 to 350 mM NaCl declined with the increase of NaCl; however, the behavior of the conidia of those fungi were not impaired (Danti and Broggio, 1997; Dikilitas, 2003; Goudarzi and Pakniyat, 2008). Negative effects of salt application on fungi encouraged horticulturists to control postharvest diseases, because ions from salt showed an inhibitory activity against mycelial development and spore germination. For example, Qin et al. (2010) used boron, an essential plant micronutrient, in the form of potassium tetraborate for control of postharvest gray mold caused by Botrytis cinerea on table grapes stored at room temperature or at 0 C. They suggested that boron resulted in the breakdown of the cell membrane and cytoplasmic materials from the hyphae. Similarly, sodium bicarbonate at 2% provided a great measure of fungicidal activity against Botrytis and Penicillium rot in apple and Monilinia and Rhizopus rot in peach. When combined with Aspire, a commercially available biocontrol agent, its curative and protective effect significantly increased (Droby et al., 2003). Application of salts, especially salts with calcium, provide a good control for rot. It is presumed that an early application of calcium chloride favors the penetraton of calcium through the skin and successive applications increase the calcium level inside the fruit, resulting in higher levels of protection (Nigro et al., 2006). Although the calcium’s protective mechanisms are not fully understood, most of it is accumulated in the middle lamella and the formation of calcium cross-linkages between and within pectin polymers may make the cell wall more resistant to hydrolytic enzymes produced by microorganisms (Tobias et al., 1993). Higher concentrations of cytosolic calcium have also been shown to induce endogenous resistance mechanisms through the synthesis of phytoalexins and phenolic compounds that decrease the activity of pathogen pectolytic enzymes (Miceli et al., 1999). The use of a salt application may be easy and cost effective compared to fungicides. However, it should be remembered that if the application of salt is to be made to the soil, the concentration should not exceed a certain level. Although it may be thought that the lower sporulation rate resulting from higher NaCl concentrations may affect the degree of virulence and pathogenicity and the distribution of the fungus, the adaptation of fungi to saline conditions, or sporulation of fungi in saline conditions might be just enough to infect crop plants under saline conditions, which seems to be the biggest potential danger for plant protection.


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It should also be kept in mind that the gradual accumulation of salt in soil may have the potential to create salt-tolerant fungi. This is because such a result was noted from studies of fungicide and pathogen interactions in which the fungicide-tolerant fungi have now become the biggest deterent to plant protection (Chaparro et al., 2011; Yang et al., 2013). For example, the growth and sporulation of Verticillium albo-atrum isolates decreased above 150 mM NaCl; however, the production of conidia above 150 mM NaCl was still sufficient to infect the roots of lucerne. Even if salt is applied to postharvest crops, one should remember that the application needs to be made more than once. Although efficacy is improved with biocontrol agents or various inorganic formulations, saltresistant fungi may still appear as in the case of fungicide-resistant microorganisms. Apart from these negative issues, development of symbiotic bacteria and mycorrhiza may also be negatively affected in terms of colonization capacity and efficiency (Asghari et al., 2008). However, for effective and environmentally friendly application of salts, there is a need to understand the basis and interactions of the chemical and biochemical mechanisms occurring among pathogen, plant, and salt. Nigro et al. (2006) suggested that applying salt has many adavantages (e.g., low cost and lack of legislative restrictions) to their utilization and proposed more salt applications to prevent disease development and increase crop resistance. However, regulatory innovation should be encouraged globally in order to use and register these substances as fungicidal products.

8.3.2 Positive effects of salinity on fungal growth Although the negative effect of salinity on plant growth is unquestionable, on the other hand, it may have a positive effect on fungal growth, including increasing the pathogenic activity through increased enzymatic and other cellular metabolic activities. There are quite a few reports about the positive effects of salinity on fungal growth. For example, Cercospora leaf spot of peanut was favored by soil salinity (Porter and Adamson, 1993). A significant increase in mycelium growth of Fusarium solani by sea salt and NaCl was also observed by Firdous and Shahzad (2001). They also reported that the levels of salt concentration encouraging the growth of F. solani were much higher than those tolerated by most crop plants. Salinity not only favors the conidial development of fungi but also increases conidial movement. For example, Ahn and Kim (2001) stated that the development of motile zoosporangia of Perkinsus sp. increased with a rise in salinity. A similar case was found with chlamydospores of F. oxysporum f.sp. vasinfectum, which were found to grow better in a saline medium; this also correlates with the increase of virulence (Ragazzi et al., 1994). Other kinds of salts (e.g., KCl) also encouraged the growth of mycelium. For example, Palmero et al. (2010) reported an increase of mycelium growth of Fusarium oxysporum strains by KCl as well as NaCl. The increase in virulence was attributed to enhanced activity of pectolytic enzymes produced by the fungus. Turco et al. (1999) reported that F. oxysporum f.sp. vasinfectum had higher enzymatic activities in saline environments with regard to pectate lyase (PL) and polygalacturonase (PG). An increase in PL activity was also reported in the Erwinia carotovora subsp. carotovora bacteria (El-Hendawy and Osman, 2005). The growth of the bacteria was stimulated, reduced, and totally inhibited in the presence of 1, 5, 3, and 6% NaCl, respectively. In addition, Regragui et al. (2003) showed an increase in the virulence of Verticillium albo-atrum through increased carboxymethylcellulase activity when cultured on an NaCl-enriched (80 mM) carboxymethylcellulose (CMC) medium. Other cell wall enzymes, such as xylanase and galactanase, produced by Sclerotium rolfsii were

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greater with increased salt concentrations (El-Abyad et al., 1992). Even a low concentration of NaCl may have the potential to activate and increase the level of enzymes and the conidial formation of fungi. For example, Dikilitas (2003) suggested that 50 mM NaCl had a positive effect on fungal growth and conidial germination. Similarly, Turco et al. (2002) reported that the NaCl concentration under 50 mM increased the production of cell wall enzymes and conidial formation leading to increased virulence of fungal pathogens. However, high concentrations of NaCl (0.51.5%) inhibited the enzymatic activity in most of the fungi (Omar and Abd-Alla, 2000). Development and growth of fungi under NaCl conditions not only encourage and lead to increases of the virulence of the pathogenic fungi but also may result in adaptation to salinity. Even if they are prone to lose their conidial germination and development rate at salinity conditions, they still have the potential to adapt to salinity after a period of time. The halophytic races of fungi, in that case, may appear and will be a threat to crop production in nonsaline soils (Dikilitas and Karakas, 2010; Dikilitas et al., 2011a).

8.3.3 Negative effects on plant growth of salinity in combination with fungi If the salinity level is within the tolerance limit of the crop plants, then the stress exerted by salt on the host may be increased by the adverse effect of a pathogen that is slightly affected by salt (Hassan and Shahzad, 2004; Goudarzi and Pakniyat, 2008; Saadatmand et al., 2008) (Figure 8.1). Even if the pathogen is negatively affected by salt, it is clear that the salt tolerance of many crop plants is much lower than those of the fungi living in salt (Attaby, 2001; Nayak et al., 2012). Therefore, the combined effect of both salt (even low concentrations) and the pathogen may cause

SALINITY

Antioxidant enzymes, osmolytes, proteins, hormones

Plant response to salinity stress

P L A N T

Reduced plant growth and development Osmotic stress Ionic imbalance Nutrient imbalance Na+ and Cl– toxicity Hormone production ROS production Plasmolysis Phenol and lignin susbtances Protein and lipid degradation

Reduced sporulation and mycelial growth Osmotic stress Ion toxicity Hormone production Amino acid synthesis Lysis Protein carbonylation ROS production or Increased sporulation Increased cell wall Enzymes

F U N G I

Antioxidant enzymes, osmolytes, proteins, hormones

Fungi response to salinity stress

Severe reduction in plant growth Further increase in ROS production Premature ageing

FIGURE 8.1 A conceptual diagram of plant and fungi responses and their interactions under salinity conditions.


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a more serious problem than that of the salt or the pathogen alone. In such conditions, additional energy may be required to cope with the disease, with an additional stress effect created by the salt (Dikilitas et al., 2009; DiLeo et al., 2010). An additional effect of salt stress on crop plants results in more symptoms resembling the severe cases of a particular pathogen involved in the host. Under these conditions, plants have to produce more metabolites to combat the negative effects of pathogens and salinity (see Figure 8.1). Similar negative effects were observed between the crop plants and other biotic stress agents. For example, a relationship between nematodes and vascular wilt diseases occurred in a wide range of crop plants. The combined effect of Pratylenchus minyus and Verticillium dahliae increased the wilt incidence of peppermint (Faulkner and Skotland, 1965). The authors suggested that the nematodes created many entry points for the fungus and liberated plant materials that favor fungal germination. Similar cases were recorded in other hostparasite combinations (Hajihassani et al., 2013). For example, Syvertsen and Levy (2005) suggested that the nematode infestation in the roots of citrus plants reduced salt tolerance while increasing Cl2 uptake. Other interactions occurred between insects and salinity by creating plants more susceptible to insect attack (Grattan and Grieve, 1999; Polack et al., 2011; Aluvilu et al., 2012). One of the earliest reports between pathogen and salt interactions was made by Holmes (1976) with regard to maple trees. He noted that the combined effects of NaCl and Verticillium albo-atrum caused more symptoms on the leaves of maple trees than each stress factor alone. Similar findings were found by Nachmias et al. (1993, 1994) who reported that the interaction of V. dahliae or Alternaria solani with salinity showed that the symptom expression of these diseases in the presence of salt remarkably increased when compared to symptoms caused by each stress factor alone. Increased salinity stress on tomato plants was also observed before or after inoculation with Phytophthora parasitica in which root and crown rot severity significantly increased compared to nonstressed controls (Swiecki and MacDonald 1991). Although salinity slightly reduced zoospore release and motility of P. parasitica, a low inoculum level resulted in young plants’ severe root rot. Salinity, on the other hand, may put the resistant cultivars in danger by breaking down their resistance. Besri (1990) reported that high salt levels in irrigation water led to a 100% breakdown of resistance in tomato cultivars resistant to V. dahliae. In saline conditions, virulent isolates of the fungus may gain more virulence and avirulent or slightly virulent isolates may also gain a degree of virulence depending on the resistance of the host. Regragui et al. (2003) reported that tomato plants var. Marmande showed susceptibility to the virulent isolate of V. albo-atrum (P80) and resistance to the avirulent isolate P(3)A of the same fungus. The cultivar became highly susceptible to P80 while becoming moderately susceptible to P(3)A isolate under saline irrigation (NaCl, 80 mM). Similarly, the defense barrier of resistant lucerne cv. NK-89786 was broken by the combined effect of both salt and V. albo-atrum. The increase in concentration of NaCl resulted in further loss of crop production (Howell et al., 1994). Another case involved a resistant tomato cultivar inoculated with Fusarium oxysporum f.sp. radicis-lycopersici under high salt stress (Triky-Dotan et al., 2005). The effect of salinity and pathogen interactions were observed in the seedling stages as well. Increasing saline irrigation from 0.01 to 5.0 dS m21 significantly increased mortality in cucmber seedlings infected with Pythium aphanidermatum (Al-Sadia et al., 2010). Salinity and pathogen interactions also were reported in horticultural trees. Levin et al. (2003) and Mohammadi et al. (2007) reported that V. dahliae in combination with salt resulted in a reduction in olive and pistachio production, respectively.

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Under saline conditions, not only pathogens become more virulent and slightly virulent pathogens become moderately virulent but also nonpathogens gain virulence, as reflected by the disease expression of the host. For example, nonpathogenic isolates (VL, VS, and VF) of V. albo-atrum caused significant reductions in growth parameters of lucerne plants under 50 mM NaCl (Dikilitas, 2003). Although this is assumed by the increase of virulence under saline conditions, the deterioration in plant defense systems also contributes to the result.

8.4 Behavior of saline-adapted fungi There are various reports of fungi surviving in saline conditions even if they are not aided by salt. For example, Sclerotinia sclerotiorum produced a great number of sclerotia in a high salt concentration. Increased sclerotial weight correlated with the survival of the pathogen in saline conditions (Hassan and Shahzad, 2004). A study with the salt-adapted strains (V2-150, adapted to 150 mM NaCl; V2-200, adapted to 200 mM NaCl) of V. albo-atrum (isolate V2) revealed that the mycelial growth in their respective NaCl conditions for at least eight months showed similar growth patterns with their nonsalt-adapted isolate V2 (grown in nonsalt conditions) (Dikilitas, 2003). Similar results were obtained with a more virulent isolate of V. albo-atrum (V1), although mycelial growth showed little decline. However, sporulation and conidial formation of both saltadapted strains declined in the long term under salt stress when compared to their nonsalt-adapted lines. When nonsalt-adapted lines (V1 or V2) were subcultured on the growth medium containing 150 and 200 mM NaCl long term, their growth rates declined drastically when compared to those of corresponding salt-adapted strains. Salt-adapted strains maintained their growth by reducing their sporulation and increasing the formation of aerial hyphae without touching the substrate to reduce the negative effects of salt. When nonsalt-adapted isolates were cultured under NaCl (150 and 200 mM NaCl), their mycelial growth and sporulation was reduced significantly. This showed that fungi under long-term salt stress may adapt to it, although higher concentrations required more time for adaptation (Ota and Morishita, 1993). For example, an isolate from saline soil, Phytophthora parasitica, proved to be more tolerant to salinity than the isolate recovered from nonsaline soils (Bouchibi et al., 1990). Llamas et al. (2008) also reported that the marine strains of Fusarium solani developed a physiological mechanism to survive in low water potential. Fungi, like plants, develop a kind of mechanism to survive in harsh conditions by accumulating proline, alanine, histidine, and other amino acids to compansate for the negative effects of water and salinity stress. For example, El-Abyad et al. (1992) reported that the higher accumulation of proline and alanine in Fusarium solani and Sclerotium rolfsii fungi under salinity conditions evidently compensates for the negative effects of salt. It is clear that salt-adapted or nonsalt-adapted fungi species result in stress in crop plants. Saltadapted fungi species develop a kind of mechanism to survive and sporulate under such conditions and have the potential to infect the host. However, the more important issue is that the salt-adapted fungal pathogens may still be pathogens when they live in nonsaline conditions. Some salt-tolerant isolates of V. albo-atrum, for example, were still highly pathogenic to tomato under nonsaline conditions, suggesting that the isolates did not lose their sporulation and infectious capacity (Dikilitas, 2003). However, loss of pathogenicity was reported in various fungi after storage in cold conditions

8.5 Pathological defense mechanisms under salt stress

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(Simpfendorfer et al., 1996). In addition, in cases of salt-adapted and nonsalt-adapted fungi under salt stress, the lower rate of sporulation was found to be efficient enough to cause pathogenicity (Dikilitas, 2003).

8.5 Pathological defense mechanisms under salt stress Salinity symptoms and defense mechanisms of crop plants were mentioned briefly at the beginning of this chapter (Section 8.2). Now, the defense mechanisms of plants after pathogen attack in the presence of salt are evaluated. For example, a nematode attack in citrus plants resulted in an increase in proline content and phenylalanine ammonia lyase (PAL) activity (Dunn et al., 1998; Lopez-Martinez et al., 2011; Banuelos et al., 2012). The combination of both stress factors resulted in a further increase in those metabolic activities. However, further incubation of the citrus plants with both stress factors resulted in a rapid decline in those parameters, suggesting that the combination of stress created sussceptibility in the defending organisms (Aluvilu et al., 2012; Safdar et al., 2013). This may be due to the attacking organism, Tylenchulus semipenetrans, gaining more entry points (Dunn et al., 1998). Similar results were obtained with the combined effect of V. albo-atrum and salinity on lucerne plants (Dikilitas, 2003). Low-level salinity (50 mM NaCl) on lucerne cells led to increased PAL activity, while a combination of salinity and an isolated carbohydrate from V. albo-atrum (0.05 mg ml21) resulted in a further increase in PAL activity. However, an increase in carbohydrate (0.1 mg ml21) content with the low level of NaCl (50 mM) resulted in a rapid decline in PAL activity, suggesting that the increase in concentration of the stress agent caused a reduction in PAL activity indicating that defense of the organism was impaired. It is clear that the combined effects of stress-containing abiotic and biotic factors result in increased stress. When the impact of either stress factor increases, the expression of symptoms increases physiologically and biochemically (Rai et al., 2011; Iglesias-Garcia et al., 2013). However, the further increases or a further incubation period under these conditions leads to a rapid decline in growth parameters as well as increased symptoms. In such cases, symptom expressions or biochemical results may be mixed with the severe cases of either stress agents. Therefore, the prolonged effect of salt as well as its high concentrations have the potential to reduce the defense barriers and facilitate pathogenic attack even if the crop plants become highly resistant (Alvarez and Sanchez-Blanco, 2013; Campanelli et al., 2013; Dehghan et al., 2013; Fu et al., 2013). Plants, in general, have various mechanisms to slow down or prevent the pathogen’s entry from its successful establishment or its spread into other tissues; however, under the combined stress of salt and pathogen, plants are not able to accumulate enough suberin, tyloses, lignin, phenol, and phytoalexins. Therefore, disease progress becomes fast and results in expression of severe symptoms (Jbir et al., 2001; Sanogo, 2004; Dikilitas et al., 2011b,c). Sulistyowati and Keane (1992) also noted that high salinity increased the severity of stem rot caused by Phytophthora citrophthora in citrus Troyer citrange, sour orange, and rough lemon rootstocks. They reported that high salinity resulted in reduced accumulation of phytoalexin 6,7-dimethoxycoumarin and, therefore, increased the susceptibility of plant tissues to invasion by fungus. Although the pathological defense mechanisms under salt stress need to be cleared and evaluated from every aspect, one of the possible mechanisms involves the toxicity of Na1 and Cl2 ions

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taken up at high rates. This may lead to excessive accumulation in tissues and reduction of the antioxidant capacity of plants. Osmotic stress created by the high salt concentration also decreases water uptake and increases the wilt symptoms of crop plants inoculated with wilt fungi. The recovery of crop plants from the effects of fungi under saline conditions also may be difficult (You et al., 2011). In severe cases, the recovery period may be longer or may not take place at all (Daleo et al., 2013). For example, the recovery of lucerne plants inoculated with 50 mM NaCl V. albo-atrum was delayed significantly. The combined stress effect was more pronounced on leaves of lucerne than with either stress factor alone (Dikilitas, 2003). It is certain that the plants exposed to salinity show marginal Ca21 deficiency (El-Iklil et al., 2002), and this results in a fragility in the membrane that permits a continuous outflow of assimilates (i.e., sugars and amino acids) (Fozouni et al., 2012; Li et al., 2013). Under these conditions, the synthesis and speed of many defense enzymes, such as peroxidase (POD), superoxide dismutase (SOD), catalase (CAT), polyphenol oxidase (PPO), and PAL, are slowed down or not produced to compensate for the negative effects of the combined stress. This is because the basic molecules, such as phenolic compounds and phytoalexins, are important defense elements (Neves et al., 2010).

8.6 Pathological responses of salt-tolerant plants To cope with the stress of salt or diseases, it is important to generate tolerant or resistant plants against abiotic or biotic stress factors. Using biochemical, physiological, or molecular pathways, it is possible to regenerate more resistant plants than before (Jain, 2013). However, when salt-tolerant or disease-resistant plants are regenerated, it is important to remember other stress issues or their combined effects on crop plants (Atkinson and Urwin, 2012; Atkinson et al., 2013). If the combined stress involves one biotic and one abiotic, then one should keep in mind that the biotic stress factor may have the potential to develop itself under the abiotic stress condition or to adapt to the abiotic stress factor. For example, regenerated salt-tolerant lucerne M. media cv. Rambler strains, R-200-N and R-350-N, showed the highest degree of salt tolerance at 200 and 350 mM NaCl, respectively; however, they showed the highest susceptibility to Verticillium albo-atrum (Dikilitas, 2003). When the salt-tolerance ability of those strains was diminished, differences in their responses to V. albo-atrum also were leveled, indicating that the physiologically induced salt tolerance was inversely correlated with resistance to wilt disease. It is important to note that the naturally disease-resistant cultivars may also lose their resistance against pathogens under saline or normal conditions (Mou, 2011). Therefore, new strategies and methods should be developed to increase the resistance of plants, as well as aim to reduce the impacts of at least one of the stress factors.

8.7 Conclusion and future prospects In many countries, various organizations and research institutes have put forth their visions, such as “Vision-2020” or “Agriculture 2020,” for the development of agriculture. They have set major goals in biology and plant sciences by evaluating how plants may survive and to help with

References

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numerous problems such as increased food demand, climate change, drought, and biotic stress issues (Dikilitas and Karakas, 2011d). However, abiotic and biotic stress factors may interact with each other and may be either in favor of microorganisms or against them. Even if they do not interact, their additive effects may create serious host plant disorders. If microorganisms exhibit higher tolerance to the adverse effects of salt than those of their hosts, then additional stress to host plants is inevitable. Therefore, either host plants need to develop resistance to both stress factors or one of the impacts of them should be minimized in order to combat the other stress factor. Advances in biotechnology and gene transfer enable plant breeders to develop more resistant plants with new traits from unrelated organisms (e.g., fungi, viruses, bacteria, or halophytic plants) living in adverse conditions (Abumhadi and Atanassov, 2010). Transfer of genetic materials from these organisms with classic breeding programs is impossible; therefore, tolerance mechanisms of salinity-adapted pathogens should be evaluated so that they can be better understood for crop plants. To reduce the impact of salt in soils, mycorrhiza, plant growth-promoting rhizobacteria (PGPR), and other beneficial organisms as well as salt-absorbing plants (halophytes) should be employed. Because bacteria or halophytes that are able to produce IAA under saline conditions may supply additional phytohormones to the plant, this may help stimulate root growth and hinder the growthinhibiting effect of salt stress (Egamberdieva and Kucharova, 2009). Further, plant stress can be reduced by ACC deaminase-producing bacteria, which can lower the level of the plant stress hormone ethylene (Belimov et al., 2009). The successful PGPRs should be screened for various plant pathogens and for their hosts in saline soils. Biocontrol mechanisms have been used for a long time to reduce disease severity, so the possible opportunities should be evaluated for diseased plants in saline soils. For example, the growth parameters of chickpea plants at 2% NaCl salinity increased in the presence of Aspergillus sp. and Penicillium sp. (Urja and Meenu, 2010). Salt-tolerant nonpathogenic fungi, such as Trichoderma harzianum, was successfully used in saline areas to prevent the wilt disease in tomato caused by Fusarium oxysporum (Mohamed and Haggag, 2006).

Acknowledgment I dedicate this chapter in memory of my deceased father Dede Dikilitas.

References Abdelhamid, M.T., Rady, M.M., Osman, A.S., Abdalla, M.A., 2013. Exogenous application of proline alleviates salt-induced oxidative stress in Phaseolus vulgaris L. plants. J. Hort. Sci. Technol. 88 (4), 439446. Abd-El-Kareem, F., 2007. Potassium or sodium bicarbonate in combination with Nerol for controlling early blight disease of potato plants under laboratory, greenhouse and field conditions. Egypt J. Phytopathol. 35 (1), 7386. Abumhadi, N.M., Atanassov, A.I., 2010. Future challenges of plant biotechnology and genomics. Roman Biotechnol. Lett. 15 (2), 127142. Aghaleh, M., Niknam, V., Ebrahimzadeh, H., Razavi, K., 2009. Salt-stress effects on growth, pigments, proteins and lipid peroxidation in Salicornia persica and S. europaea. Biol. Plant 53 (2), 243248.

186


Ahn, K.J., Kim, K.H., 2001. Effect of temperature and salinity on in vitro zoosporulation of Perkinsus sp. in Manila clams Ruditapes philippinarum. Dis. Aquat. Organ. 48 (1), 4346. Al-Rawahy, S.H., 2000. Study of the adaptive mechanisms evolved through selecting NaCl tolerant cells and plants of alfalfa (M. media cv. Rambler). Ph.D. Thesis. University of Wales, Swansea. Al-Sadia, A.M., Al-Masoudia, R.S., Al-Habsib, N., Al-Saida, F.A., Al-Rawahy, S.A., Ahmed, M., et al., 2010. Effect of salinity on Pythium damping-off of cucumber and on the tolerance of Pythium aphanidermatum. Plant Pathol. 59, 112120. Aluvilu, A., Mashela, P., Pofu, K., 2012. Interactive effects of Meloidogyne incognita, salinity and seasonal length on productivity and growth of pepper in Limpopo Province, South Africa. Int. J. Agric. Biol. 14 (4), 569574. Alvarez, S., Sanchez-Blanco, M.J., 2013. Long-term effect of salinity on plant quality, water relations, photosynthetic parameters and ion distribution in Callistemon citrinus. Plant Biol., Available from: http://dx.doi. org/10.1111/plb.12106. Amir, H., Mair, A., Riba, A., 1996. Role de la microflore dans la resistance a la Fusariose vascularie induite par la salinite dans un sol de palmeraie. Soil Biol. Biochem. 28 (1), 113122. Araya, F., Abarca, O., Zuniga, G.E., Corcuera, L.J., 1991. Effects of NaCl on glycine-betaine and on aphids in cereal seedlings. Phytochem. 30, 17931795. Arfan, M., 2009. Exogenous application of salicylic acid through rooting medium modulates ion accumulation and antioxidant activity in spring wheat under salt stress. Int. J. Agric. Biol. 11, 437442. Asghari, H.R., Amerian, M.R., Gorbani, H., 2008. Soil salinity affects arbuscular mycorrhizal colonization of halophytes. Pak. J. Biol. Sci. 11, 19091915. Atkinson, N.J., Urwin, P.E., 2012. The interaction of plant biotic and abiotic stresses: from genes to the field. J. Exp. Bot. 63 (10), 35233543. Atkinson, N.J., Lilley, C.J., Urwin, P.E., 2013. Identification of genes involved in the response of Arabidopsis to simultaneous botic and abiotic stresses. Plant Physiol. 162 (4), 20282041. Attaby, H.S.H., 2001. Influence of salinity stress on the growth, biochemical changes and response to gamma irradiation to Penicillium chrysogenum. Pak. J. Biol. Sci. 4 (6), 703706. Banuelos, J., Trejo, D., Alarcon, A., Lara, L., Moreira, C., Cruz, S., 2012. The reduction in proline buildup in mycorrhizal plants affected by nematodes. J. Soil Sci. Plant Nutr. 12 (2), 263270. Belimov, A.A., Dodd, I.C., Hontzeas, N., Theobald, J., Safronova, V.I., Davies, W.J., 2009. Rhizosphere bacteria containing 1-aminocyclopropane-1-carboxylate deaminase increase yield of plants grown in drying soil via both local and systemic hormone signalling. New Phytol. 181, 435447. Ben Ahmed, C., Magdich, S., Ben Rouina, B., Sensoy, S., Boukhris, M., Ben Abdullah, F., 2011. Exogenous proline effects on water relations and ion contents in leaves and roots of young olive. Amino Acids 40, 565573. Besri, M., 1990. Effect of salinity on the development of tomato Verticillium wilt in Morocco. Proceedings of the Fifth International Verticillium Symposium, Leningrad, pp. 61. Bhai, R.S., Anandaraj, M., Srinivasan, V., 2009. Validation of farmer’s practice of using sodium chloride for controlling foot rot disease of black pepper (Piper nigrum). Indian J. Agric. Sci. 79 (9), 722726. Bouchibi, N., van Bruggen, A.H.C., MacDonald, J.D., 1990. Effect of ion concentration and sodium: calcium ratio of a nutrient solution on Phytophthora root rot of tomato and zoospore motility and viability of Phytophthora parasitica. Phytopathol. 80, 13231329. Bridges, E.M., 1997. World Soils. third ed. Cambridge University Press, Cambridge. Campanelli, A., Ruta, C., Morone-Fortunato, I., De Mastro, G., 2013. Alfalfa (Medicago sativa L.) clones tolerant to salt stress: in vitro selection. Cent. Eur. J. Biol. 8 (8), 765776. Chandler, D., Heale, J.B., Gillespie, A.T., 1994. Effect of osmotic potential on the germination of conidia and colony growth of Verticillium lecanii. Mycol. Res. 98 (4), 384388.

References

187

Chaparro, A.P., Carvajal, L.H., Orduz, S., 2011. Fungicide tolerance of Trichoderma asperelloides and T. harzianum strains. Agric. Sci. 2 (3), 301307. Chaudhary, M.T., 1996. Salt tolerance and toxicity in NaCl-selected and non-selected cells and regenerated plants of Medicago media. Ph.D. Thesis. University of Wales, Swansea. Dajic, D., 2006. Salt stress. In: Madhava Rao, K.V., Raghavendra, A.S., Reddy, K.J. (Eds.), Physiology and Molecular Biology of Stress Tolerance in Plants. Springer, Dordrecht, Netherlands, pp. 4199. Daleo, P., Alberti, J., Pascual, J., Iribarne, O., 2013. Nutrients and abiotic stress interact to control ergot plant disease in a SW Atlantic Salt Marsh. Est. Coast 36 (5), 10931097. Danti, S., Broggio, M., 1997. Impact of salinity stress on the biometric responses of an isolate of Verticillium dahliae Kleb. from potato. Proceedings of the Seventh International Verticillium Symposium. Athens, Greece, p. 53. Dehghan, G., Amjad, L., Nosrati, H., 2013. Enzymatic and non-enzymatic antioxidant reponses of alfalfa leaves and roots under different salinity levels. Acta Biol. Hung. 64 (2), 207217. Dikilitas, M., 2003. Effect of salinity and its interactions with Verticillium albo-atrum on the disease development in tomato (Lycopersicon esculentum Mill.) and lucerne (Medicago sativa & M. media) plants. Ph.D. Thesis, University of Wales, Swansea. Dikilitas, M., Karakas, S., 2010. Salts as potential environmental pollutants, their types, effects on plants and approaches for their phytoremediation. In: Ashraf, M., Ozturk, M., Ahmad, M.S.A. (Eds.), Plant Adaptation and Phytoremediation. Springer, London, pp. 357381. Dikilitas, M., Kocyigit, A., Yigit, F., 2009. A molecular-based fast method to determine the extent of DNA damages in higher plants and fungi. Afr. J. Biotechnol. 8, 31183127. Dikilitas, M., Katırcıo˘glu, Y.Z., Altınok, H., 2011a. Fungus ve fungal materyallerin uzun do¨nem saklanması, korunması ve geri kazanımı u¨zerine varılan son geli¸sme ve yo¨ntemler. J. Agric. Fac. Harran Univ. 15 (2), 5569. Dikilitas, M., Guldur, M.E., Deryaoglu, A., Erel, O., 2011b. A novel method of measuring oxidative stress of pepper (Capsicum annuum var. Charlee) infected with tobacco mosaic virus. J. Appl. Biosci. 37, 24252433. Dikilitas, M., Guldur, M.E., Deryaoglu, A., Erel, O., 2011c. Antioxidant and oxidant levels of pepper (Capsicum annuum cv. “Charlee”) infected with pepper mild mottle virus. Not. Bot. Horti. Agrobo. 39 (2), 5863. Dikilitas, M., Karakas, S., 2011d. Agriculture in 2020: What is the target? J. Agric. Fac. Harran Univ. 14 (3), 12. DiLeo, M.V., Pye, M.F., Roubtsova, T.V., Duniway, J.M., MacDonald, J.D., Rizzo, D.M., et al., 2010. Abscisic acid in salt stress predisposition to Phytophthora root and crown rot in tomato and chrysanthemum. Phytopathol. 100, 871879. Droby, S., Wisniewski, M., El Ghaouth, A., Wilson, C., 2003. Influence of food additives on the control of postharvest rots of apple and peach and efficacy of the yeast-based biocontrol product Aspire. Postharvest. Biol. Technol. 27, 127135. Dunn, D.C., Duncan, L.W., Romeo, J.T., 1998. Changes in arginine, PAL activity, and nematode behaviour in salinity-stressed citrus. Phytochem. 49 (2), 413417. Egamberdieva, D., 2012. Pseudomonas chlororaphis: a salt-tolerant bacterial inoculant for plant growth stimulation under saline soil conditions. Acta Physiol. Plant 34, 751756. Egamberdieva, D., Kucharova, Z., 2009. Selection for root colonizing bacteria stimulating wheat growth in saline soils. Biol. Fertil. Soils 45, 563571. El-Abyad, M.S., Abu-Taleb, A.M., Khalil, M.S., 1992. Impact of salinity stress on soil-borne fungi of sugar beet. Plant Soil 143, 7583.

188


El-Hendawy, H.H., Osman, M.E., 2005. Effect of sodium chloride and glycine betaine on growth and pectate lyase production by Erwinia carotovora subsp. carotovora. Pak. J. Biol. Sci. 8 (2), 330334. El-Iklil, Y., Karrou, M., Mrabet, R., Benichou, M., 2002. Salt stress effect on metabolic concentrations of Lycopersicum esculentum and Lycopersicum cheesmanii. Can. J. Plant Sci. 82 (1), 177183. El-Mougy, N.S., Abdel-Kader, M.M., 2009. Salts application for suppressing potato early blight disease. J. Plant Prot. Res. 49 (4), 353361. Elmer, W.H., 1992. Suppression of Fusarium crown and root rot of asparagus with sodium chloride. Phytopathol. 82, 97104. Engel, R.E., Grey, W.E., 1991. Chloride fertilizer effects on winter wheat inoculated with Fusarium culmorum. Agron. J. 83 (1), 204208. Faulkner, L.R., Skotland, C.B., 1965. Interaction of Verticillium dahliae and Pratylenchus minyus in Verticillium wilt of peppermint. Phytopathol. 55, 583586. Firdous, H., Shahzad, S., 2001. Effect of some salts on in vitro growth of Fusarium solani. Pak. J. Bot. 33 (2), 117124. Flowers, T.J., 2004. Improving crop salt tolerance. J. Exp. Bot. 55, 307319. Fozouni, M., Abbaspour, N., Baneh, H.D., 2012. Leaf water potential, photosynthetic pigments and compatible solutes alterations in four grape cultivars under salinity. Vitis 51 (4), 147152. Fu, M.Y., Li, C., Ma, F.W., 2013. Physiological responses and tolerance to NaCl stress in different biotypes of Malus prunifolia. Euphytica 189 (1), 101109. Gao, S., Shain, L., 1995. Effects of osmotic potential on virulent and hypovirulent strains of the chestnut blight fungus. Can. J. Forest Res. 25 (6), 10241029. Gilbert, G.S., Mejia-Chang, M., Rojas, E., 2002. Fungal diversity and plant disease in mangrove forests: salt excretion as a possible defense mechanism. Oecologia 132, 278285. Goudarzi, A., Banihashemi, Z., Manouchehr, M., 2008. Effect of water potential on sclerotial germination and mycelial growth of Macrophomina phaseolina. Phytopathol. Mediterr. 47, 107114. Goudarzi, M., Pakniyat, H., 2008. Evaluation of wheat cultivars under salinity stress based on some agronomic and physiological traits. J. Agric. Soc. Sci. 4, 3538. Grattan, S.R., Grieve, C.M., 1999. Salinity-mineral nutrient relations in horticultural crops. Sci. Hort. 78, 127157. Hadson, A.D., Hitz, W.D., 1982. Metabolic responses of glycophytes to plant water deficit. Ann. Rev. Plant Physiol. 33, 163203. Hajihassani, A., Smiley, R.W., Afshar, F.J., 2013. Effects of co-inoculation with Pratylenchus thornei and Fusarium culmorum on growth and yield of winter wheat. Plant Dis. 97 (11), 14701477. Hare, P.D., Cress, W.A., 1997. Metabolic implication of stress-induced proline accumulation in plants. Plant Growth Regul. 21, 79102. Hasan, H.A.H., 2002. Gibberellin and auxin production by plant root-fungi and their biosynthesis under salinity-calcium interaction. Rostlinna Vyroba 48 (3), 101106. Hasan, M.F., Mahmud, T.M.M., Kadir, J., Ding, P., Zaidul, I.S.M., 2012. Severity of Colletotrichum gloeosporioides to sodium bicarbonate on the development of anthrachnose in papaya (Carica papaya L. cv. Frangi). Aust. J. Crop. Sci. 6 (1), 1722. Hassan, S.Y., Shahzad, S., 2004. Effect of sea salt on in vitro growth of Sclerotinia sclerotiorum. Pak. J. Bot. 36 (3), 677682. Holmes, E.W., 1976. Verticillium wilt of salt-injured sugar maple-preliminary study. Proc. Am. Phytopathol. Soc. 3, 305306. Howell, A.B., Erwin, D.C., 1995. Characterization and persistence of Verticillium albo-atrum isolated from alfalfa growing in high temperature regions of southern California. Plant Pathol. 44, 734748.

References

189

Howell, A.B., François, L., Erwin, D.C., 1994. Interactive effect of salinity and Verticillium albo-atrum on Verticillium wilt disease severity and yield of two alfalfa cultivars. Field Crop. Res. 37, 247251. Hua, B., Guo, W.Y., 2002. Effect of exogenous proline on SOD and POD activity of soyabean callus under salt stress. Acta Agric. Boreali-Sinica 17, 3740. Iglesias-Garcia, A.M., Villarroel-Zeballos, M.I., Feng, C.D., du Toit, L.J., Correll, J.C., 2013. Pathogenicity, virulence, and vegetative compatibility grouping of Verticillium isolates from spinach seed. Plant Dis. 97 (11), 14571469. Jain, M., 2013. Emerging role of metabolic pathways in abiotic stress tolerance. J. Plant Biochem. Physiol. 1, 108. Jbir, N., Chaibi, W., Ammar, S., Jemmali, A., Ayadi, A., 2001. Rooting growth and lignification of two wheat species differing in their sensitivity to NaCl in response to salt stress. Plant Biol. Path. 324, 863868. Johnson, H.E., 2000. The effect of salinity on tomato growth and fruit quality. PhD. Thesis. Institute of Biological Sciences, University of Wales, Aberystwyth. Jones, E.E., Stewart, A., Whipps, J.M., 2011. Water potential affects Coniothyrium minitans growth, germination and parasitism of Sclerotinia sclerotiorum sclerotia. Fungal Biol. 115, 871881. Kostandi, S.F., Soliman, M.F., 1998. The role calcium in mediating smut disease severity and salt tolerance in corn under chloride and sulphate salinity. J. Phytopathol. 146, 191195. Krokene, P., Solheim, H., 2001. Loss of pathogenicity in the blue-stain fungus Ceractocystis polonica. Plant Pathol. 50 (4), 497502. Levin, A.G., Lavee, S., Tsror (Lahkim), L., 2003. Epidemiology of Verticillium dahliae on olive (cv. Picual) and its effect on yield under saline conditions. Plant Pathol. 52, 212218. Li, X.L., Wang, C.R., Li, X.Y., Yao, Y.X., Hao, Y.J., 2013. Modifications of Kyoho grape berry quality under long-term NaCl treatment. Food Chem. 139 (14), 931937. Llamas, D.P., Gonzales, M.D., Gonzales, C.I., Lopez, G.R., Marquina, J.C., 2008. Effects of water potential on spore germination and viability of Fusarium species. J. Ind. Microbiol. Biotechnol. 35, 14111418. Lopez-Martinez, N., Colinas-Leon, M.T., Pena-Valdivia, C.B., Salinas-Moreno, Y., Fuentes-Montiel, P., Biesaga, M., et al., 2011. Alterations in peroxidase activity and phenylpropanoid metabolism induced by Nacobbus aberrans Thorne and Allen, 1944 in chilli (Capsicum annuum L.) CM334 resistant to Phytophthora capsici Leo. Plant Soil. 338 (12), 399409. Madani, B., Mohameda, M.T.M., Biggs, A.R., Kadir, J., Awang, Y., Tayebimeigooni, A., et al., 2014. Effect of pre-harvest calcium chloride applications on fruit calcium level and post-harvest anthracnose disease of papaya. Crop. Prot. 55, 5560. Mahmoud, Y.A.G., Mohamed, EHFA, Abd Elzaher, E.H.F., 2007. Response of the higher basidiomycetic Ganoderma resinaceum to sodium chloride stress. Mycobiol. 35 (3), 124128. McQuilken, M.P., Whipps, J.M., Cooke, R.C., 1992. Effects of osmotic and matric potential on growth and oospore germination of the biocontrol agent Phythium oligandrum. Mycol. Res. 96 (7), 588591. Mecteau, M.R., Arul, J., Russell, J.T., 2002. Effect of organic and inorganic salts on the growth and development of Fusarium sambucinum, a causal agent of potato dry rot. Mycol. Res. 106 (6), 688696. Mecteau, M.R., Arul, J., Tweddell, R.J., 2008. Effect of different salts on the development of Fusarium solani var. coeruleum, a causal agent of potato dry rot. Phytoprotection 89 (1), 16. Meszka, B., Bielenin, A., 2011. Activity of laminarin in control of strawberry diseases. Phytopathologia 62, 1523. Miceli, A., Ippolito, A., Linsalata, V., Nigro, F., 1999. Effect of pre-harvest calcium treatment on decay and biochemical changes in table grape during storage. Phytopathol. Mediterr. 38, 4753. Mohamed, H.A.L., Haggag, W.F., 2006. Biocontrol potential of salinity tolerant mutants of Trichoderma harzianum against Fusarium oxysporum. Braz. J. Microbiol. 37, 181191.

190


Mohammadi, A.H., Banihashemi, Z., Maftoun, M., 2007. Interaction between salinity stress and Verticillium Wilt disease in three pistachio rootstocks in a calcareous soil. J. Plant Nutr. 30, 241252. Monirifar, H., Barghi, M., 2009. Identification and selection for salt tolerance in alfalfa (Medicago sativa L.) ecotypes via physiological traits. Not. Sci. Biol. 1 (1), 6366. Mou, B., 2011. Improvement of horticultural crops for abiotic stress tolerance: An introduction. HortSci 46 (8), 10681069. Nachmias, A., Kaufman, Z., Livescu, L., Tsror, L., Meiri, A., Caligari, P.D.S., 1993. Effects of salinity and its interactions with disease incidence on potatoes grown in hot climates. Phytoparasitica 21 (3), 245255. Nachmias, A., Livescu, L., Tsror, L., Ben Hador, G., Orenstein, J., Sabbah, S., et al., 1994. Enhancement of Verticillium infection in potato under stress. Sixth International Verticillium Symposium, Dead Sea, Israel. Phytoparasitica 23: 51. Nadeem, S.M., Zahir, Z.A., Naveed, M., Ashraf, M., 2010. Microbial ACC-Deaminase: prospects and applications for inducing salt tolerance in plants. Crit. Rev. Plant Sci. 29, 360393. Namdjoyana, S., Kermanian, H., 2013. Exogenous nitric oxide (as sodium nitroprusside) ameliorates arsenicinduced oxidative stress in watercress (Nasturtium officinale R. Br.) plants. Sci. Hort. 161, 350356. Nayak, S.S., Gonsalves, V., Nazareth, S.W., 2012. Isolation and salt tolerance of halophilic fungi from mangroves and solar salterns in Goa-India. Indian J. Geo-Marine Sci. 41 (2), 164172. Neves, G.Y.S., Marchiosi, R., Ferrarese, M.L.L., Siqueira-Soares, R.C., Ferrarese-Filho, O., 2010. Root growth inhibition and lignification induced by salt stress in soybean. J. Agron. Crop. Sci. 196, 467473. Nigro, F., Schena, L., Ligorio, A., Pentimone, I., Ippolito, A., Salerno, M.G., 2006. Control of table grape storage rots by pre-harvest applications of salts. Postharvest. Biol. Technol. 42, 142149. Omar, S.A., Abd-Alla, M.H., 2000. Physiological aspects of fungi isolated from root nodules of faba bean (Vicia faba L.). Microbiol. Res. 154 (4), 339347. Ota, A., Morishita, H., 1993. Effect of NaCl on the growth and morphology of Saccharomycopsis fibuligera. Microbios 73 (295), 149155. Palmero, D., De Cara, M., Moreno, M.M., Iglesias, C., Tello, J.C., 2010. Stimulation of mycelial growth of pathogenic and seabed isolates of Fusarium oxysporum in presence of salts. Afr. J. Microbiol. Res. 4 (17), 18591861. Polack, L.A., Pereyra, P.C., Sarandon, S.J., 2011. Effects of plant stress and habitat manipulation on aphid control in greenhouse sweet peppers. J. Sustain Agric. 35 (7), 699725. Porter, D.M., Adamson, J.F., 1993. Effect of sodic water and irrigation on sodium levels and the development of early leaf spot in peanut. Plant Dis. 77, 480840. Qadir, M., Qureshi, R.H., Ahmad, N., 2002. Ameloriation of calcareous saline sodic soils through phytoremediation and chemical strategies. Soil Use Manage. 18, 381385. Qin, G., Zong, Y., Chen, Q., Hua, D., Tian, S., 2010. Inhibitory effect of boron against Botrytis cinerea on table grapes and its possible mechanisms of action. Int. J. Food Microbiol. 138, 145150. Ragazzi, A., Vechio, V., Dellavalle, I., Cucchi, A., Mancini, F., 1994. Variations in the pathogenicity of Fusarium oxysporum f.sp. vasinfectum in relation to the salinity of the nutrient medium. J. Plant Dis. Prot. 101 (3), 263266. Rai, G.K., Kumar, R., Singh, J., Rai, P.K., Rai, S.K., 2011. Peroxidase, polyphenol oxidase activity, protein profile and phenolic content in tomato cultivars tolerant and susceptible to Fusarium oxysporum f.sp. lycopersici. Pak. J. Bot. 43 (6), 29872990. Regragui, A., Rahouti, M., Et Lahlou, H., 2003. Effet Du Stress salin sur Verticillium albo-atrum: pathogénécité et production d’enzymes cellulolytiques in vitro. Cryptogamie Mycol. 24 (2), 167174. Reid, T.C., Hausbeck, M.K., Kizilkaya, K., 2001. Effects of sodium chloride on commercial asparagus and of alternative forms of chloride salt on Fusarium crown and root rot. Plant Dis. 85, 12711275.

References

191

Roos, J., Hopkins, R., Kvarnheden, A., Dixelius, C., 2011. The impact of global warming on plant diseases and insect vectors in Sweden. Eur. J. Plant Pathol. 129, 919. Rougon-Cardoso, A., Zipfel, C., 2010. A new approach to confer broad-spectrum disease resistance in plants. Inform. Syst. Biotechnol. News Rep. June, 58. Ruiz, K.B., Trainotti, L., Bonghi, C., Ziosi, V., Costa, G., Torrigiani, P., 2013. Early methyl jasmonate application to peach delays fruit/seed development by altering the expression of multiple hormone-related genes. Plant Growth Regul. 32, 852864. Saadatmand, A.R., Banihashemi, Z., Sepaskhah, A.R., Maftoun, M., 2008. Soil salinity and water stress and their effect on susceptibility to Verticillium wilt disease, ion composition and growth of pistachio. J. Phytopathol. 156, 287292. Safdar, A., Javed, N., Khan, S.A., Safdar, H., Ul Haq, I., Abbas, H., et al., 2013. Synergistic effect of a fungus, Fusarium semitectum, and a nematode, Tylenchulus semipenetrans, on citrus decline. Pak. J. Zoo. 45 (3), 643651. Sairam, R.K., Tyagi, A., 2004. Physiology and molecular biology of salinity stress tolerance in plants. Curr. Sci. 86, 407421. Sanogo, S., 2004. Response of chile pepper to Phytophthora capsici in relation to soil salinity. Plant Dis. 88, 205209. Shibli, R.A., Kushad, M., Yousef, G.G., Lila, M.A., 2007. Physiological and biochemical responses of tomato microshoots to induced salinity stress with associated ethylene accumulation. Plant Growth Regul. 51, 159169. Simpfendorfer, S., Harden, T.J., Murray, G.M., 1996. Viability and pathogenicity of Phytophthora clandestina after storage in water and liquid nitrogen. Australias. Plant Path. 25, 234239. Sorkheh, K., Shiran, B., Khodambashi, M., Rouhi, V., Mosavei, S., Sofo, A., 2012. Exogenous proline alleviates the effects of H2O2-induced oxidative stress in wild almond species (Prunus spp.). Russ. J. Plant Physl. 59 (6), 788798. Sosa, L., Llanes, A., Reinoso, H., Reginato, M., Luna, V., 2005. Osmotic and specific ion effects on the germination of Prosopis strombulifera. Ann. Bot. 96, 261267. Sugano, S., Sugimoto, T., Takatsuji, H., Jiang, C.J., 2013. Induction of resistance to Phytophthora sojae in soyabean (Glycine max) by salicylic acid and ethylene. Plant Pathol. 62 (5), 10481056. Sulistyowati, L., Keane, P.J., 1992. Effect of soil-salinity and water-content on stem rot caused by Phytophthora citrophthora and accumulation of phytoalexin in citrus rootstocks. Phytopathol. 82 (7), 771777. Swiecki, T.J., MacDonald, J.D., 1991. Soil salinity enhances Phytophthora root rot of tomato but hinders asexual reproduction by Phytophthora parasitica. J. Am. Soc. Hort. 116 (3), 471477. Syklowska-Baranek, K., Pietrosiuk, A., Naliwajski, M.R., Kawiak, A., Jeziorek, M., Wyderska, S., et al., 2012. Effect of L-phenylalanine on PAL activity and production of naphthoquinone pigments in suspension cultures of Arnebia euchroma (Royle) Johnst. In Vitro Cell. Dev. Biol.—Plant 48, 555564. Syvertsen, J., Levy, Y., 2005. Salinity interactions with other abiotic and biotic stresses in citrus. Horttechnol. 15 (1), 100103. Tester, N., Davenport, R., 2003. Na1 tolerance and Na1 transport in higher plants. Ann. Bot. 91, 125. Tobias, R.B., Conway, W.S., Sams, C.F., Gross, K.C., Whitaker, B.E., 1993. Cell wall composition of calcium-treated apples inoculated with Botrytis cinerea. Phytochemi. 32, 3539. Triky-Dotan, S., Yermiyahu, U., Katan, J., Gamliel, A., 2005. Development of crown and root rot disease of tomato under irrigation with saline water. Phytopathol. 95, 14381444. Turco, E., Broggio, M., Ragazzi, A., 1999. Enzymes produced by Fusarium oxysporum f.sp. vasinfectum compared on a saline and a non-saline substrate. J. Plant Dis. Prot. 106, 333341.

192


Turco, E., Naldini, D., Ragazzi, A., 2002. Disease incidence and vessel anatomy in cotton plants infected with Fusarium oxysporum f.sp. vasinfectum under salinity stress. J. Plant Dis. Prot. 109 (1), 1524. Urja, P., Meenu, S., 2010. Role of single fungal isolates and consortia as plant growth promoters under saline conditions. Res. J. Biotechnol. 5 (3), 59. Wenneker, M., Kanne, J., 2010. Use of potassium bicarbonate (Armicarb) on the control of powdery mildew (Sphaerotheca mors-uvae) of gooseberry (Ribes uva-crispa). Commun. Agric. Appl. Biol. Sci. 75 (4), 563568. Wisniewski, M., Droby, S., Chalutz, E., Eilam, Y., 1995. Effects of Ca21 and Mg21 on Botrytis cinerea and Penicillium expansum in vitro and on the biocontrol activity of Candida oleophila. Plant Pathol. 44, 10161024. Yang, L., Gao, F., Shang, L., Zhan, J., McDonald, B.A., 2013. Association between virulence and triazole tolerance in the phytopathogenic fungus Mycosphaerella graminicola. PLoS One 8 (3), e59568. You, M.P., Colmer, T.D., Barbetti, M.J., 2011. Salinity drives host reaction in Phaseolus vulgaris (common bean) to Macrophomina phaseolina. Funct. Plant Biol. 38 (12), 984992.

CHAPTER

Preventing Potential Diseases of Crop Plants Under the Impact of a Changing Environment

9

Memoona Ilyas, Khola Rafique, Sania Ahmed, Sobia Zulfiqar, Fakiha Afzal, Maria Khalid, Alvina Gul Kazi and Abdul Mujeeb-Kazi

9.1 Introduction Climatic change is one of the most challenging situations for scientists today. It poses threats to food security, natural ecosystems, as well as the economic stability of the world (Reynolds and Ortiz, 2010). It has been stated that changes in climate are directly proportional to crops and their interaction with microbial pests; that is, any change in climate affects them directly (Bent, 2003). Crops are one of the major sources of the food that everyone consumes and are subjected to various biotic and abiotic stresses, which affect their growth and development. Weather extremes, diseases, and pests negatively affect crops. It has been estimated that 36.5% of the world’s total crops are affected by insects and weeds every year (Agrios, 2005), and pests are one of the most notorious factors contributing to decreases in yield (Gregory et al., 2009). Plant disease can be defined as the condition when a plant is not able to carry out vital functions properly by losing form and integrity due to pathogenic attack (infectious disease) and other factors (noninfectious disease) (Mehrotra and Aggarwal, 2003). This in turn leads to the death or partial impairment of certain plant parts (Agrios, 2005). Various pathogens require different conditions for pathogenesis. The fundamental requirements for the progression of a successful infectious disease are: (1) a vulnerable host, (2) an infectious or virulent pathogen, (3) suitable weather conditions for infection to start, (4) inhabitation of pathogens in the host leading to colonization, and (5) generation of infectious propagules to transmit infection. All these are necessary for an infection to develop in plants, and weather is the most significant factor because of its dynamic nature (Yán˜ez-Lo´pez et al., 2012). Changes in climate in the coming years may negatively affect agriculture as a result of weather extremes, deforestation, the rising level of carbon dioxide, floods, desertification, and droughts (IPCC, 2009). Because of the increasing population globally and climatic change, the greatest challenge is to provide food to all people in the future. This chapter focuses on the techniques that can be used for the prevention of potential diseases of major crop plants under the impact of a changing environment.


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CHAPTER 9 Preventing Potential Diseases of Crop Plants

9.2 Major crops and techniques for preventing hazardous stress Certain conditions optimum to pathogen spread, such as humidity and a rise in temperature, may lead to an increase in the number of epidemics in many geographic areas. Thus, there is a significant need for new strategies in agriculture to prevent the potential hazards pathogens may cause due to climatic change. The following subsections describe the diseases of major crops and research done for their prevention.

9.2.1 Wheat Wheat (Triticum aestivum L.) is an important cereal crop and a primary food source for humans. Wheat can be affected by a variety of biotic stresses, some of which are discussed next.

9.2.1.1 Powdery mildew Powdery mildew is caused by Blumeria graminis and is one of the most devastating anomalies of wheat; it can reduce crop yield from 13 to 34% (Leath and Bowen, 1989; Griffey et al., 1993). Race-specific resistance has monogenic inheritance and is expressed at the vegetative stage, whereas plant resistance retards growth and reproduction of pathogens at the adult stage. Knox and its derivative Massey inherited ample amounts of adult plant resistance (APR) against powdery mildew disease (Starling and Roane, 1984). Chromosomes 6B and 7B have the highest number of powdery mildew resistance genes. Molecular markers, such as amplified fragment length polymorphism (AFLP), restriction fragment length polymorphisms (RFLP), randomly amplified polymorphic DNA (RAPD), simple sequence repeats (SSR), and sequence tagged sites (STS), are paramount for identification of powdery mildew resistance genes across different types of wheat populations (Michelmore et al., 1991). The following list summarizes the research work done to characterize the molecular basis of powdery mildew in wheat: •

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F2:3 lines derived by a cross of Libellula/Huixianhong were phenotyped for two years in Beijing and for one year in Anyang. Three quantitative trait loci (QTL) identified on chromosomes 2DS and 6BL (QPm.caas-2DS, QPm.caas-6BL.1, and QPm.caas-6BL.2) were characterized as new. The QTLs identified on the short arm of chromosome 7A (QPm.caas-7DS) coincided with the slow rusting and slow mildewing locus Lr34/Yr18/Pm38 (Asad et al., 2012). Three QTLs for adult plant resistance were identified in a population of F2:3 derived from Becker/Massey (BM). The QTLs identified on 1B (QPm.vt-1BL), 2A (QPm.vt-2AL), and 2B (QPm.vt-2BL) explained 12 to 13%, 59 to 69%, and 22 to 48% of the phenotypic variance for powdery mildew severity, respectively (Tucker et al., 2006). Zhang et al. (2010) mapped the powdery mildew resistance gene (Ml3D232) flanked by a marker interval of Xgwm415 and Xwmc75 on chromosome 5BL of the F2 population. More than 60 allelic variants of powdery mildew resistance genes have been identified and localized across the whole genome of bread wheat (Alam et al., 2011; Xue et al., 2012). However, virulence genes of Bgt isolates hamper their resistance potential (Limpert et al., 1987). Doubled haploid (DH) lines derived from the cross of Bainong 64 3 Jingshuang 16 were genotyped with SSR in order to identify the QTLs associated with adult plant resistance. Four

9.2 Major crops and techniques for preventing hazardous stress

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QTLs with phenotypic variation in the range of 6.3 to 22.7% for resistance to powdery mildew were detected on chromosomes 1A, 4DL, 6BS, and 7A through composite interval mapping. The QTLs identified on chromosomes 4D and 6B (QPm.caas-4DL and QPm.caas-6BS) were stable with phenotypic variation in the range of 15.2 to 22.7% and 9.0 to 13.2% (Lan et al., 2009). An accession of Triticum boeoticum (AbAb), the progenitor of A genome donor, showed resistance against a number of Bgt isolates. The recombinant inbred line (RIL) population derived from crosses of powdery mildew-resistant T. boeoticum acc. pau5088 with a powdery mildew-susceptible T. monococcum acc. pau14087 was genotyped with SSR, RFLP, STS, and DArT markers. QTL mapping identified two powdery mildew-resistance genes (PmTb7A.1 and PmTb7A.2) on the long arm of chromosome 7A. PmTb7A.2 is thought to be an allelic variant of Pm1. A powdery mildew-resistant gene (PmG25) flanked by simple sequence repeat has been mapped on chromosome 5 of Chinese Spring nulli-tetrasomic and ditelosomic lines (Alam et al., 2013).

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9.2.1.2 Wheat rust disease The most hazardous and widespread obligate pathogen of wheat is rust, which reduces crop yield due to decreased number of kernels per head and low kernel weight (Knott, 1989). The three different types of rusts are stem, leaf, and stripe. Wheat leaf rust, caused by Puccinia triticina Eriks, leads to more wide-scale epidemics than stem rust or stripe rust. There are more than 120 leaf and stem rust-resistance genes in wheat, and molecular markers linked to these resistant genes have been identified (Chelkowski and Stepien, 2001). Triticum aestivum cultivars are a prime source of Lr resistance genes but initially resistance genes were introduced from wild species; the contribution of these with respect to Lr resistance genes is presented in Table 9.1. Leaf rust resistance genes cover the whole genome of hexaploid wheat. Four allelic variants of Lr2 (McIntosh and Baker, 1968) and two allelic variants of Lr22 (Rowland and Kerber, 1974) have been mapped on chromosome 2DS, whereas three variants of Lr3 have been identified on the long arm of chromosome 6BL (Haggag and Dyck, 1973). Two tightly linked allelic variants of Lr14 mapped on the long arm of chromosome 7B are considered important resistant loci against rust disease (Dyck and Samborski, 1970). Table 9.2 lists the cloned and sequenced Lr genes in wheat. The common feature of Lr1, Lr10, and Lr21 is the occurrence of nucleotide-binding site (NBS)leucine-rich repeat (LRR) regions, which is characteristic of disease-resistance genes in plants. Molecular characterization of these resistance genes results in new biological systems for in-depth study of the signal transduction pathway and function. All the identified stem rust-resistance genes

Table 9.1 Major Wild Species Contributors in Leaf Rust Resistance Number

Species

Resistance Genes

1 2 3 4 5

Aegilops umbellulata Aegilops squarrosa Agropyron elongatum Aegilops speltoides Aegilops ventricosa

Lr 9 Lr 21, Lr 22, Lr 32, Lr 39, Lr 40, Lr 41, Lr 42, Lr 43 Lr 19, Lr 24, Lr 29 Lr 28, Lr 35, Lr 36, Lr 47 Lr 37

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Table 9.2 List of Cloned and Sequenced Lr Genes in Wheat Number

Genes

Reference

1 2 3

Lr 1 Lr 10 Lr 21

Cloutier et al. (2007) Feuillet et al. (2003) Huang et al. (2003)

are race-specific except Sr2, a prime source of durable nonrace-specific resistance (McIntosh et al., 1995; Singh et al., 2004). The Sr2 gene identified on the short arm of chromosome 3B has been used extensively for improvement of wheat against stem rust resistance. Pyramiding of the Sr2 locus with other stem resistance genes ameliorates the devastating impact of Ug99 (Soliman et al., 1964). It is a prime resource for studying the inheritance of polygenic traits (e.g., stem rust resistance), as described in the following. •

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Sr2/Yr30 genes have been mapped on chromosome 3B and Sr57/Lr34/Yr18/Pm38 genes on 7D. In addition to these genomic regions, APR genes have been mapped on chromosomes 1A, 2B, 2D, 4A, 4B, 5A, 5B, 6B, and 7A (Bhavani et al., 2011). APR stem rust resistance QTLs have also been mapped on the long arm of chromosome 2B (Kolmer et al., 2011). Stem rust-resistant QTLs have been identified on chromosomes 3B, 5DL, and 7A of the recombinant inbred population derived from HD2009/WL711 (Kaur et al., 2009). Major and minor QTLs have been mapped on chromosomes 5B and 7D, 1AS, and 7B in a RIL population derived from Arina/Forno (Bansal et al., 2008). Epistatic interaction of stem rust-resistance genes has also been investigated in durum (Singh et al., 2012a), spring wheat (Yu et al., 2011), and winter wheat (Yu et al., 2012). A DH population derived from Canadian wheat cultivars, AC Cadillac and Carberry, was genotyped with DArT and SSR markers in order to identify stem rust severity and infection response to Ug99 in Kenya and Canada for a number of years. Eight QTLs for stem rust resistance with a phenotypic variance in the range of 2.4 to 48.8% were identified on eight chromosomes and three QTLs for pseudo-black chaff. Both parents contributed rust resistance, although this impact was greater than the AC Cadillac parent. Epistatic QTLs were identified on chromosomes 3B, 4B, 5B, 6D, and 7B. Synergistic interactions of QTLs on chromosomes 6D and 5B improved the disease resistance response to rust (Singh et al., 2013). An International Triticeae Mapping Initiative (ITMI) population was phenotyped for leaf rust and stripe rust in India. A linkage map containing 1345 markers identified 14 main-effect QTL (M-QTL) for leaf rust and 12 M-QTL for stripe rust. Two novel QTLs were identified for leaf and stripe rust resistance in the ITMI mapping population. Epistatic QTLs were identified for 16 leaf rust and 14 yellow rust. Four genomic regions contained QTLs for both leaf rust and stripe rust. Major QTLs for leaf rust resistance explained the phenotypic variation in the range of 2.16 to 29.07% and from 0.80 to 7.05% for stripe rust resistance. Phenotypic variation of epistatic QTLs for leaf and stripe rust resistance was 26.01% and 31.51%, respectively (Kumar et al., 2013).


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A recombinant inbred population derived from Chuanmai 32/Chuanyu 12 was used to map QTLs for APR for stripe rust in Chengdu and Yaan, Sichuan, from 2005 to 2008. Two QTLs, QYr.caas-3BL and QYr.caas-3BS, originating from Chuanmai 32 and Chuanyu 12 explained 20.1% and 6.6% of the phenotypic variation respectively (Ling et al., 2012). Three RIL populations, Capo 3 Isengrain, Capo 3 Furore, and Capo 3 Arina, were screened for adult plant leaf rust resistance across multiple environments. These populations were genotyped with SSR, AFLP, and DArT. Significant Capo-derived QTLs were identified on chromosomes 2A, 2B, and 3B for leaf rust resistance. Major QTLs analogous to Lr14a for leaf rust derived from susceptible parent Isengrain in the Capo 3 Isengrain population was mapped on chromosome 7B. Two major QTLs for stripe rust resistance were identified on chromosomes 2B and 3B in the Capo 3 Furore population (Matiasch et al., 2011). Two adult plant stripe resistance genes, Yr18 and Yr36, have been cloned in wheat (Ausemus et al., 1946). A DH population derived from Bainong 64 3 Jingshuang 16 was phenotyped for leaf and stripe rust. Genotyping was accomplished through bulk segregant analysis by using simple sequence repeats. QTL analysis identified five genomic regions conferring resistance to two types of rust disease. Two QTLs identified on the long arm of chromosome 1B and the short arm of chromosome 6B conferred resistance to both diseases. Minor QTLs for stripe rust response were identified on chromosomes 7AS and 4DL, whereas one major QTL for leaf rust was identified on the short arm of chromosome 6B near the centromeric region. The loci identified on chromosomes 1BL and 4DL were also significantly linked with powdery mildew response. Adult plant resistance is an efficient strategy to provide long-term protection against the plethora of biotic stresses to crops. Recombinant inbred lines were produced by a cross of Naxos and Shanghai 3/Catbird. QTL analysis through composite interval mapping identified four stripe rust-resistant QTLs having phenotypic variation in the range of 1.9 to 27.6% across two environments. QTLs for stripe rust resistance identified on chromosome 1D (QYr.caas1DS) flanked by molecular markers XUgwm353-Xgdm33b were considered new for stripe rust (Ren et al., 2012a,b). An RIL population derived from PBW343/Muu was phenotyped at Njoro, Kenya, and genotyped with diversity arrays technology (DArT) markers. Three QTLs (QSr.cim-2BS, QSr. cim-3BS, and QSr.cim-7AS) derived from Muu and one locus derived from PBW343 (QSr.cim5BL) were mapped on chromosomes 2BS, 3BS, 7AS, and 5BL, respectively. The QTL identified on chromosome 3BS mapped on the matching region as the well-known APR gene Sr2 (Singh et al., 2013). Another stripe rust-resistant gene Yr26, conferring resistance to all races of Puccinia striiformis f. sp. tritici (Pst), was mapped on the long arm of chromosome 1B of the deletion bin. F2 population and F2:3 progenies derived from Avocet S 3 92R137 were used to saturate the chromosomal region harboring Yr26 locus. The EST-STS markers flanking in the vicinity of Yr26 were used to identify the collinearity of wheat with rice and Brachypodium distachyon genomes. Conserved markers found in the collinear genome were used for fine mapping of Yr26 and two putative-resistant analogs were identified in the collinear region of B. distachyon. The conserved markers in the collinear genome provides a potential target site for further map-based cloning of Yr26 and are paramount in marker-assisted selection (MAS) for pyramiding the gene with other resistance genes (Zhang et al., 2013).

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9.2.1.3 Karnal bunt and fusarium head blight Another cause of damage to wheat is Tilletia indica Karnal bunt. Two recombinant inbred populations derived from crosses of the susceptible cultivar WH542 with resistant lines HD29 and W485 were used to map QTLs for Karnal bunt. Two QTLs, Qkb.ksu-5BL.1 and Qkb.ksu-6BS.1 with resistance alleles from HD29, were identified in the vicinity of markers Xgdm116-Xwmc235 and Xwmc105-Xgwm88, which explained 19% and 13% of phenotypic variation, respectively; Qkb. ksu-4BL.1 carrying a resistance allele from W485 explained 15% of phenotypic variance (Singh et al., 2007). A recombinant inbred population derived from HD29 and WH542 was phenotyped for multiple traits across multiple environments. Multitrait analysis identified 13 QTLs on 9 chromosomes for Karnal bunt, tan spot, stripe rust, and leaf rust with phenotypic variations of 57%, 55%, 38%, and 22%, respectively. The most significant QTLs for Karnal bunt resistance were identified on chromosomes 1BS, 2DS, 3BS, 4BL, 5BL, and 5DL. Chromosomes 3AS and 4BL were significantly linked with tan spot resistance. Major QTLs for stripe rust resistance were identified on chromosomes 2AS, 4BL, and 5BL. Leaf rust-resistant loci were identified on the short arm of chromosome 6D. The long arm of chromosome 4B of the RIL population was significantly linked with Karnal bunt, tan spot, and stripe rust-resistant QTLs (Singh et al., 2012). Fusarium head blight is a fungal disease of wheat in both temperate and semitropical regions. DHs derived from the cross “CM-82036” (resistant)/“Remus”(susceptible) were phenotyped for fusarium head blight. DHs were genotyped with AFLP and SSR. A major QTL for fusarium head blight resistance was identified on the short arm of chromosome 3B and explained up to 60% of the phenotypic variance. Two other loci for disease resistance were identified on chromosomes 5A and 1B. QTL identified on chromosome 1B was cosegregating with high-molecular-weight proteins (Buerstmayr et al., 2002). QTL mapping of 358 recent European winter wheat varieties plus 14 spring wheat varieties identified fusarium head blight QTLs on all chromosomes except 6B. Chromosome 5B was characterized with the highest number of marker trait associations (Kollers et al., 2013).

9.2.1.4 Stagonospora nodorum blotch One of the important foliar and glume diseases in cereals is Stagonospora nodorum blotch. A DH mapping population derived from a cross of partially resistant Triticum aestivum “Liwilla” and susceptible Triticum aestivum “Begra” was genotyped through bulk segregant analysis by using 240 microsatellite markers. Four QTLs associated with partial resistance components were found to be localized on chromosomes 2B, 3B, 5B, and 5D (Czembor et al., 2003). Chromosomes 4B, 5B, and 6A of a DH population were reported to contain QTLs significantly linked with Stagonospora nodorum blotch resistance (Reszka et al., 2007). A recombinant inbred population developed from a cross of Salamouni and Katepwa was genotyped with 441 SSR, 9 RFLP, 29 expressed sequence tag STS markers, and 5 phenotypic markers. Total length of the linkage map was 3228 centimorgans (cM) with an average marker density of 6.7 cM/marker. Two QTLs for Stagonospora nodorum (QSnb.fcu-1A and QSnb.fcu-7A) were identified on chromosome arms 1AS and 7AS with phenotypic variation of 23.5% and 16.4%, respectively (Abeysekara et al., 2012). Host resistance plays an important role in eliminating the devastating impact of Stagonospora nodorum blotch disease. Toxin-sensitive genes of the host can be mapped by purification and characterization of


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host-specific toxins. The Snn3 QTL linked with SSR and SNP was mapped in a Kenyon/86ISMN 2137 population (Friesen et al., 2008). Tan spot, caused by the fungus Pyrenophora tritici-repentis, results in serious yield losses in wheat (Triticum aestivum). Recombinant inbred lines derived by a cross of Indian spring wheat. WH542 (resistant) and HD29 (moderately susceptible) were phenotyped for tan spot. Two QTLs originating from WH542 for tan spot were identified on chromosomes 3A and 5B, explaining 23% and 27% of the phenotypic variation (Singh et al., 2008).

9.2.2 Maize Maize is a C4 and cross-pollinating crop. These important attributes contribute to high biomass production and a broad spectrum of geographic adaptation. In addition to economic significance, corn is a model crop for genetic research. Common diseases of maize and techniques for their prevention are described in the following subsections.

9.2.2.1 Maize streak virus Maize streak virus (MSV) disease is common in maize. Resistance to MSV is a significant quantitative attribute for maize breeding. The F2:3 lines derived from a cross between maize inbred lines, CML202 (resistant) and Lo951 (susceptible), were used to map QTLs for resistance to MSV. Major and minor QTLs for maize streak virus were identified on chromosomes 1, 2, 3, and 10 of an F2 population of D211 (resistant) 3 B73 (susceptible). These QTLs explained 48 to 62% of phenotypic variation (Pernet et al., 1999). RILs derived from one resistant MAL13 and one susceptible MAL9 were genotyped by using simple sequence repeats. This population was phenotyped in replicated trails under an artificial inoculation system. Three significantly linked markers, umc2228, umc2229, and bnlg1832, explained 93%, 78.9%, and 71.3% of phenotypic variation at an LOD score of 27.7, 13, and 18.7, respectively (Lagat et al., 2008). Recombinant inbred lines derived from a cross between hA9104 and hA9035 inbred lines were genotyped with SSR with a total length of 2123.1 cM. A multiple QTL mapping identified 15 loci on chromosomes 1, 2, 5, 6, 9, and 10. Both parents contributed the positive allele against southern corn rust (Wanlayaporn et al., 2013).

9.2.2.2 Leaf blight Northern leaf blight (NLB) caused by Exserohilum turcicum is a significant fungal disease of maize. The inbred mapping (IBM) population, an advanced inter-cross RIL population, derived from a cross between Mo17 and B73 lines, was evaluated for NLB resistance. Two QTLs conferring resistance to northern leaf blight were identified for this mapping population (Balint-Kurti et al., 2010). Genetic resistance to leaf blight is a quantitative polygenic trait and its effect can be additive or recessive (Kump et al., 2010). QTLs for blight resistance have been mapped in a population derived from a cross between maize lines B73 and Ki14 (Zwonitzer et al., 2010). QTLs for southern leaf blight have been mapped on chromosomes 3, 8, 9, and 10 in three different mapping populations derived from maize lines (Negeri et al., 2011). An inter-cross RIL population identified a significant correlation between northern leaf blight disease and gray leaf spot. Twenty-nine QTLs with multiple alleles were identified in 5000 inbred-line nested association mapping populations for

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resistance to northern leaf blight. Genotyping of the nested population with 1.6 million SNPs identified multiple candidate genes involved in plant defense phenomena (Polanda et al., 2011).

9.2.2.3 Head smut Maize head smut, caused by the fungus Sphacelotheca reiliana 21 (Ku¨hn) Clint, results in significant yield loss worldwide (Vanderplank, 1968). Scarcity of resistant cultivars is a significant obstacle to conventional breeding. Maize breeders are trying to identify molecular markers closely associated with resistant genes; 120 markers were used to map 100 individuals of recombinant inbred populations derived by a cross of Hi34 and TZil7. Four QTLs for head smut resistance were identified on chromosomes 1, 3, 9, and 10 by Lu and Brewbaker (1999). Li et al. (2008a) detected five QTLs on chromosomes 1, 2, 3, 4, 7, 8, and 9. A major head smut-resistant QTL (qHSR1) was fine mapped in bin 2.09 of RILs derived from the cross of Ji1037 and Huangzao4 (Chen et al., 2008). A genome-wide association study (GWAS) of head smut is a powerful molecular approach for identification of genetic factors for resistance in maize. Eighteen novel candidate genes involved in the resistance genes and pathogencity were identified by using single nucleotide polymorphic markers on 144 individuals of RILs (Wang et al., 2012). An F2 population with 191 individuals derived from the cross of two elite inbreds, Mo17 and Huangzao4, and the corresponding 184 F3 families were evaluated for head smut resistance. Genotyping of the F2 population was accomplished with 49 AFLP and 91 SSR markers, and QTL analysis was conducted with composite interval mapping (CIM). Five putative QTLs with phenotypic variation in the range of 10.0 to 16.3% were detected on chromosomes 1, 2, 3, 8, and 9.

9.2.2.4 Stewart’s disease Stewart’s bacterial wilt caused by Erwina stewartii, syn. Pantoea stewartii, is increasing day by day because of favorable weather and resistant hybrids. Partial resistance is more durable compared to simple resistance (Vanderplank, 1968). Transfer of partial resistance is difficult owing to its multigenic inheritance. A molecular mapping approach coupled with MAS is preferable for identification and exploitation of resistant cultivars (Young, 1996). Resistance exhibited by IL677a and IL731a is an example of simple inheritance (Meyer et al., 1991), whereas Ming et al. (1999) identified the major QTLs (swl) for Stewart’s resistance on chromosome 1S and a minor QTL on chromosome 9. An F2:3 population of maize derived from IL731a and W6786 was mapped with RFLP markers in order to identify QTLs conferring resistance to Stewart’s disease. QTLs for this trait were identified on chromosomes 4, 5, and 6 (Brown et al., 2001).

9.2.2.5 Gray leaf spot One of the foliar diseases of maize is gray leaf spot (GLS); it is a result of the causal fungal pathogen Cercospora zeae-maydis. A segregating population derived by a cross of highly resistant inbred line Y32 and a susceptible line, Q11, was used for genetic analysis and QTL mapping. Four QTLs with phenotypic variation in the range of 2.53 to 23.90% identified on chromosomes 1, 2, 5, and 8 were found to confer GLS resistance. Two major QTLs, qRgls1 and qRgls2, identified on chromosomes 5 and 8 were consistently detected across different locations and replicates. QTL qRgls2 was located in the vicinity of GLS resistance, whereas QTL-qRgls1 was fine-mapped on an interval of


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1.4 Mb, flanked by the markers GZ204 and IDP5. This identified QTL is a potential candidate to increase resistance of cultivars to gray leaf spot (Zhang et al., 2012). An F2 population was genotyped with SSR and single marker analysis was performed to identify significant associations of markers with QTL. Two markers, umc2082 and umc1117, identified in bins 4.03 and 4.04 are promising for cultivar screening against gray leaf spot (Veiga et al., 2012).

9.2.2.6 Anthracnose stalk rot Two maize populations derived from a cross of DE811ASR 3 DE811 and of DE811ASR 3 LH132 were used to identify genes conferring resistance to anthracnose stalk rot (ASR). Restriction fragment length polymorphism-based molecular markers identified strong QTL on linkage group 4 in both mapping populations (Jung et al., 1994). Resistant QTL to anthracnose stalk rot derived from the maize line MP305 has been identified on the long arm of chromosome 4. One candidate gene (Rcg1) with homology to a putative disease-resistance gene in rice has been identified in B73 and Mo17 BAC sequences.

9.2.3 Rice Rice is a staple for more than half of the population of the world. Acute reduction in rice production due to biotic and abiotic stresses is a serious threat to food security. The following subsections discuss major biotic stresses encountered by rice.

9.2.3.1 Rice blast One of the serious threats to rice yield is blast caused by Magnaporthe oryzae. The rice plant is vulnerable to M. oryzae at all growth stages (Sharma and Bambawale, 2008). Resistance of the rice plant to this disease can be achieved by pyramiding resistance genes, identified on chromosomes 6, 11, and 12 (Koide et al., 2009). Two consistent QTLs for blast resistance were identified on chromosome 11 of the RILs population at two growth stages and multiple inconsistent QTLs were detected due to complex epistatic and environmental interactions (Li et al., 2008b,c). Xu et al. (2008) mapped a major QTL (BFR4-1) on chromosome 4, originating from upland rice Kahei under field conditions by using a novel resistance strategy on a recombinant inbred population. Annotation analysis confirmed the presence of a nucleotide-binding site and leucine-rich repeat (NBS-LRR)-type; landmarks for resistance genes. RILs derived from Oryza minuta and O. sativa subsp. japonica var. Junambyeo were genotyped with STS and SSR markers. QTL mapping identified five loci against blast on chromosomes 6, 7, 9, and 11 (Rahman et al., 2011). Resistance to rice blast is a polygenic trait and inherited by multiple major and minor QTL. QTL analysis was conducted on the F3 population to dissect the complex genetic inheritance of blast resistance. Fifteen QTLs for blast resistance with varying levels of phenotypic variation were detected on chromosomes 1, 2, 3, 5, 6, 11, and 12 (Ashkani et al., 2012). QTL mapping of DH populations derived from a cross between Mowanggu (resistant cultivar) and Ewan8 (susceptible cultivar) identified three QTLs with phenotypic variations in the range of 7.7 to 15.2% on chromosome 6 of rice (Xiao-lin et al., 2012).

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9.2.3.2 Brown spot Brown spot caused by Cochliobolus miyabeanus is one of the serious diseases of rice. Three QTLs for brown spot with an LOD score of .3.3 explaining 9.5% and 18.4% of phenotypic variation were identified on chromosomes 4, 6, and 8 in a DH mapping population of rice (Dudhare et al., 2008). Two other QTLs (BSq4.1 and BSq11) associated with brown spot on chromosomes 4 and 11 were identified by Katara et al. (2010) as good candidates for fine-mapping and positional cloning studies.

9.2.3.3 Sheath blight Sheath blight disease of rice caused by Rhizoctonia solani is a significant devastating anomaly for rice worldwide. A total of 33 QTLs linked with sheath blight resistance cover the whole genome of rice. Ten of 33 identified ShB-resistant QTL were cosegregating with plant height and days to heading attributes (Laetitia and Serge, 2011). Jasmine 85, an indica cultivar, is reported to be highly resistant for this pathogen. Ten Sh blight-resistant QTLs were identified on chromosomes 1, 2, 3, 5, 6, and 9 of RILs at the seedling stage, inoculated using micro-chamber and mist-chamber assays under greenhouse conditions. A major ShB-QTL (qShB9-2) cosegregating with a SSR marker, RM245, explained 27.2% of the phenotypic variation on chromosome 9 (Liu et al., 2009). Association mapping of 217 subcore entries from the US Department of Agriculture rice core collection yielded the highest number of putative ShB-resistant QTLs in entry GSOR 310389 (Jia et al., 2012). A doubled haploid population of Maybelle and Baiyeqiu was used to identify QTLs controlling rice ShB resistance. QTLs for rice sheath blight were identified on four different chromosomes; the loci identified on chromosome 1B (qShB1) explained 8.9% and 13.2% of phenotypic variation across two years (Xu et al., 2011). A recombinant inbred population was evaluated for sheath blight; the QTLs were identified on chromosome 1 and explained 12.7% of variation at Shanghai and 42.6% at Hainan (Fu et al., 2012). Liu et al. (2013) confirmed the presence of major ShB-QTL on chromosome 9 under field conditions and also identified one new QTL for sheath blight resistance in the vicinity of markers RM221 and RM112 on chromosome 2 across multiple environments.

9.2.3.4 Bacterial leaf blight and leaf streak One of the major hazardous diseases to rice is bacterial blast caused by Xanthomonas oryzae pv. oryzae (Xoo) (Wen et al., 2003). As a result of this anomaly, 15 to 25% yield losses have been observed each year. There are two types of bacterial blight resistance: (1) vertical resistance is race-specific, has monogenic inheritance, and can be easily dissected (Mew et al., 1992); and (2) horizontal inheritance is a complex, nonrace-specific polygenic inheritance (Nelson, 1972). Bacterial leaf streak (BLS) is a major disease in rice caused by the pathogen Xanthomonas oryzae pv. oryzicola. An F2 and an RI population were used for mapping of bacterial leaf streak. QTL mapping by composite interval mapping detected 11 QTLs on six chromosomes that explained 84.6% of phenotypic variation (Tang et al., 2000). Anchoring of in silico was performed on a CT9993-5-10-1-M/IR 62266-42-6-2 DH population to identify QTL for bacterial blight resistance and one QTL was mapped on chromosome 10 (Reddy et al., 2008). A bacterial blight-resistant gene (Xa7) has been identified in an Indonesian local rice population. The translated sequence of 60 amino acids showed similarity with BTB/POZ,


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a gene involved in a defense system against biotic stresses (Utami et al., 2013). Basmati rice having resistance against bacterial blight, blast, and sheath blight has been developed by Singh et al. (2012b) through MAS. A multiparent advanced generation inter-cross population (MAGIC) was genotyped using a genotyping-by-sequencing (GBS) approach. With it phenotyping was accomplished across multiple environments in order to identify genomic regions associated with blast and bacterial blight resistance, salinity and submergence tolerance, and grain quality. Genome-wide association mapping identified Xa4 and Xa5 loci associated with resistance to bacterial blight (Bandillo et al., 2013).

9.2.4 Barley Barley is a major crop cultivated all over the world. The work done by many researchers has contributed to a better understanding of plants’ genetic basis against stress resistance (Ramsay et al., 2011). Major biotic stresses encountered by barley are highlighted in the next subsections.

9.2.4.1 Net blotch Barley net form net blotch (NFNB), caused by the necrotrophic fungus Pyrenophora teres f. teres, is a significant foliar malady of barley, particularly in medium and low rainfall areas. Lesions appear as thin brown streaks both in longitudinal and horizontal form giving a net-like appearance. This disease affects both the quality and quantity of the grain. Twenty to 30% yield losses have been observed due to the reduced number of grains per spike and thousand grain weight. The sixrowed Canadian barley cultivar, Heartland, was characterized as a prime source of resistance against net blotch (Steffenson and Smith, 2006). Retrotransposon markers mapped dominant genes for NFNB seeedling resistance on chromosome 6H (Manninen et al., 2000). This chromosone has been reported to contain multiple independent resistance genes against this disease (Abu Qamar et al., 2008). QTL analysis of the DH population derived from a cross of SM89010 and Q21861 identified major loci for net blotch resistance on chromosome 6H (Friesen et al., 2006). One spot blotch QTL identified on chromosome 1H explained 79% of phenotypic variation (Tajinder et al., 2012). A mapping population of RILs derived from “Hector” (susceptible) and “NDB112” (resistant) was genotyped with 692 SNP and 77 SSR markers. One QTL governing barley net blotch resistance was identified on chromosome 6H (Liu et al., 2012).

9.2.4.2 Scald Scald, caused by the fungus Rhynchosporium secalis, is a common and widespread disease of barley, which appears as oval, gray-green spots on leaves, sheaths, and heads. Yield losses up to 45% have been observed due to this fungal disease causing leaf senescence and a reduced number of grains per ear. A recombinant inbred population containing 103 individuals derived from the L94 3 Vada cross was evaluated under field conditions for resistance against powdery mildew (Blumeria graminis f.sp. hordei) and scald (Rhynchosporium secalis). Three QTLs (Rbgq1, Rbgq2, and Rbgq3) for resistance against powdery mildew were detected on chromosomes 2 (2H), 3 (3H), and 7 (5H), respectively. Four QTLs for scald resistance were identified on chromosomes 3 (3H), 4 (4H), and 6 (6H) (Shtaya et al., 2006).

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Two barley DH populations derived from TX9425 3 Franklin and Yerong 3 Franklin were screened for APR against powdery mildew and scald in the field and glasshouse under natural infection. Two QTLs for resistance against powdery mildew were identified in the TX9425 3 Franklin population to chromosomes 7H and 5H and explained 22% and 17% of phenotypic variation. Three major loci were identified in the Yerong 3 Franklin population for resistance against powdery mildew. The major QTL among this group identified on the short arm of chromosome 1H explained 66% of phenotypic variation. A major QTL for scald resistance was identified on chromosome 3H on both mapping populations (Li and Zhou, 2011).

9.2.4.3 Powdery mildew Powdery mildew disease, caused by the fungus Blumeria graminis f.sp. hordei synonym Erysiphe graminis f.sp. hordei, appears as fluffy white growth on the surface of the leaf. The race-specific locus Mla identified on choromosome 1H encodes 32 different Bgh-resistant genes (Wei et al., 1999). Another significant source of race nonspecific resistance to Bgh is mlo (Lyngkjaer et al., 2000). One powdery mildew-resistant gene mapped on chromosome 7H of RIL explained 45% of the phenotypic variance (Silvar et al., 2010). An F2 population derived from the accession PI466197 of wild barley (Hordeum vulgare sp. spontaneum) and Blumeria graminis f.sp. hordei was genotyped with SSRs, STS, and one cleaved amplified polymorphic sequence (CAPS) marker. One of the resistance genes from H. vulgare ssp. spontaneum PI466197 was identified on the short arm of chromosome 1H. The other gene for resistance was identified on the short arm of chromosome 2H (Teturova et al., 2010). Fungal spores grow in colonial form and infection results in senescence and abscission. A yield loss of 10 to 15% has been observed due to this disease. Orthologous QTL was identified in barley for powdery mildew disease resistance and showed collinearity with wheat powdery mildew disease-resistant QTL (Schweizer and Stein, 2011). Race nonspecific resistance is difficult to study because of its polygenic inheritance. An association-genetic study was conducted on a worldwide collection of spring barley in order to identify candidate genes of race nonspecific resistance to the powdery mildew fungus Blumeria graminis f.sp. hordei (Bgh). Eleven associated genes conferring resistance to this disease were identified (Spies et al., 2012).

9.2.4.4 Leaf rust Round, light orange-brown pustules on barley leaf caused by the fungus Puccinia hordei is severely hazardous to crop yield. Infection at an early stage of growth reduces yield by 30%. A recombinant IBM population derived by the single seed descent method of susceptible parent L94, with partially resistant parent Vada, was used to map QTL for rust resistance at the seedling and adult plant stage. Three loci (Rphq1, Rphq2, and Rphq3) identified at the seedling stage explained 55% of phenotypic variation for this trait, whereas five loci were stage specific and explained 60% of phenotypic variation (Qi et al., 1998). Rust-resistant QTL effective at seedling and adult plant stages have been identified on chromosome 6H (Marcel et al., 2007; Varshney et al., 2007). The leaf rust-resistant QTLs identified on chromosomes 2H and 3H were cosegregating with loci for flowering time (Castro et al., 2008). Resistant alleles for rust have been identified on the short arm of chromosome 5H by Hickey et al. (2011) and Liu et al. (2011). The QTL identified on chromosome 1H across multiple environments was in close vicinity to Rcs6, an SB resistance gene mapped by Bilgic et al. (2006) in the Calicuchima-sib/Bowman-BC mapping population. A new pathogen-conferring


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resistance to the rust pathogen of barley was detected on the short arm of chromosome 6H of DHs (Mehmet Cakir et al., 2011).

9.2.4.5 Spot blotch Spot blotch of barley is caused by the fungus Cochliobolus sativus (Ito & Kuribayashi) Drechs. ex Dastur (anamorphic: Bipolaris sorokiniana (Sacc.) Shoemaker) and is a common foliar disease. It is particularly prevalent in the upper Midwest of the United States. Spot blotch can cause marked reductions in both yield and the quality of the crop; therefore the disease is considered economically significant (Drader, 2011). Association mapping of barley germplasm identified three major QTLs against spot blotch disease on chromosomes 1H, 3H, and 7H during the seedling and adult plant stages (Zhou and Steffenson, 2013). A resistant QTL to spot blotch was identified on chromosomes 3HS and 7HS of four different mapping populations. The phenotypic variance of adult and seedling plants ranged from 16 to 25% and 52 to 64%, respectively (Jessica et al., 2010). A DH mapping population was phenotyped for spot blotch and leaf rust resistance across multiple environments. Ten loci for spot blotch were detected at the adult plant stage. The most consistent QTL for leaf rust segregating with markers, Bmag173-Bmag009, was identified on chromosome 6H (Castro et al., 2012).

9.2.5 Cotton Cotton is cultivated worldwide and yields 25 million tons per year. The United States has been the largest exporter of cotton for a long time. This important crop is threatened by various diseases, which result in yield losses. The following subsections describe the major biotic stresses of cotton.

9.2.5.1 Root-knot nematode disease Significant yield losses in cotton crops have been observed as a result of the soil-inhabiting southern root-knot nematode (RKN), Meloidogyne incognita. Host plant resistance is an important strategy for increasing cotton crop plants’ defense against RKN disease. Resistance can be effectively achieved through transgressive segregation in which a segregating hybrid exhibits novel phenotypes due to the epistatic interactions of genes (Rieseberg et al., 2003). In a cross of Pima S-7 3 Acala NemX and NemX 3 SJ-2, segregating factors from susceptible parents contributed to host plant resistance against RKN disease (Wang et al., 2006, 2008a). Transgressive segregation has also been observed for Verticillium wilt resistance in an F2 (resistant Pima S-7 3 susceptible Acala 44) (Bolek et al., 2005). In addition, in an F2:3 family, Wang et al. (2008b) observed fusarium wilt resistance in the F2 or F3 populations (resistant Pima S-7 3 susceptible Acala NemX or Acala SJ-2) (Wang et al., 2006). Bayles et al. (2005) found bacterial blight resistance in the BC4F4 generation within an intraspecific cross of cotton. Transgressive segregants have also been identified in Auburn 623 RNR and some N lines. Major QTLs for resistance of nematode disease have been identified in Acala NemX 3 Acala SJ-2, Acala SJ-2 3 Clevewilt, and Pima S-7 3 Acala NemX (Wang et al., 2006). Telomeric segmentation on chromosome 11 is well documented in harboring resistance genes against root knot in different mapping populations (Ulloa et al., 2010). Chromosome 11 of cotton contains many genes including resistance to RKN (Gutiérrez et al., 2010), reniform nematode (Dighe et al., 2009), fusarium wilt (Ulloa et al., 2010), Verticillium wilt, and black root rot. The marker CIR316-191/196 mapped on chromosome 11 was reported to be involved in both GI and EGR (Wang et al., 2006). A minor

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locus identified on chromosome 21 was found to be linked with egg production and root galling phenotypes in the F2 population of Pima S-7 3 Acala NemX (Ulloa et al., 2010). The homologous chromosome pair 11/21 has also been reported to be involved in reniform nematode resistance (Gutiérrez et al., 2010).

9.2.5.2 Cotton leaf curl virus QTL mapping of the F2 population derived from (Gossypium barbadense 3 Gossypium anomaulum) 3 Gossypium hirsutum identified two significant loci (qCLCVa1 and qCLCVa2) for the cotton leaf curl virus on chromosome 9 at 25 cM and 22.1 cM, respectively.

9.2.5.3 Fusarium wilt One of the major QTLs of Fov4 (Fov4-C14 1) has been identified on chromosome 14 of RILs. Additional genetic and QTL analyses also identified a set of 11 SSR markers linked with FOV race 4 resistance on chromosomes 3, 6, 8, 14, 17, and 25. Progeny derived from crosses of Upland and Pima cotton identified a major resistance gene for race 4 of the fusarium (Fov4) fungus. This single Fov4 gene has a major dominant expression and conferred resistance to FOV race 4 in Pima-S6 9 (Mauricio et al., 2013).

9.2.5.4 Verticillium wilt One of the serious threats to cotton is Verticillium wilt. The F2:3 families derived from XinLuZao1, susceptible cultivar (Gossypium hirsutum L.) and Hai7124, a resistant line (Gossypium barbadense L.), were genotyped with 430 SSR loci to construct 41 linkage groups. The total genetic map length of this population was 3745.9 cM with an average distance of 8.71 cM. Nine QTLs with phenotypic variation in the range of 10.63 to 28.83% were detected; all nine QTLs were D genome specific (Wang et al., 2008a). Jiang et al. (2009) used the F2:3 families to construct a genetic linkage map of this population. One-hundred and thirty-one loci constructed 31 linkage groups covering a distance of 1165 cM with an average distance of 8.38 cM. Two mapping populations of upland cotton (M3S2F5 and M3S2F5:6) were used to verify the significant linkage of 39 reported molecular markers with QTLs for Verticillium wilt resistance of cotton. JESPR153 and BNL3031 markers were identified as potential candidate loci for MAS (Li et al., 2013).

9.3 Conclusion and future prospects Occurrence of a certain disease in a plant depends on a multitude of factors including a diseasecausing virulent pathogen, a vulnerable host plant, and the environment. This forms a three-keyfactors triangle for the development of diseases. The changing climate becomes a significant issue and may be intensely associated with increases in yield losses in the coming years. An increased level of ozone and carbon dioxide, altered precipitation patterns, flooding, drought, temperature extremes, global warming, and salinity are the outcomes of climatic changes. These all directly or indirectly affect the occurrence and severity of diseases in plants. Conditions more optimum to pathogenic spread, such as humidity and increased temperature, may lead to increases in the number of epidemics in plants in new geographical areas. Thus, there is a significant necessity for new agricultural strategies to prevent the potential hazards that may be the result of pathogens due to

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climatic change. This chapter reviews different research strategies in order to characterize the root cause of diseases in major crops worldwide. Expression of fungal diseases can be modified by changes in atmospheric conditions. Increasing carbon dioxide may result in more incidences of disease and their increased severity (Shin and Yun, 2010). In the same way, temperature combined with rain is the key factor that determines disease incidence. Climate change may lead to the spread of diseases to new areas worldwide and affect the definite, spatial, as well as temporal, spread of crop diseases. Today, most agriculturists are well aware of new techniques, such as improved biotechnology and microbial and molecular tools, to increase yield, to fight pathogens, and to alter soil composition. All these have positively affected plant varieties; however, changes in climate and the emergence of new diseases are anticipated to pose a severe threat to some of the essential crops. Therefore, being dependent on agriculture for food, there is still a need for significant investments in this sector to avoid stunning and lethal consequences. Climate change is somewhat predictable and can be prepared for to lessen the side effects that may be caused by it. Clearly, agricultural research has increased and scientists have completed many biotic and abiotic stress studies in order to determine how to increase plant yield. Still a lot more is left to be done with regard to the climatic change. Because global warming may add to an area’s pretentious pests and diseases, more studies should be carried out. Researchers need to evaluate the effect of these changes and discover ways to manage the magnitude of diseases in order to lessen the infections’ threats. On the basis of host pathogen interfaces, disease risk investigations should be done so that the effect of imminent climatic change on disease occurrence can be better understood, as the following list suggests: •

• • • • •

Assess existing management plans and propose new alternatives according to the anticipated change in climate in the coming years. It would not only prepare breeders for the challenges of the changing environment but also allow them to mitigate stresses with effective measures, thus increasing crops’ ability to adapt to changes. Risk assessment of diseases should be analyzed more thoroughly. Model plants should be constructed for research in order to study interactions among the three variables: weather, disease, and crop. Characterize the factors affecting the growth of pathogens such as temperature, humidity, rain, and so on. Develop new tools to enhance adaptation of crops under different climatic conditions. Develop new crop varieties that are more productive in harsh environments.

References Abeysekara, N.S., Faris, J.D., Chao, S., McClean, P.E., Friesen, T.L., 2012. Whole genome QTL analysis of stagonospora nodorum blotch resistance and validation of the SnTox4-Snn4 interaction in hexaploid wheat. Phytopathology 102 (1), 94104. Abu Qamar, M.A., Liu, Z.H., Faris, J.D., Chao, S., Edwards, M.C., Lai, Z., et al., 2008. A region of barley chromosome 6H harbors multiple major genes associated with net type net blotch resistance. Theor. Appl. Genet. 117, 12611270. Agrios, G.N., 2005. Plant Pathology. fifth ed. Elsevier, USA, p. 922.

208


Alam, M.A., Xue, F., Wang, C., Ji, W., 2011. Powdery mildew resistance genes in wheat: identification and genetic analysis. J. Mol. Biol. Res. 1 (1). Alam, M.A., Mandal, M.S.N., Wang, C., Ji, W., 2013. Chromosomal location and SSR markers of a powdery mildew resistance gene in common wheat line N0308. Afr. J. Microbiol. Res. 7 (6), 477482. Asad, M.A., Bai, B., Lan, C.X., Yan, J., Xia, X.C., Zhang, Y., et al., 2012. Molecular mapping of quantitative trait loci for adult-plant resistance to powdery mildew in Italian wheat cultivar Libellula. Crop Past. Sci. 63 (6), 539546. Ashkani, S., Rafii, M.Y., Rahim, H.A., Latif, M.A., 2012. Genetic dissection of rice blast resistance by QTL mapping approach using an F3 population. Mol. Biol. Rep. 40 (3), 25032515. Ausemus, E.R., Harrington, J.B., Reitz, L.P., Worzella, W.W., 1946. A summary of genetic studies in hexaploid and tetraploid wheats. J. Am. Soc. Agron. 38, 10821099. Balint-Kurti, P.J., Yang, J., Van Esbroeck, G., Jung, J., Smith, M.E., 2010. Use of a maize advanced intercross line for mapping of QTL for northern leaf blight resistance and multiple disease resistance. Crop Sci. 50, 458466. Bandillo, N., Raghavan, C., Muyco, P.A., Sevilla, M.A., Lobina, I.T., Ermita, C.J.D., et al., 2013. Multi-parent advanced generation inter-cross (MAGIC) populations in rice: progress and potential for genetics research and breeding. Rice 6, 11. Bansal, U.K., Bossolini, E., Miah, H., Keller, B., Park, R.F., Bariana, H.S., 2008. Genetic mapping of seedling and adult plant stem rust resistance in two European winter wheat cultivars. Euphytica 164, 821828. Bayles, M.B., Verhalen, L.M., McCall, L.L., Johnson, W.M., Barnes, B.R., 2005. Recovery of recurrent parent traits when backcrossing in cotton. Crop Sci. 45, 20872095. Bent, A.F., 2003. Crop diseases and strategies for their control. In: Chrispeels, M.J., Sadava, D.E. (Eds.), Plants, Genes and Crop Biotechnology, second ed. Jones and Bartlett Publishers, Sudbury, MA, pp. 391413. Bhavani, S., Singh, R.P., Argillier, O., Huerta-Espino, J., Singh, S., Njau, P., et al., 2011. Mapping durable adult plant stem rust resistance to the race Ug99 group in six CIMMYT wheats. In: McIntosh, R. (Ed.), Proceedings of Borlaug Global Rust Initiative Technical Workshop. Saint Paul MN, pp. 4353. Bilgic, H., Steffenson, B.J., Hayes, P.M., 2006. Molecular mapping of loci conferring resistance to different pathotypes of the spot blotch pathogen in barley. Phytopathology 96, 699708. Bolek, Y., El-Zik, K.M., Pepper, A.E., Bell, A.A., Magill, C.W., Thaxton, P.M., et al., 2005. Mapping of verticillium wilt resistance genes in cotton. Plant Sci. 168 (6), 15811590. Brown, F., Juvik, J.A., Pataky, J.K., 2001. Quantitative trait loci in sweet corn associated with partial resistance to Stewart’s wilt, northern corn leaf blight, and common rust. Phyto. 91 (3), 293300. Buerstmayr, H., Lemmens, M., Hartl, L., Doldi, L., Steiner, B., Stierschneider, M., et al., 2002. Molecular mapping of QTLs for fusarium head blight resistance in spring wheat. I. Resistance to fungal spread (Type II resistance). Theor. Appl. Genet. 104 (1), 8491. Castro, A., Hayes, P.M., Viega, L., Vales, M.I., 2008. Transgressive segregation for phenological traits in barley explained by two major QTL alleles. Plant Breed. 127, 561568. Castro, A.J., Gamba, F., German, S., Gonzalez, S., Hayes, P.M., Pereyra, S., et al., 2012. Quantitative trait locus analysis of spot blotch and leaf rust resistance in the BCD47 3 Baronesse barley mapping population. Plant Breed. 131 (2), 258266. Chelkowski, J., Stepien, J., 2001. Molecular markers for leaf rust resistance genes in wheat. J. Appl. Genet. 42, 117126. Chen, Y., Chao, Q., Tan, G., Zhao, J., Zhang, M., Ji, Q., et al., 2008. Identification and fine mapping of a major QTL conferring resistance against head smut in maize. Theor. Appl. Genet. 117, 12411252. Cloutier, S., McCallum, B.D., Loutre, C., Banks, T.W., Wicker, T., Feuillet, C., et al., 2007. Leaf rust resistance gene Lr1, isolated from bread wheat (Triticum aestivum L.) is a member of the large psr567 gene family. Plant Mol. Biol. 65, 93106.

References

209

Czembor, P.C., Arseniuk, E., Czaplicki, A., Song, Q., Cregan, P.B., Ueng, P.P., 2003. QTL mapping of partial resistance in winter wheat to Stagonospora nodorum blotch. Genom. 46 (4), 546554. Dighe, N., Robinson, A.F., Bell, A., Menz, M., Cantrell, R., Stelly, D., 2009. Linkage mapping of resistance to reniform nematode in cotton (Gossypium hirsutum L.) following introgression from G. longicalyx (Hutch and Lee). Crop Sci. 49, 11511164. Drader, T.B., 2011. Cloning of the seedling spot blotch resistance gene Rcs5. Dissertations and Theses. Washington State University, Pullman, USA. Dudhare, M.S., Jadhav, P.V., Mishra, S.K., 2008. Molecular mapping of QTLs for resistance to brown spot. J. Plant Dis. Sci. 3 (1), 2123. Dyck, P.L., Samborski, D.J., 1970. The genetics of two alleles of rust. Can. J. Genet. Cytol. 12, 689694. Feuillet, C., Travella, S., Stein, N., Albar, L., Nublat, L., Keller, B., 2003. Map-based isolation of the leaf rust disease resistance gene Lr10 from the hexaploid wheat (Triticum aestivum L.) genome. Proc. Natl. Acad. Sci. USA 100, 1525315258. Friesen, T.L., Faris, J.D., Lai, Z., Steffenson, B.J., 2006. Identification and chromosomal location of major genes for resistance to Pyrenophora teres in a doubled-haploid barley population. Genome 49, 855859. Friesen, T.L., Zhang, Z., Solomon, P.S., Oliver, R.P., Faris, J.D., 2008. Characterization of the interaction of a novel Stagonospora nodorum host-selective toxin with a wheat susceptibility gene. Plant Physiol. 146 (2), 682693. Fu, D., Chen, L., Yu, G., Liu, Y., Lou, Q., Mei, H., et al., 2012. QTL mapping of sheath blight resistance in a deep-water rice cultivar. Euphytica 180 (2), 209218. Gregory, P.J., Johnson, S.N., Newton, A.C., Ingram, J.S.I., 2009. Integrating pests and pathogens into the climate change/food security debate. J. Exp. Bot. 60, 28272838. Griffey, C.A., Das, M.K., Stromberg, E.L., 1993. Effectiveness of adult-plant resistance in reducing grain yield loss to powdery mildew in winter wheat. Plant Dis. 77, 618622. Gutiérrez, O.A., Jenkins, J.N., McCarty, J.C., Wubben, M.J., Hayes, R.W., et al., 2010. SSR markers closely associated with genes for resistance to root-knot nematode on chromosomes 11 and 14 of Upland cotton. Theor. Appl. Genet. 121, 13231337. Haggag, M.E.A., Dyck, P.L., 1973. The inheritance of leaf rust resistance in four common wheat varieties possessing genes at or near the LR3 locus. Can. J. Genet. Cytol. 15, 127134. Hickey, L.T., Lawson, W., Platz, G.J., Dieters, M., Arief, V.N., Germán, S., et al., 2011. Mapping Rph20: a gene conferring adult plant resistance to Puccinia hordei in barley. Theor. Appl. Genet. 123, 5568. Huang, L., Brooks, S.A., Li, W., Fellers, J.P., Trick, H.N., Gill, B.S., 2003. Map-based cloning of leaf rust resistance gene Lr21 from the large and polyploid genome of bread wheat. Genet. 164165. Intergovernmental Panel on Climate Change (IPCC), 2009. IPCC Home Page. Available at ,www.ipcc.ch.. Jessica, B., Anke, L., Mark, S., Greg, P., Terry, U., Jerome, F., et al., 2010. Mapping spot blotch resistance genes in four barley populations. Mol. Breed. 26 (4), 653666. Jia, L., Yan, W., Zhu, C., Agrama, H.A., Jackson, A., et al., 2012. Allelic analysis of sheath blight resistance with association mapping in rice. PLoS ONE 7 (3), e32703. Jiang, F., Zhao, J., Zhou, L., Guo, W., Zhang, T., 2009. Molecular mapping of Verticillium wilt resistance QTL clustered on chromosomes D7 and D9 in upland cotton. Sci. China. C. Life. Sci. 52 (9), 872884. Jung, M., Weldekidan, T., Schaff, D., Paterson, A., Tingey, S., Hawk, J., 1994. Generation-means analysis and quantitative trait locus mapping of anthracnose stalk rot genes in maize. Theor. Appl. Genet. 89, 413418. Katara, J.L., Sonah, H., Deshmukh, R.K., Ravinder, C., Kotasthane, A.S., 2010. Molecular analysis of QTLs associated with resistance to brown spot in rice (Oryza sativa L.). Ind. J. Genet. Plant Breed. 70 (1), 1721.

210


Kaur, J., Bansal, U.K., Khana, R., Saini, R.G., Bariana, H.S., 2009. Molecular mapping of stem rust resistance in HD2009/WL711 recombinant inbred line population. Int. J. Plant Breed. 3, 2833. Knott, D.R., 1989. The wheat rust breeding for resistance. In: Yeo, A.R., Flowers, T.J. (Eds.), Monographs on Theoretical and Applied Genetics, vol. 12. Springer-Verlag, Berlin. Koide, Y., Kobayashi, N., Xu, D., Fukuta, Y., 2009. Resistance genes and selection DNA markers for blast disease in rice (Oryza sativa L.). Jpn. Agric. Res. Q. 43, 255280. Kollers, S., Rodemann, B., Ling, J., Korzun, V., Ebmeyer, E., et al., 2013. Whole genome association mapping of fusarium head blight resistance in European winter wheat (Triticum aestivum L.). PLoS ONE 8 (2), e57500. Kolmer, J.A., Garvin, D.F., Jin, Y., 2011. Expression of a thatcher wheat adult plant stem rust resistance QTL on chromosome arm 2BL is enhanced by Lr34. Crop Sci. 51, 526533. Kumar, J., Chhuneja, P., Jain, S., Kaur, S., Balyan, H.S., Gupta, P.K., 2013. Mapping main effect QTL and epistatic interactions for leaf rust and yellow rust using high density ITMI linkage map. Aust. J. Crop Sci. 7 (4), 492499. Kump, K.L., Holland, J.B., Jung, M.T., Wolters, P., BalintKurti, P.J., 2010. Joint analysis of near isogenic and recombinant inbred line populations yields precise positional estimates for QTL. Plant Genet. 3, 142153. Laetitia, W., Serge, S., 2011. Resistance to rice sheath blight (Rhizoctonia solani Ku¨hn) [(teleomorph: Thanatephorus cucumeris (A.B. Frank) Donk.] disease: current status and perspectives. Euphytica 178, 122. Lagat, M., Danson, J., Kimani, M., Kuria, A., 2008. Quantitative trait loci for resistance to maize streak virus disease in maize genotypes used in hybrid development. Afr. J. Biotechnol. 7 (14), 25732577. Lan, C., Liang, S., Wang, Z., Yan, J., Zhang, Y., Xia, X., et al., 2009. Quantitative trait loci mapping for adult-plant resistance to powdery mildew in Chinese wheat cultivar Bainong 64. Phytopathology 99, 11211126. Leath, S., Bowen, K.L., 1989. Effects of powdery mildew, triadimenol seed treatment, and triadimefon foliar sprays on yield of winter wheat in North Carolina. Phytopathology 79 (2), 152155. Li, C.Q., Liu, G.S., Zhao, H.H., Wang, L.J., Zhang, X.F., Liu, Y., et al., 2013. Marker-assisted selection of Verticillium wilt resistance in progeny populations of upland cotton derived from mass selection-mass crossing. Euphytica 191 (3), 469480. Li, H.B., Zhou, M.X., 2011. Quantitative trait loci controlling barley powdery mildew and scald resistances in two different barley doubled haploid populations. Mol. Breed. 27 (4), 479490. Li, X.H., Wang, Z.H., Gao, S.R., Shi, H.L., Zhang, S.H., George, M.L.C., et al., 2008a. Analysis of QTL for resistance to head smut (Sporisorium reiliana) in maize. Field Crop Res. 106, 148155. Li, Y., Wu, C., Xing, Y., Chen, H., He, Y., 2008b. Dynamic QTL analysis for rice blast resistance under natural infection conditions. Aust. J. Crop Sci. 2 (2), 7382. Li, Y., Ya-dong, Z., Zhen, Z., Ling, Z., Cai-Lin, W., 2008c. QTL analysis for resistance to rice false smut by using recombinant in bread lines in rice. Chin. J. Rice Sci. 22 (5), 472476. Limpert, E., Felsenstein, F.G., Andrivon, D., 1987. Analysis of virulence in populations of wheat powdery mildew in Europe. J. Phytopathol. 120, 18. Ling, W., Xian-Chun, X., You-liang, Z., Zheng-yu, Z., Hua-zhong, Z., Jian, L.Y., et al., 2012. QTL mapping for adult-plant resistance to stripe rust in a common wheat RIL population derived from Chuanmai 32/ Chuanyu 12. J. Integr. Agri. 11 (11), 17751782. Liu, F., Gupta, S., Zhang, X., Jones, M., Loughman, R., Lance, R., et al., 2011. PCR markers for selection of adult plant leaf rust resistance in barley (Puccinia hordei L.). Mol. Breed. 28, 657666. Liu, G., Jia, Y., Correa-Victoria, F.J., Prado, G.A., Yeater, K.M., McClung, A., et al., 2009. Mapping quantitative trait loci responsible for resistance to sheath blight in rice. Phytopathology 99 (9), 10781084. Liu, G., Jia, Y., McClung, A., Oard, J.H., Lee, F.N., Correll, J.C., 2013. Confirming QTLs and finding additional loci responsible for resistance to rice sheath blight disease. Plant Dis. 97 (1), 113117.

References

211

Liu, Z., Chao, S., Faris, J.D., Edwards, M.C., Friesen, T.L., 2012. QTL mapping reveals effector-triggered susceptibility underlying the barley-Pyrenophora teres f. teres interaction. Am. Phytopathol. Soc. Annual Meeting, 48 August 2012, Providence, Rhode Island, USA. Lu, X.W., Brewbaker, J.L., 1999. Molecular mapping of QTLs conferring resistance to Sphacelotheca reiliana (Ku¨hn) Clint. Maize Genet. Coop. News Lett. 73, 36. Lyngkjaer, M.F., Newton, A.C., Atzema, J.L., Baker, S.J., 2000. The barley mlo-gene: an important powdery mildew resistance source. Agron 20, 745756. Manninen, O., Kalendar, R., Robinson, J., Schulman, A.H., 2000. Application of BARE-1 retrotransposon markers to the mapping of a major resistance gene for net blotch in barley. Mol. Gen. Genet. 264, 325334. Marcel, T., Varshney, R., Barbieri, M., Jafary, H., de Kock, M., Graner, A., et al., 2007. A high density consensus map of barley to compare the distribution of QTLs for partial resistance to Puccinia hordei and of defence gene homologues. Theor. Appl. Genet. 114, 487500. ˇ ˇ Matiasch, L., Buerstmayr, M., Herzog, K., Kraic, J., Sudyov´ a, V., Slikov´ a, S., et al., 2011. QTL mapping of adult plant leaf rust and stripe rust resistance derived from the Austrian winter wheat cultivar Capo. Lehrund Forschungszentrum fu¨r Landwirtschaft Raumberg-Gumpenstein. Mauricio, U., Robert, H., Philip, R., Steven, W., Robert, N., Davis, R., 2013. Inheritance and QTL mapping of Fusarium wilt race 4 resistance in cotton. Theor. Appl. Genet. 126 (5), 14051418. McIntosh, R.A., Baker, E.P., 1968. A linkage map for chromosome 2. In: Finlay, K.W., Shepard, K.W. (Eds.), Third International Wheat Genetics Symposium. Butterworth, Sydney, pp. 305308. McIntosh, R.A., Wellings, C.R., Park, R.F., 1995. Wheat rusts: an atlas of resistance genes. Plant Dis. 77, 11031106. Mehmet Cakir, A.H., Gupta, A.B.S., Chengdao, L.B., Matthew, C.H., Mather, D.E., Gary, A., et al., 2011. Genetic mapping and QTL analysis of disease resistance traits in the barley population Baudin 3 AC Metcalfe. Crop Past. Sci. 62 (2), 152161. Mehrotra, R.S., Aggarwal, A., 2003. Plant Pathology. second ed. Tata McGraw-Hill, New Delhi. Mew, T.W., Vera Cruz, C.M., Medalla, E.S., 1992. Changes in race frequency of Xanthomonas oryzae pv. oryzae in response to the planting of rice cultivars in Philippines. Plant Dis. 76, 10291032. Meyer, A.C., Pataky, J.K., Juvik, J.A., 1991. Partial resistance to northern corn leaf blight and Stewart’s wilt in sweet corn germplasm. Plant Dis. 75, 10941097. Michelmore, R.W., Paran, I., Kesseli, R.V., 1991. Identification of markers linked to disease-resistance genes by bulked segregant analysis: a rapid method to detect markers in specific genomic regions by using segregating populations. Proc. Natl. Acad. Sci. USA 88, 98289832. Ming, R., Brewbaker, J.L., Moon, H.G., Musket, T.A., Holley, R., Pataky, J.K., et al., 1999. Identification of RFLP markers linked to a major gene, sw1, conferring resistance to Stewart’s wilt in maize. Maydica 44, 319323. Negeri, A.T., Coles, N.D., Holland, J.B., Balint-Kurti, P.J., 2011. Mapping QTL controlling southern leaf blight resistance by joint analysis of three related recombinant inbred line populations. Crop Sci. 51, 15711579. Nelson, R.R., 1972. Stabilizing racial populations of plant pathogens by use of resistance genes. J. Environ. Qual. 1 (3), 220227. Pernet, A., Hoisington, D., Franco, J., Isnard, M., Jewell, D., Jiang, C., et al., 1999. Genetic mapping of maize streak virus resistance from the Mascarene source. I. Resistance in line D211 and stability against different virus clones. Theor. Appl. Genet. 99 (34), 524539. Polanda, J.A., Bradburya, P.J., Bucklera, E.S., Nelsona, R.J., 2011. Genome-wide nested association mapping of quantitative resistance to northern leaf blight in maize. Edited by Major M. Goodman. Proc. Natl. Acad. Sci. USA 108 (17).

212


Qi, X., Niks, R.E., Stam, P., Lindhout, P., 1998. Identification of QTLs for partial resistance to leaf rust (Puccinia hordei ) in barley. Theor. Appl. Genet. 96, 12051215. Rahman, F., Khanam, S., Roh, J., Koh, H., 2011. Mapping of QTLs involved in resistance to Rice Blast (Magnaporthe grisea) using Oryza minuta Introgression Lines. Czech. J. Genet. Plant Breed. 47 (3), 8594. Ramsay, L., Comadran, J., Druka, A., Marshall, D.F., Thomas, W.T.B., Macaulay, M., et al., 2011. Intermedium C, a modifier of lateral spikelet fertility in barley, is an ortholog of the maize domestication gene Teosinte branched 1. Nat. Genet. 43, 169172. Reddy, B.P.N., Deshmukh, R.K., Gupta, B., Deshmukh, N.K., Bhaganagare, G., Shivraj, S.M., et al., 2008. Identification of candidate genes for bacterial leaf blight resistance in rice by integration of genetic QTL map with the physical map. Asian J. Biol. Sci. 3, 2429. Ren, Y., He, Z., Li, J., Lillemo, M., Wu, L., Bai, B., et al., 2012a. QTL mapping of adult-plant resistance to stripe rust in a population derived from common wheat cultivars Naxos and Shanghai 3/Catbird. Theor. Appl. Genet. 6 (125), 12111221. Ren, Y., Li, Z., He, Z., Wu, L., Bai, B., Lan, C., et al., 2012b. QTL mapping of adult-plant resistances to stripe rust and leaf rust in Chinese wheat cultivar Bainong 64. Theor. Appl. Genet. 6 (125), 12531262. Reszka, E., Song, Q., Arseniuk, E., Cregan, P.B., Ueng, P.P., 2007. The QTL controlling partial resistance to stagonospora nodorum blotch disease in winter Triticale bogo. Plant Pathol. Bull. 16, 161167. Reynolds, M.P., Ortiz, R., 2010. Adapting crops to climate change: a summary. In: Reynolds, M.P. (Ed.), Climate Change and Crop Production. CABI Publishers, UK, Wallingford, Oxfordshire, pp. 18. Rieseberg, L.H., Widmer, A., Arntz, A.M., Burke, J.M., 2003. The genetic architecture necessary for transgressive segregation is common in both natural and domesticated populations. Philos. Trans. R. Soc. Lond. B. Biol. Sci. 358, 11411147. Rowland, G.C., Kerber, E.R., 1974. Telocentric mapping in hexaploid wheat of genes for leaf rust resistance and other characters derived from Aegilops squarossa. Can. J. Genet. Cytol. 16, 137144. Schweizer, P., Stein, N., 2011. Large-scale data integration reveals colocalization of gene functional groups with meta-QTL for multiple disease resistance in barley. Mol. Plant Microbe Inter. 24 (12), 14921501. Sharma, O., Bambawale, O., 2008. Integrated management of key diseases of cotton and rice. In: Ciancio, A., Mukerji, K.G. (Eds.), Integrated Management of Diseases Caused by Fungi, Phytoplasm and Bacteria. Springer, Dordrecht, pp. 271302. Shin, J.W., Yun, S.C., 2010. CO2 and temperature effects on the incidence of four major chili pepper diseases. Plant Pathol. J. 26 (2), 178184. Shtaya, M.J.Y., Marcel, T.C., Sillero, J.C., Niks, R.E., Rubiales, D., 2006. Identification of QTLs for powdery mildew and scald resistance in barley. Euphytica 151, 421429. Silvar, C., Dhif, H., Igartua, E., Kopahnke, D., Gracia, M.P., Lasa, J.M., et al., 2010. Identification of quantitative trait loci for resistance to powdery mildew in a spanish barley landrace. Mol. Breed. 25, 581592. Singh, A., Pandey, M.P., Singh, A.K., Knox, R.E., Ammar, K., Clarke, J.M., et al., 2012a. Identification and mapping of leaf, stem and stripe rust resistance QTL and their interactions in durum wheat. Mol. Breed. 31, 405418. Singh, A., Singh, V.K., Singh, S.P., Pandian, R.T.P., Ellur, R.K., Singh, D., et al., 2012b. Molecular breeding for the development of multiple disease resistance in Basmati rice. AoB Plants pls029, 2012. Singh, A., Knox, R.E., DePauw, R.M., Singh, A.K., Cuthbert, R.D., Campbell, H.L., et al., 2013. Identification and mapping in spring wheat of genetic factors controlling stem rust resistance and the study of their epistatic interactions across multiple environments. Theor. Appl. Genet. 126 (8), 19511964. Singh, R.P., Huerta-Espino, J., Pfeiffer, W., Figueroa-Lo´pez, P., 2004. Occurrence and impact of a new leaf rust race on durum wheat in northwestern Mexico from 2001 to 2003. Plant Dis. 88, 703708.

References

213

Singh, S., Sharma, I., Sehgal, S.K., Bains, N.S., Guo, Z., Nelson, J.C., et al., 2007. Molecular mapping of QTLs for Karnal bunt resistance in two recombinant inbred populations of bread wheat. Theor. Appl. Genet. 116 (1), 147154. Singh, S., Bockus, W., Sharma, I., Bowden, R.L., 2008. A novel source of resistance in wheat to Pyrenophora tritici-repentis race 1. Plant Dis. 92, 9195. Singh, S., Hernandez, M.V., Crossa, J., Singh, P.K., Bains, N.S., et al., 2012. Multi-trait and multienvironment QTL analyses for resistance to wheat diseases. PLoS ONE 7 (6), e38008. Singh, S., Singh, R.P., Bhavani, S., Huerta-Espino, J., Eugenio, L.V.E., 2013. QTL mapping of slow-rusting, adult plant resistance to race Ug99 of stem rust fungus in PBW343/Muu RIL population. Theor. Appl. Genet. 126 (5), 13671375. Soliman, A.S., Heyne, E.G., Johnston, C.O., 1964. Genetic analysis for leaf rust resistance in the eight differential varieties of wheat. Crop Sci. 4, 246248. Spies, A., Korzun, V., Bayles, R., Rajaraman, J., Himmelbach, A., Hedley, P.E., et al., 2012. Allele mining in barley genetic resources reveals genes of race-non-specific powdery mildew resistance. Plant Sci. 2, 113. Starling, T.M., Roane, C.W., Camper, H.M., 1984. Registration of massey wheat. Crop Sci. 24, 772774. Steffenson, B.J., Smith, K.P., 2006. Breeding barley for multiple disease resistance in the upper Midwest region of the USA. Czech. J. Genet. Plant Breed. 42, 7985. Tajinder, G., Brian, R., Graham, S., 2012. Mapping quantitative trait loci associated with spot blotch and net blotch resistance in a doubled-haploid barley population. Mol. Breed. 30 (1), 267279. Tang, D., Wu, W., Li, W., Lu, H., Worland, A.J., 2000. Mapping of QTLs conferring resistance to bacterial leaf streak in rice. Theor. Appl. Genet. 101, 286291. Teturova, K., Repkova, J., Lızal1, P., Dreiseitl, A., 2010. Mapping of powdery mildew resistance genes in a newly determined accession of Hordeum vulgare ssp. Spontaneum. Ann. Appl. Biol. 156 (2), 157165. Tucker, D.M., Griffey, C.A., Liu, S., Brown-Guedira, G., Marshall, D.S., Saghai Maroof, M.A., 2006. Confirmation of three Quantitative Trait Loci conferring adult plant resistance to powdery mildew in two winter wheat populations. Euphytica 155, 113. Ulloa, M., Wang, C., Roberts, P.A., 2010. Gene action analysis by inheritance and Quantitative Trait Loci mapping of resistance to root-knot nematodes in cotton. Plant Breed. 129, 541550. Utami, D.W., Lestari, P., Koerniati, S., 2013. A relative expression of Xa7 gene controlling bacterial leaf blight resistance in Indonesian local rice population (Oryza sativa L.). J. Crop Sci. Biotechnol. 16 (1), 17. Vanderplank, J.E., 1968. Disease Resistance in Plants. Academic Press, New York. Varshney, R., Marcel, T., Ramsay, L., Russell, J., Ro¨der, M., Stein, N., et al., 2007. A high density barley microsatellite consensus map with 775 SSR loci. Theor. Appl. Genet. 114, 10911103. Veiga, A.D., Pinho, R.G.V., Resende, L.V., 2012. Quantitative Trait Loci associated with resistance to gray leaf spot and grain yield in corn. Cieˆnc. Agrotec. 36 (1), 3138. Wang, C., Matthews, W.C., Roberts, P.A., 2006. Phenotypic expression of rkn1-mediated Meloidogyne incognita resistance in Gossypium hirsutum populations. J. Nematol. 38, 250257. Wang, C., Ulloa, M., Roberts, P.A., 2008a. A transgressive segregation factor (RKN2) in Gossypium barbadense for nematode resistance clusters with gene rkn1 in G. hirsutum. Mol. Genet. Genomics 279, 4152. Wang, H., Lin, Z., Zhang, X.L., Chen, W., Guo, X.P., Nie, Y.C., et al., 2008b. Mapping and QTL analysis of verticillium wilt resistance genes in cotton. J. Integr. Plant Biol. 50 (2), 174182. Wang, M., Yana, J., Zhaob, J., Songb, W., Zhanga, X., Xiaoa, Y., et al., 2012. Genome-wide association study (GWAS) of resistance to head smut in maize. Afr. J. Biotechnol. 7 (14), 25732577. Wanlayaporn, K., Authrapun, J., Vanavichit, A., Tragoonrung, S., 2013. QTL mapping for partial resistance to southern corn rust using RILs of tropical sweet corn. Am. J. Plant Sci. 4, 878889.

214


Wei, F., Gobelman-Werner, K., Morroll, S.M., Kurth, J., Mao, L., Wing, R., et al., 1999. The Mla (powdery mildew) resistance cluster is associated with three NBS-LRR gene families and suppressed recombination within a 240-kb DNA interval on chromosome 5S (1HS) of barley. Genetics 153, 19291948. Wen, N., Chu, Z., Wang, S., 2003. Three types of defence-response genes are involved in resistance to bacterial blight and fungal blast disease in rice. Mol. Genet. Genomics 269, 331339. Xiao-lin, Y., Hua-xiong, Q.I., De-suo, Y.I.N., 2012. Mapping QTLs for rice blast resistance in DH line derived from muwanggu and E’wan8. Acta Phytopathol. Sin. 42 (6), 600607. Xu, Q., Yuan, X., Yu, H., Wang, Y., Tang, S., Wei, X., 2011. Mapping Quantitative Trait Loci for sheath blight resistance in rice using double haploid population. Plant Breed. 130, 404406. Xu, X., Chen, H., Fujimura, T., Kawasaki, S.T., 2008. Fine mapping of a strong QTL of field resistance against rice blast Pikahei-1(t) from utilizing a novel resistance evaluation system in the greenhouse. Theor. Appl. Genet. 6, 9971008. Xue, F., Ji, W.Q., Wang, C.Y., Zhang, H., Yang, B., 2012. High-density mapping and marker development for the powdery mildew resistance gene PmAS846 derived from wild emmer wheat (Triticum turgidum var. dicoccoides). Theor. Appl. Genet. 124, 15491560. Yán˜ez-Lo´pez, R.I., Torres-Pacheco, R.G., Guevara-González, M.I., Hernández-Zul, J.A., Quijano-Carranza, Rico-Garcıá E, 2012. The effect of climate change on plant diseases. Af. J. Biotechnol. 11 (10), 24172428. Young, N.D., 1996. QTL mapping and quantitative disease resistance in plants. Annu. Rev. Phytopathol. 34, 479501. Yu, L.X., Lorenz, A., Rutkoski, J., Singh, R.P., Bhavani, S., Huerta-Espino, J., et al., 2011. Association mapping and genegene interaction for stem rust resistance in CIMMYT spring wheat germplasm. Theor. Appl. Genet. 123, 12571268. Yu, L.X., Morgounov, A., Wanyera, R., Keser, M., Singh, S.K., Sorrells, M., 2012. Identification of Ug99 stem rust resistance loci in winter wheat germplasm using genome-wide association analysis. Theor. Appl. Genet. 125, 749758. Zhang, H., Guan, H., Li, J., Zhu, J., Xie, C., Zhou, Y., et al., 2010. Genetic and comparative genomics mapping reveals that a powdery mildew resistance gene Ml3D232 originating from wild emmer co-segregates with an NBS-LRR analog in common wheat (Triticum aestivum L.). Theor. Appl. Genet. 121, 16131621. Zhang, X., Han, D., Zeng, Q., Duan, Y., Yuan, F., et al., 2013. Fine mapping of wheat stripe rust resistance gene Yr26 based on collinearity of wheat with Brachypodium distachyon and rice. PLoS ONE 8 (3), e57885. Zhang, Y., Xu, L., Fan, X., Tan, J., Chen, W., Xu, M., 2012. QTL mapping of resistance to gray leaf spot in maize. Theor. Appl. Genet. 125 (8), 17971808. Zhou, H., Steffenson, B., 2013. Genome-wide association mapping reveals genetic architecture of durable spot blotch resistance in US barley breeding germplasm. Mol. Breed. 32 (1), 139154. Zwonitzer, J., Coles, N.D., Krakowsky, M.D., Arellano, C., Holland, J.B., McMullen, M.D., et al., 2010. Mapping resistance quantitative trait loci for three foliar diseases in a maize recombinant inbred line population—evidence for multiple disease resistance. Phytopathology 100, 7279.

CHAPTER

10

Plant Responses to Metal Stress: The Emerging Role of Plant Growth Hormones in Toxicity Alleviation

Savita Gangwar, Vijay Pratap Singh, Durgesh Kumar Tripathi, Devendra Kumar Chauhan, Sheo Mohan Prasad and Jagat Narayan Maurya

10.1 Introduction Heavy metals are natural constituents of the Earth’s crust. However, due to human activities and industrial waste input, heavy metal contamination of soil and water resources has become a concern of scientific interest (Chen et al., 2010a,b; Elbaz et al., 2010; Singh and Prasad, 2011; Gill et al., 2013). The increased addition of heavy metal to soil and water has resulted in the widespread occurrence of metal contamination in ecosystems (Elbaz et al., 2010; Basile et al., 2012; Temmerman et al., 2012; Yan and Lo, 2013). Heavy metals are not biodegradable and persist in the environment indefinitely (Singh and Prasad, 2011). In developing countries, untreated wastewater is commonly used for irrigation of agricultural land (Singh and Prasad, 2011). Long-term use of wastewater for irrigation results in the accumulation of heavy metals in soils and thus changes the quality of the soil (Dai et al., 2006; Singh and Agrawal, 2010). Heavy metals can enter the food chain as a result of their uptake by plants. Thus, when in the soil they not only reduce plant growth but also pose risks to the health of humans and animals (Sharma et al., 2008; Singh et al., 2010). Among the various heavy metals, some are essential for plant growth and development; however, at elevated concentrations they adversely affect the physiology and biochemistry of plants (Gangwar et al., 2010; Kalinowska and Pawlik-Skowrońska, 2010; Chou et al., 2011; Gangwar et al., 2011a,b; Thounaojam et al., 2012; Li et al., 2013). Previous studies have shown that heavy metal causes a significant decrease in growth and biomass accumulation (Chen et al., 2010a,b; Dho et al., 2010; Singh et al., 2011; Ali et al., 2013). Excessive concentration of heavy metals is known to cause deleterious effects on many physiological processes of plants such as photosynthesis, mineral nutrition, and the relationship with water (Rodriguez et al., 2012; Ali et al., 2013; Li et al., 2013). In addition to the direct deleterious impact of heavy metals on plants, they adversely affect plants indirectly by producing an excess reactive oxygen species (ROS) (Chen et al., 2010a,b; Elbaz et al., 2010; Vanhoudt et al., 2010; Thounaojam et al., 2012; Li et al., 2013). Thus, heavy metals cause adverse effects on flora from the molecular to the whole plant level. Therefore, investigation of heavy metals’ toxicity remains an area of scientific interest so that their mechanisms can be better understood, as well as minimize health hazards by regulating their entry into crop plants. P. Ahmad (Ed): Emerging Technologies and Management of Crop Stress Tolerance, Volume 2. DOI: http://dx.doi.org/10.1016/B978-0-12-800875-1.00010-7 © 2014 Elsevier Inc. All rights reserved.

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CHAPTER 10 Plant Responses to Metal Stress

In recent years, much attention has been given to developing strategies to alleviate the adverse effects of metal toxicity on crops in order to fulfill the food demand of an increasing population. Chemical application and agronomical crop management practices have been used to alleviate metal toxicity with some success. In the past decade, exogenous application of plant hormones has emerged as an alternative strategy to induce plants’ capability to successfully face the detrimental situation caused by metal toxicity. Plant hormones are a group of chemical messengers that regulate plant growth and development (Matsuoka, 2003; Pasternak et al., 2005; Perilli et al., 2010; Peto et al., 2011; Claeys et al., 2012). Studies have shown that exogenous application of hormones provides protection to plants against abiotic stress and increases crop yield (Quint and Gray, 2006; Koprivova et al., 2008; Peto et al., 2011; Rubio-Wilhelmi et al., 2011; Claeys et al., 2012; Elobeid et al., 2012; Nam et al., 2012; Zhu et al., 2012; Krishnamurthy and Rathinasabapathi, 2013; Srivastava et al., 2013). Taking into account the potential significance of plant hormones in alleviating stress, this chapter contains an overview of the impact of heavy metals on plants, together with their related defense mechanisms and the role of hormones with reference to auxins, gibberellic acids (GAs), and cytokinins (CKs) to alleviate metal toxicity.

10.2 Sources of heavy metal pollution Sources of heavy metals in the environment can be both natural and anthropogenic such as geogenic/natural process, industrial effluents, refuse burning, organic wastes, transport, and power generation (Table 10.1). Industrial effluents and drainage water carry a high amount of metallic pollution into the hydrosphere. Heavy metals can be carried to places far away from their source by the wind, depending on whether they are in gaseous form or are particulates that ultimately wash out of the air as rain that goes into the land and water bodies (Agarwal, 2009). Disposal of municipal waste is considered one of the major sources of heavy metal pollution to the soil (Singh and Prasad, 2011). Metal-rich materials’ disposal results in the formation of metalliferous mine spoils and metalliferous tailings that cause heavy metal contamination. Further, some agricultural practices, such as excess use of pesticides and fertilizers, have contributed to increased concentrations of heavy metal in the soil (McBride, 2003; Lone et al., 2008; Singh and Prasad, 2011).

10.3 Transport and distribution of metal in plants Uptake and translocation of heavy metals may vary considerably and depend on plant species and type of metals. Metals, such as iron (Fe), manganese (Mn), nickel (Ni), zinc (Zn), and copper (Cu), are essential and necessary cofactors for many enzymatic reactions (Fox and Guerinot, 1998); however, excess amounts of them produce cytotoxic effects. In contrast to the essential elements, heavy metals (e.g., Cr, As, Cd, Pb, Hg) with no biological function are harmful to plants even at a very low concentration. Therefore, plants have acquired specialized mechanisms to sense, transport, and maintain essential metals within physiological limits and to control excessive accumulation of nonessential metals (Mendoza-Co´zatl et al., 2011). It has been shown that metal transporters are

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Table 10.1 Sources of Heavy Metal Pollution Metal

Source(s)

Chromium (Cr) Lead (Pb)

Mining, industrial coolants, chromium salts manufacturing, leather tanning Lead acid batteries, paints, e-waste, smelting operations, coal-based thermal power plants, ceramics, bangle industry Chlor-alkali plants, thermal power plants, fluorescent lamps, hospital waste (damaged thermometers, barometers, sphygmomanometers), electrical appliances, etc. Geogenic/natural processes, smelting operations, thermal power plants, fuel burning Mining, electroplating, smelting operations Spent catalyst, sulfuric acid plant Smelting operations, thermal power plants, battery industry Zinc smelting, waste batteries, e-waste, paint sludge, incinerations and fuel combustion Spent catalyst Smelting, electroplating

Mercury (Hg) Arsenic (As) Copper (Cu) Vanadium (Va) Nickel (Ni) Cadmium (Cd) Molybdenum (Mo) Zinc (Zn)

Source: Gautam SP, CPCB, New Delhi.

essential to maintaining intracellular metal homeostasis (Nelson, 1999; Pilon et al., 2009). The transporter proteins mediate metal uptake in root cells and metal transfer between cells and organs. Metal transporters are also involved in metal detoxification by mediating the transport of metals from the cytosol to the vacuolar compartment (Salt and Wagner, 1993; Ortiz et al., 1995; Salt and Rauser, 1995; Rea et al., 1998). Thus, metal concentrations within cells are carefully controlled, so plants and other organisms possess a range of potential mechanisms for metal ion homeostasis and tolerance, including membrane transport processes (Clemens, 2001; Hall, 2002). Studies have demonstrated that membrane transport systems are likely to play a key role in metal transport. Previously, very little was known about the molecular mechanisms of metal transport across cell membranes; however, within the last 10 years rapid progress has been made using molecular and genetic approaches (Pilon et al., 2009; Puig and Penãrrubia, 2009). Studies have shown that uptake and distribution of Cd and As in plants is a dynamic process that is driven by root plasma membrane transporters (Verbruggen et al., 2009; Ye et al., 2010). Other studies demonstrated that the influx of arsenate is driven by phosphate transporters, while arsenite is taken up by aquaporin nodulin 26-like intrinsic proteins (Bienert et al., 2008; Verbruggen et al., 2009). Hg, which is a class B metal, is thought to enter the cell through ionic channels competing with other heavy metals (e.g., cadmium) or essential metals such as zinc, copper, and iron (Nagajyoti et al., 2010). The uptake of Cd, which is highly toxic and a nonessential heavy metal, occurs via Fe21, Ca21, Zn21, and Mn21 transporters (Clemens, 2006). The most-studied transporter is the ZIP IRT1, which loads Cd into the xylem by the heavy metal ATPases: HMA2 and HMA4 (Mendoza-Co´zatl et al., 2011). Not long ago, it was demonstrated that Al31, which is believed to be highly toxic to cells, even at a lower concentration, is transported through the Nramp aluminum transporter 1 (Nrat1) (Xia et al., 2010). Further, this study found that Nrat1 is localized on plasma membranes of all cells of

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the root tip except the epidermal cells. Studies revealed that uptake and transport of Zn, Fe, and Mn are also mediated by the ZIP family of transporters (Pilon et al., 2009; Puig and Penãrrubia, 2009). In addition, it has been demonstrated that P-type ATPase AtECA3 is expressed in root tip and that the vasculature can transport both Mn and Ca into an endomembrane system, as shown by complementary studies in yeast (Li et al., 2008; Mills et al., 2008). Talke et al. (2006) noted that ZIP transporters involved in the uptake of Zn are up-regulated by Zn and Fe deficiency in Arabidopsis thaliana. In the case of Cu, it has been shown that it enters into plants through the copper transporter (COPT) protein family of transporters (Sancenon et al., 2003). Studies revealed that COPT transporters belong to an evolutionary conserved family, known as the copper transporter (CTR), which have three transmembrane domains and are characterized by a high methionine content that is believed to play a role in Cu translocation (Pilon et al., 2006). It is evident that metal uptake and homeostasis require coordination of several processes in order to regulate uptake and carry out long-distance transport and distribution of metals to different parts of plants. For essential metals, understanding the complex processes of metal uptake and transport is necessary to enhance metal acquisition under metal-limiting conditions in order to increase productivity and to check their accumulation under excess metal conditions. However, in the case of nonessential metals, understanding and identifying their transporters may further help to enhance the metal-tolerance capacity of plants and to reduce their accumulation in crop plants.

10.4 Heavy metal toxicity in plants Heavy metal (e.g., Cd, Hg, Pb, Cr, As, Zn, Cu, Ni) toxicity is manifested in many ways when plants accumulate them in high concentrations (Hossain et al., 2012). It is considered one of the major abiotic stresses leading to the reduced yield of plants.

10.4.1 Direct effects Metals accumulated in plant tissues can cause toxic effects, especially when translocated to aboveground tissues. The effects can be measured at both the biochemical and cellular level, but most studies have focused on growth as the response to the toxicant. Heavy metals that enter plants’ system may lead to various changes in physiological processes and thus a decline in growth (Singh and Prasad, 2011). One study showed that 100 μM of Cu led to a decline in root and shoot fresh mass of rice seedlings by 44% and 35%, respectively (Thounaojam et al., 2012). Li et al. (2013) observed that Cr toxicity led to a significant decline in the growth of wheat seedlings by arresting the photosynthetic process. Such inhibition of the photosynthetic process due to metal stress had occurred as a result of altered chloroplast morphology, gas exchange, the net CO2 assimilation rate, and Rubisco activity. Further, the study showed that Cr stress led to a decline in biomass accumulation in barley plants by causing ultrastructure disorders in leaves—for example, uneven thickening and swelling of the chloroplast, an increased amount of plastoglobuli, and a disintegrated thylakoid membrane. This resulted in a decline in net stomatal conductance (Gs), cellular CO2 concentration (Ci), transpiration rate (Tr), photochemical efficiency (Fv/Fm), and the net photosynthetic rate (Pn) (Ali et al., 2013).

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Metal-induced toxicity to plants has also been related to DNA fragmentation and microtubule disorganization, which resulted in the arrest of cell division (Dho et al., 2010). Another study showed that Al treatment adversely affected root growth of Zea mays by disturbing Ca21 homeostasis (Garzoń et al., 2011). Studies by Hsu and Kao (2004) and Backor et al. (2007) showed that heavy metals do cause the release of lipids, proteins, and elemental components from thylakoid membranes and thus lead to damage to light-harvesting complexes and photosystems. Heavy metals can replace the Mg atom in chlorophyll, thus a reduction in chlorophyll is generally observed under metal stress (Shakya et al., 2008). High levels of Hg are also reported to be extremely phytotoxic to cells and can cause visible injuries and physiological disorders in plants (Zhou et al., 2007). Hg21 can bind to water channel proteins, thus inducing leaf stomata to close and physically obstruct water flow into plants (Zhang and Tyerman, 1999). Further, it has been observed that Hg can interfere with the electron transport systems of chloroplast as well as mitochondrion and thus induce oxidative stress that results in disruption of the cellular metabolism (Cargnelutti et al., 2006; Singh et al., 2012a,b). Arsenic, which is a well-established human carcinogen, also severely affects plant growth and development and its toxicity is very dependent on the concentration, exposure time, and physiological state of plants (Dho et al., 2010). Arsenic is known to interfere with various metabolic processes in the cell, interact with sulfhydryl groups, and replace phosphate from ATP. A study by Shri et al. (2009) demonstrated that AsIII and AsV significantly inhibited seed rice seedlings’ germination and growth. Gusman et al. (2013) reported that As treatment decreased the relative growth rate and photochemical efficiency of lettuce plants, which resulted in decreased growth. Further, it has been reported that As toxicity inhibits the activity of nitrogenase- and nitrogen-metabolizing enzymes— nitrate reductase and nitrite reductase (Porter and Sheridan, 1981; Singh et al., 2009). Studies on different plant species revealed that Cd is also strongly phytotoxic and causes growth inhibition and even plant death (Wu et al., 2007). It has been observed that barley plants grown under Cd (5 μM) stress show growth inhibition, chlorosis, necrosis, and finally death (Chen et al., 2010a,b). Pb has also been reported to cause adverse effects on the morphology, growth, anatomy, and photosynthetic processes of plants (Yadav, 2010; Singh et al., 2011). There are increasing numbers of studies that show that Pb toxicity affects chlorophyll biosynthesis and photosynthesis, membrane integrity, cell ultrastructure, and genomic stability, which results in decreased biomass accumulation in plants (Branquinho et al., 1997; Cenkci et al., 2010; Zheng et al., 2012). High levels of Pb have also been shown to lead to inhibition of enzyme activities, alterations in membrane permeability, disturbances in mineral nutrition, and water imbalance (Sharma and Dubey, 2005). Concentrations of Ni in polluted soil may reach up to 200 to 26,000 mg/kg in comparison to the overall range (101000 mg/kg) found in natural soil (Izosimova, 2005). Excess Ni (0.11 mM) caused a decline in growth of soybean and Pisum sativum L. seedlings by reducing photosynthetic pigments and inhibiting the photosynthetic electron transport chain and 14CO2-fixation (Prasad et al., 2005; Srivastava et al., 2012). Molas (2002) observed that Ni (40 and 85 μM) affects chloroplast structure and chlorophyll content in cabbage. Gabbrielli et al. (1999) demonstrated that Ni toxicity adversely affected Pisum sativum seedlings by altering K uptake and water content. Further, Gajewska and Sklodowska (2008) observed that wheat seedlings treated with Ni (10200 μM) showed a decline in growth due to enhanced Ni accumulation that led to oxidative stress. Moreover, heavy metals may cause disturbances in nutrient homeostasis, which results in altered uptake of essential elements (Fodor, 2002). Gangwar and Singh (2011) reported that Cr(VI) inhibited

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nitrogen-metabolizing enzymes such as nitrate reductase (NR) and nitrite reductase (NiR), in addition to the ammonium-metabolizing enzymes glutamine synthetase (GS) and glutamine-2 oxoglutarate aminotransferase (GOGAT); this resulted in a significant decline in the growth of pea seedlings.

10.4.2 Indirect effects Besides the direct impact of heavy metals on plants, a common consequence of metal toxicity is excessive accumulation of ROS that can cause peroxidation of lipids, oxidation of protein, inactivation of enzymes, DNA damage, and/or interact with other vital constituents of plant cells. Heavy metal toxicity affects biological molecules, for example, when metals bind to the S group and/or block the active site of enzymes. They may cause conformational changes in enzymes, disrupt cellular homeostasis, and cause oxidative damage by generating ROS such as singlet oxygen (1O2), superoxide radical (O2•2), hydrogen peroxide (H2O2), and hydroxyl radical (•OH); this can cause lipid peroxidation, membrane defects, and instability of enzymes in higher plants (Halliwell and Gutteridge, 1989; Hossain et al., 2012). Chloroplast, mitochondrion, and plasma membrane are linked to electron transport and thus generate ROS as by-products (Becana et al., 2000). A variety of abiotic stresses, including drought, salinity, extreme temperatures, high irradiance, UV light, nutrient deficiency, air pollutants, metallic stress, and so on, lead to formation of ROS and result directly or indirectly in molecular damage. Therefore, regulation of ROS is a crucial process to avoid unwanted cellular cytotoxicity and oxidative damage (Halliwell and Gutteridge, 1989). The heavy metals of biological significance have been divided into two groups: redox active and inactive elements (Schu¨tzendu¨bel and Polle, 2002). Redox active elements directly involve redox reactions in cells and result in the formation of ROS such as superoxide radical (O2•2), hydrogen peroxide (H2O2), and hydroxyl radicals (•OH) via the Haber-Weiss and Fenton reactions (Aust et al., 1985; Dietz et al., 1999). Exposure of plants to redox inactive heavy metals also results in formation of ROS by an indirect mechanism such as interruption of electron transport chains (Hossain et al., 2012). It is known that different ROS, including 1O2, O2•2, H2O2, and •OH, occur transiently in aerobic organisms (Pinto et al., 2003). These reactive oxygen species are normal byproducts of the oxidative metabolism and pose a constant threat to all aerobic organisms. Although some of them may function as important signaling molecules that alter gene expression and modulate the activity of specific defense proteins, all ROS can be extremely harmful to organisms at high concentrations. ROS can oxidize lipids, proteins, and nucleic acids often leading to alterations in cell structure and mutagenesis (Halliwell and Gutteridge, 1999). Gajewska and Sklodowska (2010) observed that treatment with Cu, Ni, and Cd significantly increased electrolyte leakage, lipid peroxidation, and protein oxidation in wheat seedlings by enhancing the level of ROS. Further, Maheshwari and Dubey (2009) reported Ni-mediated generation of O2•2 and H2O2 in rice seedlings that causes tissue damage and a reduction in growth. Rare earth elements, such as cerium (Ce), have also been reported to enhance ROS generation in cells. Xu and Chen (2011) reported that treatment of rice seedlings with Ce41 significantly accelerated production of O2•2 and H2O2; subsequently, this damaged the cellular system and resulted into oxidative stress. Cadmium has been shown to cause a decline in the growth of barley seedlings by enhancing generation of ROS that resulted in enhancement of lipid peroxidation (Chen et al., 2010a,b). Thounaojam et al. (2012) noticed that Cu significantly decreased the growth of rice seedlings by enhancing the level of H2O2 and lipid peroxidation. Wang et al. (2010) reported that higher Pb

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concentrations (251000 mg/kg) caused growth inhibition of Vicia faba seedlings by enhancing oxidative stress and damage. Further, these researchers observed that O2•2 and lipid peroxidation increased with the rise of available Pb in soils, and Pb contents in roots displayed a “J”-shaped doseresponse curve, whereas H2O2 showed a biphasic doseresponse curve (a consecutive J-shaped and inverted “U”-shaped curve). Requejo and Tena (2005) demonstrated the effect of arsenic toxicity on Zea mays L. root proteome and concluded that the induction of oxidative stress is the main process underlying arsenic toxicity in plants. Similarly, Semane et al. (2010) reported that metal (Cd) stress caused toxicity in Arabidopsis thaliana through proteomic changes that resulted in oxidative stress and damage. The same as other toxic metals, Hg (0.26 μM) has been reported to decrease the growth of Nostoc muscorum by inhibiting chlorophyll synthesis, photosynthetic electron transport chains, and 14CO2fixation by enhancing generation of ROS and causing damage to lipids (Singh et al., 2012a,b). Zinc (0.53 mM) has been reported to enhance generation of ROS and lipid peroxidation that have been correlated with wheat seedlings’ reduced yield (Li et al., 2013). Gangwar et al. (2011b) demonstrated that Mn (50250 μM) significantly decreased the growth of pea seedlings by enhancing H2O2 and lipid peroxidation. It has been shown that production of ROS during environmental stresses (e.g., metal toxicity) is one of the main causes for decreases in productivity (Halliwell and Gutteridge, 1989; Asada, 1994; Pinto et al., 2003; Prasad and Zeeshan, 2005). Therefore, understanding the connections between an organism’s initial responses and the downstream events that constitute successful adjustment to its altered environment (metal contamination), which causes oxidative stress, is one of the next grand challenges of plant biology.

10.5 Plant defense systems Life originally began on Earth under a reducing atmosphere (Dietrich et al., 2006; Latifi et al., 2009). The atmosphere became oxidant as oxygen-producing photosynthesis evolved after the proliferation of cyanobacteria between 3.2 and 2.4 billion years ago (Brocks et al., 1999). Oxygen accumulation allowed the development of aerobic organisms that used oxygen as a powerful electron acceptor. At the same time, these organisms had (i.e., through the evolvement of an antioxidant system) to cope with the damaging effects of oxygen (i.e., the reactive derivative of oxygen—that is, ROS) on the metabolic networks that had originally evolved in an anoxic environment (Latifi et al., 2009). This is because ROS are unavoidably generated as intermediates of oxygen reduction, or by its energization. ROS can be very toxic at higher concentrations, which damage lipids, proteins, and nucleic acids, and thus cause oxidative stress in cells. Plants, because they are not mobile, cannot escape environmental stresses. The ability of higher plants to scavenge the toxic effects of ROS seems to be a very important determinant of their tolerance to stresses. To scavenge ROS and avoid oxidative damage, plants possess antioxidative enzymes (Kanazawa et al., 2000), which are critical for maintaining the optimum health of plant cells. However, when the balance between an organism’s ROS and its antioxidant capacity is disrupted, oxidative stress occurs. An antioxidant system is comprised of two types of antioxidants (i.e., enzymatic and nonenzymatic). There are several antioxidant enzymes—superoxide dismutase (SOD), catalase (CAT), ascorbate peroxidase (APX), dehydroascorbate reductase (DHAR), and

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O2•– SOD H2O2 NADPH

AA

Photosynthetic process

CAT

MDHAR

APX

H2O+O2

and hexose

NADP+

MDHA Disproportionation DHA GSH DHAR AA

GSSG

Monophosphate shunt

NADPH GR

Photosynthetic process and hexose

NADP+ Monophosphate shunt

FIGURE 10.1 Schematic drawing showing role of antioxidants in scavenging of reactive oxygen species.

glutathione reductase (GR)—and nonenzymatic antioxidants such as ascorbate and glutathione; all these are effectively involved in the scavenging of ROS in plants (Chen et al., 2010a,b; Elbaz et al., 2010; Gondim et al., 2012; Thounaojam et al., 2012). These antioxidants directly or indirectly scavenge various ROS and protect organisms from oxidative stress. The importance of enzymatic and nonenzymatic antioxidants in preventing oxidative stress in plants is based on the fact that the level of one or more antioxidants increases under stress; this is generally related to increased stress tolerance (Figure 10.1).

10.5.1 Enzymatic antioxidants 10.5.1.1 Superoxide dismutase (EC 1.15.1.1; O2•2 1 O2•2 1 2H12H2O2 1 O2)

Superoxide radicals (O2•2) produced in the photosynthetic and respiratory chain are very reactive and, therefore, dismutate into comparatively less damaging ROS (i.e., H2O2 by enzyme SOD) (Karpinska et al., 2001). Thus, superoxide dismutase (SOD) is considered to be a first line of defense against ROS. The SODs are metalloenzymes that can be divided into three classes: (1) Mn-SODs are found in the cytosol, thylakoid membrane, and mitochondrial lumen. (2) Fe-SODs are found in the cytosol and in the chloroplast stroma of photosynthetic plant cells. They are not usually found in eukaryotes other than plants. (3) Cu/ZnSODs are present only in eukaryotes and may be found in the cytosol, chloroplast, and mitochondrial intermembrane spaces (Alscher et al., 2002). Despite varied evolutionary histories, the catalytic activities of the different types of SODs have been shown to be similar. One class of SOD can complement the deletion mutations of other classes of SODs within and between species, families, and even kingdoms (Purdy and Park, 1994; Takeshima et al., 1994; Myouga et al., 2008). The existence of multiple SODs may result from the fact that the cells of eukaryotes are divided into compartments by internal membranes. Because O2•2 radicals are negatively charged and cannot cross the plasma membrane, they are effectively


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trapped within the compartments where they are generated. Therefore, this may have been used for the evolution of several types of SODs in compartmentalized cells. In many cases, it appears that a SOD is a key enzyme for providing protection against oxidative stress. It plays a determinant role in protection against the toxic effects of oxidative stress by scavenging O2•2 (Myouga et al., 2008). Studies revealed that SOD activity shows differential responses against metal stress in plants. Chen et al. (2010a,b) observed that SOD activity increased in a Cdresistant variety of barley, while it was substantially decreased in a sensitive variety. Further, these researchers noticed that under Cd stress Cu/ZnSOD increased while MnSOD decreased in both varieties. Agrawal and Mishra (2009) also noticed the enhanced activity of SOD in Pisum sativum L. seedlings under Cd stress. Gangwar et al. (2011b) reported that Mn stress significantly enhanced SOD activity in pea seedlings. Cr(VI) at 20 μM enhanced SOD activity in pea seedlings, while at 200 μM a reduction in SOD activity was recorded (Dixit et al., 2002). In addition, it has been observed that SOD activity was enhanced at Zn deficient (0 ppm) and Zn excess (50 ppm) levels in bean seedlings; this increased activity was related to the enhanced production of H2O2. However, Li et al. (2013) demonstrated that SOD activity remains unchanged in Zn-treated wheat seedlings. In Vicia faba, Pb (02000 mg/kg) has been shown to enhance SOD activity. Shri et al. (2009) observed that As stress up-regulates activity and the isoenzymes of SOD in rice seedlings. Similarly, Cu, Ni, and Hg have been reported to induce SOD activity (Prasad et al., 2005; Singh et al., 2012a,b). Contrary to this, a decrease in SOD activity has also been reported by several researchers. Sinha et al. (2005) noticed a decrease in SOD activity in roots of P. stratiotes at 48 h of Cr(VI) exposure. Zhang et al. (2007) also observed that heavy metal stress decreased SOD activity in seedlings of Kandelia candel and Bruguiera gymnorrhiza. Further, it has been demonstrated that Pb and Cd considerably redued SOD activity in Amaranthus (Bhattacharjee, 1997). Under metal stress, enhancement in SOD activity generally is related to proper scavenging of O2•2 and/or enhanced O2•2 production, while declines in SOD activity is a result of the lower production of O2•2. In transgenic studies, the importance of SOD for increasing metal tolerance has also been studied. Basu et al. (2001) demonstrated that transgenic Brassica plants overexpressing mitochondrial MnSOD showed increased resistance to Al toxicity. Tseng et al. (2007) observed that introduction of Cu/ZnSOD in the chloroplast of Brassica campestris L. sp. pekinensis cv. tropical pride enhanced tolerance to 400 ppb SO2. Further, this study showed that transgenic plants also accumulate more K, Ca, and Mg than control plants. In tall fescue plants, overexpression of Cu/ZnSOD has been shown to confer oxidative tolerance caused by Cu, Cd, and As (Lee et al., 2007). Mahanty et al. (2012) also reported that overexpression of Cu/ZnSOD enhanced tolerance against oxidative stress.

10.5.1.2 Catalase (EC 1.11.1.6; 2H2O22O2 1 2H2O) Catalase (CAT) is a heme-containing enzyme that is one of the most potent catalysts known (Salin, 1988); it is found abundantly in a cellular compartment called the peroxisome. CAT catalyzes reactions that are crucial to life—for example, the conversion of H2O2, a powerful and potentially harmful oxidizing agent, to water and molecular oxygen. Catalase also uses H2O2 to oxidize toxins including phenols, formic acid, formaldehyde, and alcohol. One study showed that CAT acts as a sink for H2O2 and is indispensible for stress defense in C3 plants because CAT-deficient plants show increased susceptibility to stress (Willekens et al., 1997).

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Further, Gondim et al. (2012) demonstrated that CAT activity plays a key role in the stress acclimation process of maize. Studies also revealed that CAT activity shows a differential response under heavy metal stress. In Vicia faba, increased activity of CAT has been reported under Pb toxicity (Wang et al., 2010). Elbaz et al. (2010) reported that Hg (06 μM) increased activity as well as the transcript level of CAT. In wheat seedlings, Zn (0.53 mM) enhanced CAT activity in leaves while there was a decline of it into roots, showing a differential response (Li et al., 2013). Mallick et al. (2011) observed that As enhanced CAT activity in Zea mays L. (cv Azad kamal) in a dose-dependent manner after three days, while in Zea mays L. (cv Azad uttam) CAT activity decreased at higher concentrations. An increase in CAT activity was noticed with a moderate toxic dose of Cd (100 μM), while a marked decline in CAT activity was observed at highly toxic levels of Cd (500 μM) in rice seedlings (Shah et al., 2001). It has been reported that Cr(VI) significantly stimulated CAT activity in the roots of green gram and the results were correlated with increased protection against Cr toxicity (Shanker et al., 2004). In contrast, Gangwar et al. (2011a) observed that Cr(VI) (50250 μM) decreased CAT activity in pea seedlings. Similarly, Mn has been reported to significantly reduce CAT activity in pea seedlings (Gangwar et al., 2011b). Under Cr and Mn stress, a decline in CAT activity was noted with increased oxidative stress. In Zea mays, 1000 mg/kg of Zn treatment was reported to significantly decrease CAT activity (Cui and Zhao, 2011). In addition, Singh et al. (2007) observed that As (10 and 50 μM) treatment resulted in a significant decline of CAT activity in mung bean. Transgenic studies also revealed that CAT plays an important role in enhancing tolerance against oxidative stress caused by metal stress. Guan et al. (2009) demonstrated that transgenic tobacco plants that overexpress the CAT gene from Brassica juncea (BjCAT3 gene) exhibit normal growth under Cd (100 μM) stress. However, wild-type plants grown under similar treatment with Cd become chlorotic and almost die. It has been demonstrated that CAT-deficient plants become nectrotic under high light conditions, while complementary CAT activity protected plants against high light stress (Willekens et al., 1997). Further studies showed that the presence of the CAT gene (Cat1) is necessary for protecting tobacco plants against stress conditions (Chamnongpol et al., 1996). These studies clearly revealed that the functioning of CAT activity is indispensible for protecting plants against stress.

10.5.1.3 Ascorbate peroxidase (EC 1.11.1.11; AA 1 H2O22DHA 1 2H2O) Ascorbate peroxidase (APX) is also a H2O2-scavenging enzyme and is indispensable for the protection of chloroplasts and other cell constituents from damage by H2O2 and hydroxyl radicals (•OH). Ascorbate peroxidase uses ascorbate (AsA) as its specific electron donor to reduce H2O2 to water with the concomitant generation of monodehydroascorbate (MDHA), a univalent oxidant of ascorbate (AA). Monodehydroascorbate is spontaneously disproportionate to AsA and dehydroascorbate (DHA). APX has been identified in most higher plants and comprises a family of isoenzymes with different characteristics (Shigeoka et al., 2002). The isoenzymes of APX are found in at least four distinct cellular compartments: cytosolic APX (cAPX), thylakoid membrane bound APX (tAPX) in chloroplasts, stromal APX (sAPX), and microbody (including glyoxysome and peroxisome) membrane-bound APX (mAPX) (Yamaguchi et al., 1995; Yoshimura et al., 2000). The various APX isoforms respond differentially to metabolic and environmental signals (Yoshimura et al., 2000).


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Studies demonstrated that APX activity exhibited a differential response under heavy metal stress. In rice seedlings, APX activity is reported to increase progressively in a concentrated and time-dependent manner in both shoots and roots under Cu (50 and 100 μM) stress (Thounaojam et al., 2012). Several other studies noted that heavy metal stress also stimulated APX activity in plants (Elbaz et al., 2010; Vanhoudt et al., 2010; Wang et al., 2010). Wang et al. (2010) demonstrated that Pb stimulated APX activity in Vicia faba and played a crucial role in ROS scavenging when CAT activity declined with Pb stress. In the root and shoot of wheat seedlings, significantly increased activity of APX has also been reported after six days of Zn (0.53 mM) treatment (Li et al., 2013). Under Cd (4 and 40 μM) stress, an increase in APX activity was observed in the root and shoot of pea seedlings; however, higher induction in enzyme activity occurred at 4 μM when compared to a 40 μM concentration of Cd (Dixit et al., 2001). In maize seedlings, an ` lvarez et al., 2006). increased cytosolic activity of APX was noticed under Cd stress (Rellán-A Similarly, Gangwar et al. (2011a,b) reported that Mn and Cr(VI) significantly stimulated APX activity in pea seedlings. Contrary to this, a decline in the activity of APX under heavy metal stress ` lvarez et al. (2006) reported that Hg (30 μM) signifihas been reported by several authors. Rellán-A cantly decreased APX activity due to enhanced protein oxidation. In Alyssum, it has been observed that Cu treatment caused a significant decline in APX activity in comparison to the untreated plants (Schickler and Caspi, 1999). Moreover, Ni (426 μM) has been reported to cause a decrease in APX activity; it decreased by 61% in comparison to the control plants (Boominathan and Doran, 2002). However, studies also showed that heavy metal stress did not bring a change in APX activity (Boˇcová et al., 2012). Transgenic studies also revealed that overexpression of APX genes confers tolerance against multiple stresses. It has been demonstrated that transgenic tobacco plants overexpressing ascorbate peroxidase exhibited enhanced tolerance against oxidative stress (Faize et al., 2011). In transgenic tobacco, overexpression of the Arabidopsis ascorbate peroxidase gene (APX3) has been shown to enhance tolerance against oxidative stress (Wang et al., 1999). Kwon et al. (2002) also demonstrated that overexpression of APX in transgenic tobacco does increase its tolerance to stress. In addition, these researchers showed that overexpression of APX together with Cu/ZnSOD provided greater stress tolerance than their individual overexpression. Further, in Arabidopsis thaliana, expression of APX has been demonstrated to increase Cd tolerance (Chiang et al., 2006).

10.5.1.4 Dehydroascorbate reductase (EC 1.8.5.1; 2GSH 1 DHA2GSSG 1 AA) Dehydroascorbate reductase (DHAR) plays a critical role in the ascorbateglutathione recycling reaction in higher plants. DHAR is located in the chloroplast (Hossain and Asada, 1984) and cytosol (Arrigoni et al., 1981) of higher plants. Dehydroascorbate reductase uses glutathione (GSH) to reduce dehydroascorbate (DHA) and thereby regenerates reduced AsA. Ascorbate, a major antioxidant that serves many functions in plants’ tissues, is oxidized to DHA via successive reversible single-electron transfers with monodehydroascorbate (MDHA) as a free radical intermediate. The univalent oxidation of ascorbate leads to the formation of MDHA that is converted into the divalent oxidation product DHA through spontaneous disproportionation (Ishikawa et al., 1998) because MDHA radicals have a relatively short lifetime. Dehydroascorbate is then reduced to ascorbate by DHAR in a reaction requiring reduced GSH. Moreover, DHAR converts reduced glutathione into the oxidized form of glutathione (GSSG), liberating protons that are incorporated into the recycling reaction of AsA (Washko et al., 1992). Therefore, the expression of DHAR responsible for

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regenerating ascorbate from an oxidized state regulates the cellular AsA redox state, which in turn affects cell responsiveness and tolerance to environmental stress. The same as other antioxidant enzymes, differential response of DHAR has been demonstrated under heavy metal stress. Shanker and Pathmanabhan (2004) observed that Cr(VI) caused a significant increase in DHAR activity in Sorghum bicolor. However, Gangwar et al. (2011a) observed that Cr DHAR activity declined in pea seedlings. Balestrasse et al. (2001) reported that DHAR activity was enhanced in soybean seedlings at a lower concentration of Cd (50 μM), while its activity declined at higher Cd concentrations (100 and 200 μM). Further, Gangwar et al. (2011b) reported enhanced activity of DHAR in pea seedlings under Mn stress. In maize seedlings, however, Ni (250 μM) treatment did not bring a significant change in DHAR activity (Baccouch et al., 2001). Transgenic studies also revealed that overexpression of DHAR activity played an important role in mitigating heavy metal toxicity. It has been demonstrated that overexpression of DHAR, but not MDHAR, confers Al tolerance in transgenic tobacco (Yin et al., 2010). Further, Martret et al. (2011) demonstrated that overexpression of the DHAR gene, together with glutathione reductase and glutathione-S-transferase genes, provides protection against oxidative stress caused by heavy metal, methyl viologen, salt, and cold.

10.5.1.5 Glutathione reductase (EC 1.6.4.2; NADPH 1 GSSG2NADP1 1 2GSH) The ascorbateglutathione cycle plays a very important role in the mitigation of ROS and thus their damaging consequences on macromolecules. Glutathione reductase (GR) is one of the important enzymes of the ascorbateglutathione cycle. It provides a reduced form of glutathione and thus maintains the level of GSH in the plant cell for scavenging of ROS by the other enzymes; however, GSH itself may also scavenge ROS directly. The enzyme GR is a member of the flavoenzyme family that catalyzes the NADPH-dependent reduction of oxidized glutathione into GSH (Rendoń et al., 1995). The simple tripeptide GSH is found in almost all living cells and takes part in numerous biochemical reactions (Noctor et al., 2000). The oxidized form of GSSG is reduced to GSH by the activity of the enzyme GR. The enzyme protein, although synthesized in cytoplasm, can be targeted to both the chloroplast and mitochondria (Mullineaux and Creissen, 1997). In higher plants, GR is involved in defense against oxidative stress, whereas GSH plays an important role within the cell system, which includes participation in the ascorbateglutathione cycle, maintenance of the sulfhydryl groups of cystein in a reduced form, storage of reduced sulfur, and a substrate for glutathione-S-transferase (Noctor et al., 2000). Based on the metal and plant material used, there is an increase and/or a decline in the activity of GR. Laspina et al. (2005) reported that Cd (0.5 mM) enhanced GR activity in sunflower seedlings. Besides this, Dixit et al. (2001) noted that Cd (4 and 40 μM) caused a progressive increase in GR activity in pea seedlings by 76% and 172%, respectively. However, Singh et al. (2008) observed that Cd (50 and 250 μM) caused a decrease in GR activity in wheat seedlings. Like Cd, other heavy metals have been shown to produce differential effects on GR activity in plants. In Vigna radiata, Cr(VI) treatment has been reported to cause significant stimulation in GR activity (Shanker et al., 2004). In wheat seedlings, Thounaojam et al. (2012) observed that 100 μM of Cu increased GR activity by 48% in shoots and by 60% in roots. However, Gangwar et al. (2011a) observed that treatment of pea seedlings with Cr(VI) resulted in a significant decline in GR activity.


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Similarly, it has been reported that Zn (0.53 mM) caused a significant decline in GR activity in the roots and shoots of wheat seedlings. According to these studies, transcriptomic results also revealed that metal stress down-regulates expression of the GR gene (GR1) in Arabidopsis thaliana (Vanhoudt et al., 2010). Under stress conditions, an increase or decrease in GR activity has been related to enhanced or suppressed metal tolerance, respectively. Transgenic studies also revealed the important role of GR in enhancing plants’ tolerance of stress. It has been demonstrated that overexpression of the GR gene in transgenic tobacco enhances tolerance against metal stress (Martret et al., 2011). Pilon-Smits et al. (2000) reported that the bacterial GR gene, when targeted in cytosol (cytGR) or plastid (cpGR) of Brassica juncea L., enhanced tolerance against Cd (100 μM) but cpGR transgenics were more resistant. Further, Hong et al. (2009) reported that expression of chloroplastic (OsGR3) and cytosolic (OsGR2) isoforms of GR are essential for stress tolerance in rice.

10.5.2 Nonenzymatic antioxidants 10.5.2.1 Glutathione Glutathione is a tripeptide with the sequence L-γ-glutamyl-L-cysteinylglycine (γ-Glu-Cys-Gly) that is widely distributed in plant tissues with an antioxidant function facilitated by the sulfhydryl group of cystein (Rouhier et al., 2008). In plants, GSH has a number of important functions in metabolism, catalysis, and transport. Research on GSH-deficient Arabidopsis mutants has demonstrated that glutathione has critical functions in embryo and meristem development (Vernoux et al., 2000). On oxidation, it forms a thiyl radical that reacts with the second oxidized glutathione, forming a disulfide bond when oxidized (Halliwell and Gutteridge, 1999). The ratio of GSH/GSSG is often used as an indicator of oxidative stress in cells and performs an antioxidant function by quenching many ROS such as 1O2, O2•2, and •OH. Further, GSH can stop free radical-based chain reactions and also is an essential substrate for the glutathione peroxidase enzyme (Halliwell and Gutteridge, 1999). Maintenance of the GSH level is reported to be crucial in preventing oxidative damage to cells exposed to stressors that promote oxidative stress. It occurs abundantly in a reduced form in many plant tissues and is localized in all cell compartments (e.g., cytosol, endoplasmic reticulam, vacuoles, mitochondria, chloroplasts, peroxisomes) as well as in apoplast with concentrations in the millimolar range (Jiménez et al., 1997; Rouhier et al., 2008). In chloroplast, the concentration of GSH is estimated to be between 1 and 4.5 mM (Noctor and Foyer, 1998). The reduced form of glutathione is necessary to maintain the normal reduced state of cells to minimize all damaging effects of stress. It can potentially scavenge 1O2 (Smirnoff, 1993; Noctor and Foyer, 1998) as well as other ROS (e.g., •OH) for which nonenzymatic enzymes have evolved. The change in the ratio of its reduced (GSH) and oxidized (GSSG) forms occurs during the degradation of H2O2 and is important in certain redox-signaling pathways (Rouhier et al., 2008). It has been suggested that the ratio of GSH/GSSG, indicative of the cellular redox balance, may be involved in ROS perception and protection mechanisms (Foyer and Noctor, 2005). In addition, GSH plays a key role in the antioxidative defense system by regenerating another potential water-soluble antioxidantascorbate via the ascorbateglutathione cycle (Foyer et al., 1997; Noctor and Foyer, 1998). Several studies revealed the importance of GSH in protecting plants against metal stress. Vanhoudt et al. (2010) demonstrated that the redox balance of glutathione is an important defense

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function to protect Arabidopsis thaliana against uranium and cadmium stress. In Vicia faba, Hg is reported to enhance GSH content, and its increased level was related to the elimination of H2O2 via the ascorbateglutathione cycle (Wang et al., 2010). In barley genotypes, it has been reported that an elevated level of GSH protected stressed seedlings against oxidative stress by depressing O2•2, H2O2, and MDA accumulation (Chen et al., 2010a,b). Kalinowska and Pawlik-Skowrońska (2010) reported that maintenance of a higher level of GSH, concomitant with phytochelatin production, was responsible for a higher Cu resistance to Stichococcus minor. Transgenic studies also revealed that GSH plays a crucial role in initiating tolerance against metal stress. It has been demonstrated that the Escherichia coli gshl gene encoding γ-glutamylcysteine synthetase (γ-ECS)—a rate-limiting enzyme of glutathione biosynthesis when targeted to plastid of Brassica juncea—enhanced Cd (0.150.25 mM) tolerance (Zhu et al., 1999b). Researchers concluded that overexpression of γ-ECS increases biosynthesis of glutathione and phytochelatins which in turn enhances Cd tolerance. Further, overexpression of the Escherichia coli gshII gene encoding glutathione synthetase (GS) in the cytosol of Brassica juncea has also been shown to enhance Cd tolerance (Zhu et al., 1999a). In Thlaspi, it has been reported that increased biosynthesis of glutathione plays an important role in Ni accumulation and tolerance (Freeman et al., 2004). More recently, it has been demonstrated that blocking of glutathione biosynthesis by the specific inhibitor of γ-glutamylcysteine synthetase (GSH1), buthionine sulfoximine, resulted in loss of Fe-mediated Zn tolerance (Shanmugam et al., 2012). In addition, the results of this study showed that two glutathione-deficient mutant alleles of GSH1, pad2-1, and cad2-1 contain a very low level of glutathione when compared to the wild-type glutathione level. Thus, these studies clearly show importance of glutathione in regulating the extent of metal toxicity.

10.5.2.2 Ascorbate Ascorbate (AsA) is a key antioxidant that reacts with 1O2, O2•2, and •OH radicals (Chen and Gallie, 2004). AsA is the major, and probably the only, antioxidant buffer in the apoplast that performs multiple functions in cells (Gest et al., 2013). Ascorbate is found in chloroplasts and cytosols, where it also acts as a substrate for ascorbate peroxidase. It has been shown that AsA is low cost in terms of synthesis and toxicity, and its benefits include proper protection of ranges of enzymes and the glutathione pool (Gest et al., 2013). In plant cells, ascorbate is the most important reducing substrate for H2O2 detoxification (Mehlhorn et al., 1996; Nakano and Asada, 1998). Ascorbate scavenges ROS enzymatically as well as nonenzymatically and limits ROS-induced damage to macromolecules (Dixon et al., 2009; Foyer and Noctor, 2011). Further, AsA can terminate free radical-based chain reactions by serving as a stable electron donor in interactions with free radicals being converted into dehydroascorbate (DHA). Studies revealed that the content of ascorbate and related genes is differentially regulated by stressors. In bean seedlings, Zn stress (50 ppm) has been shown to significantly enhance AsA content (Michael and Krishnaswamy, 2011). In Oryza sativa cv. Taichung Native 1, Cd (5 mM) treatment has also been shown to enhance ascorbate content and results were correlated with enhanced Cd tolerance (Hsu and Kao, 2004). A study by Vanhoudt et al. (2010) demonstrated that the AsAredox balance played an important role in mitigating uranium and Cd toxicity. In rice seedlings, Cu stress (10100 μM) has been shown to enhance ascorbate content; it increased by 24% in shoots and by 29% in roots at 100 μM after a 5-day treatment (Thounaojam et al., 2012). Besides an increased content of AsA, a decline has been observed under heavy metal stress. Gangwar et al.

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(2011a,b) obversed that Cr(VI) and Mn treatments of pea seedlings resulted into a decline of ascorbate content. However, another study showed that AsA content was unchanged under heavy metal stress (Ratkevicius et al., 2003). The importance of ascorbate in protecting plants against oxidative stress has been confirmed in Arabidopsis ascorbate-deficient vtc1. Huang et al. (2005) demonstrated that in vtc1 plants oxidative stress sensitivity increased more dramatically than in wild types. Veljovic-Jovanovic et al. (2001) noted that vtc1 plants contain 70% less AsA than wild-type plants and exhibit a redistribution of the antioxidant system. In addition, Mu¨ller-Moulá et al. (2003) observed that vtc1 Arabidopsis plants were unable to acclimate against stress and showed an increased degree of lipid peroxidation. Further, it has been reported that mutation in GDP-mannose pyrophosphorylase, an enzymegenerating GDP-mannose for AsA biosynthesis, leads to hypersensitivity against ammonium stress; ultimately, this resulted in Arabidopsis root growth inhibition, altered ammonium metabolism, and hormone homeostasis (Barth et al., 2010). Thus, these studies clearly indicate the importance of ascorbate in mitigating oxidative stress and normal growth and development of plants.

10.6 Plant growth hormones Plant hormones (also known as phytohormones) are organic substances that regulate plant growth and development. Plants produce a wide variety of hormones, including auxins, gibberellins (GA), abscisic acid (ABA), cytokinins (CK), salicylic acid (SA), ethylene (ET), jasmonates (JA), brassinosteroids (BR), and peptides. A large number of related synthetic chemical compounds are used to regulate the growth of cultivated plants, weeds, and in vitro grown plants and plant cells. These human-made compounds are called plant growth regulators (PGRs). Plant hormones may be part of a signal-transduction pathway, or their presence may stimulate reactions that are signal and/or causative agents for stress responses (Argueso et al., 2010; Leyser, 2010; Qin et al., 2011). Plant hormones as signal molecules regulate cellular processes in targeted cells locally and when moved to other locations of the plant. They also determine the formation of the root, stem, leaf, and flower and facilitate the shedding of leaves and the development and ripening of fruits. Hormones shape the plant and affect seed growth, time of flowering, sex of flowers, and senescence of leaves and fruits. They affect which tissues grow upward and which grow downward and even plant death. Hormones are vital to plant growth and lacking them, plants would be mostly a mass of undifferentiated cells. Plant hormones play important roles in diverse growth and developmental processes as well as various biotic and abiotic stress responses in plants. Studies revealed that endogenous regulations (e.g., biosynthesis, transport, redistribution, and conjugation of plant hormones) play a crucial role during the acclimation process against stress (Du et al., 2012; He et al., 2012a; Wilkinson et al., 2012; Krishnamurthy and Rathinasabapathi, 2013; Srivastava et al., 2013). Besides this, exogenous application of plant hormones has also been reported to enhance stress tolerance in plants affected by heavy metals (Quint and Gray, 2006; Koprivova et al., 2008; Gangwar et al., 2011a,b; Peto et al., 2011; Rubio-Wilhelmi et al., 2011; Claeys et al., 2012; Elobeid et al., 2012; Nam et al., 2012; Zhu et al., 2012; Krishnamurthy and Rathinasabapathi, 2013; Srivastava et al., 2013). During the last decade, extensive work has been carried out to understand plant hormone-mediated enhancement in stress tolerance using physiological, biochemical, genetic, molecular, and genomic approaches for crop breeding and management.

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Next in this chapter, we summarize the roles and mechanisms of auxins, cytokinins, and gibberellic acids in enhancing tolerance of heavy metals including other stresses.

10.7 Role of plant growth hormones under stress 10.7.1 Behavior of auxins under stress There is increasing evidence that auxins play an important role in the protection and regulation of plants’ metabolism under stress conditions. The endogenous levels of auxins generally decreases following metal stress; thus, it is quite possible that exogenous application of auxins may complement the function of endogenous auxins, as reported in studies where indole-3-acetic acid (IAA) was exogenously applied. In Brassica juncea, it has been reported that As stress causes toxicity by changing the levels of auxins (i.e., indole-3-acetic acid, indole-3-butyric acid, and naphthalene acetic acid) and altering expression of nearly 69 microRNAs belonging to 18 plant miRNA families (miRNAs) (Srivastava et al., 2013). However, an exogenous supply of IAA improved growth of Brassica juncea under As stress by modulating expression of miR167, miR319, and miR854, suggesting a protective role of IAA in enhancing metal tolerance. Similarly, Gangwar et al. (2011a,b) demonstrated that exogenous application of IAA protected metabolic processes, such as nitrogen metabolism, in pea seedlings against Cr(VI) and Mn toxicity by regulating oxidative stress and the antioxidant defense system. In wheat seedlings, exogenous application of IAA is reported to increase growth of the root and shoot and to protect plants against stress (Egamberdieva, 2009). Chakrabarti and Mukherji (2003) also reported that exogenous application of IAA improved growth and nitrogen metabolism and protected Vigna radiata under stress conditions. It also has been reported that Medicago truncatula plants modulated by RD64 (MtRD64—IAA-overproducing strain) accumulated a higher level of trehalose as its endogenous osmolyte and showed an increased tolerance to several stress conditions; this occurred while Mt-1021 (low IAA-producing strain) plants almost die, thus indicating the role of auxin in imparting tolerance against stress (Bianco and Defez, 2009). In addition to protecting plants under stress, exogenous application of IAA has been shown to enhance heavy metal accumulation in plants that may be beneficial from the point of view of a phytoremediation program. Fa¨ssler et al. (2010) observed that exogenous application of IAA may protect plants as well as enhance phytoextraction of heavy metals. Similarly, Hadi et al. (2010) reported IAA improved phytoextraction of Pb by maize. Studies have shown that distribution and an active pool of auxins play a crucial role in plants’ metal tolerance. It has been demonstrated that the auxin transporter mutants aux1, pin1, and pin2 were significantly more sensitive to As(III) than the wild type (WT), and auxin transport inhibitors significantly reduced plant tolerance to As(III) in the WT due to the increased levels of H2O2 (Krishnamurthy and Rathinasabapathi, 2013). However, an exogenous supply of IAA improved As (III) tolerance of aux1 and not that of the WT, suggesting a positive role for auxin transport through AUX1 on plants’ tolerance to As(III) stress via ROS-mediated signaling. An active auxins pool has also been shown to be involved in reducing the toxicity of heavy metals. In the Populus 3 canescens line-expressing glycoside hydrolase (GH) family 3 (GH3) enzymes, Cd (50 μM) inhibited growth and photosynthetic performance by triggering increased activities of GH3 (Elobeid et al., 2012). Because GH3 enzymes remove auxin from the active pool by conjugation

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and act as mediators between growth and defense, and thus a metal stress-induced increase in GH3 activities may deplete the auxin in plants, which in turn stunts the metabolism. Further, Du et al. (2012) demonstrated that overexpression of the OsGH-2 gene resulted in a decreased active auxins pool, and this effect was accompanied by hypersensitivity of rice seedlings to drought stress. Besides protecting plants against excess heavy metal stress, the significance of auxins has also been reported to protect plants against essential element deficiency. Chen et al. (2010a,b) reported that Fe-deficiency increased auxin levels in WT Arabidopsis thaliana; this was accompanied by up-regulation of root ferricchelate reductase (FCR) activity and the expression of the basic helixloophelix transcription factor (FIT) and the ferric reduction oxidase 2 (FRO2) genes. The up-regulation of these parameters was further stimulated by application of exogenous auxin (a-naphthaleneacetic acid) but was suppressed by polar auxin transport inhibition with 1-naphthylphthalamic acid, thus suggesting a possible implication of auxin signaling in mitigating the adverse consequences of Fe-deficiency. Under stress, auxin signaling is not yet well known but by using genetic, genomic, and molecular approaches several components have been deciphered. With the recent finding that F-box TRANSPORT INHIBITOR RESPONSE 1 (TIR1)/AUXIN SIGNALING F-BOX (AFB) proteins also function as auxin receptors, it has been theorized that the mechanism of auxin action is via TIR1 and that the TIR1 family could account for all auxin responses (Badescu and Napier, 2006; Quint and Gray, 2006). It has been demonstrated that TIR1 mediates Aux/IAA (i.e., acts as a repressor of auxin-induced gene expression) protein degradation and auxin-regulated gene transcription (Dharmasiri et al., 2005). Other studies have also shown that ROS-enhanced auxin responsiveness plays a role in reorientation of growth under stress conditions (Pasternak et al., 2005). It has been reported that an endogenous pool of auxin is tightly regulated by GH3 gene encoding and auxin-conjugating enzymes under stress and determines the fate of stressed plants. The Arabidopsis mutant, wes1-D, in which a GH3 gene WES1 was activated, exhibited auxin-deficient traits (e.g., reduced growth); however, wes1-D was resistant to both biotic and abiotic stresses. Further, a T-DNA insertional mutant showed reduced stress resistance (Park et al., 2007). Meng et al. (2010) have shown implications of microRNA in auxin signaling. Nitric oxide (NO) has also been shown to be involved in auxin signal transduction under Cu stress (Peto et al., 2011). From these studies it can be concluded that endogenous regulation of auxin and receptor and auxin-responsive genes together crosstalk with NO and that microRNAs are involved in auxin signaling.

10.7.2 Behavior of gibberellic acids under stress The gibberellins (GAs) are a large family of tetracyclic diterpinoid plant growth substances associated with various growth and development processes such as seed germination, stem and hypocotyls elongation, leaf expansion, floral initiation, floral organ development, fruit development, and induction of some hydrolytic enzymes in the aleurone of cereal grains (Matsuoka, 2003). Gibberellins also affect the rate of cell division, seed and bud dormancy, and induce growth at lower temperatures. Young, growing meristematic cauline tissue, apical root cells, and young fruits, as well as unripe or germinating seeds, are all rich in GAs. Gibberellic acids promote fructose-1,6biphosphatase and sucrose phosphate synthase and stimulate phloem loading (Iqbal et al., 2011).

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Gibberellic acid is one of the major contributors in the process of source and sink formations and thus is a thoroughly studied plant hormone. Many GA-related mutants have been identified from plant species and can be categorized as either GA-sensitive or GA-insensitive (Matsuoka, 2003). GA-sensitive mutants respond to exogenous GA treatment to rescue their abnormal phenotypes. These mutations are usually caused by deficiencies in the genes encoding GA catalytic enzymes and play an important role in understanding GA signaling (Matsuoka, 2003; Schwechheimer, 2008). To alleviate the deleterious effects of stress, different types of phytohormones have been used. Of these, GAs have been the main focus of some plant scientists (Hisamatsu et al., 2000; Tuna et al., 2008; Iqbal et al., 2011; Zhu et al., 2012). Because reduced plant growth can result from an altered hormonal status, exogenous application of phytohormone has been an attractive approach to attenuate stress. Several studies have appeared in leading journals showing GA-mediated alleviation of stress. In Arabidopsis thaliana, GA (5 μM) is reported to alleviate Cd toxicity by reducing Cd uptake and lipid peroxidation (Zhu et al., 2012). Further results of this study revealed that GA enhanced reduced NO which in turn down-regulated expression of the IRT1 gene, which is involved in Cd absorption, as indicated by the fact that there is no effect of GA in the reduction of Cd uptake in an IRT1 knockout mutant, irt1. In wheat seedlings, Ni (50 mM) has been reported to decrease growth, chlorophyll content, and carbonic anhydrase activity by enhancing oxidative stress while adding GA-ameliorated toxic effects (Siddiqui et al., 2011). Gangwar et al. (2011a) also observed that GA ameliorated the toxic effects of Cr (50250 μM) on growth and ammonium assimilation of pea seedlings by regulating oxidative stress and the antioxidant system. Exogenous application of GA has been shown to reprogram the higher growth of soybeans under stress conditions by enhancing the levels of daidzein and genistein (commonly known as phytoestrogens), suggesting the protective role of GA in mitigating the adverse consequences of stress factors (Hamayun et al., 2010). Meng et al. (2009) reported that GA (50 μM) alleviated Cd (10400 μM) induced adverse effects on seed germination and growth of Brassica napus L. by regulating oxidative stress and damage. In wheat plants, priming with GA has been shown to enhance tolerance of them by protecting photosynthesis and regulating ionic distribution and hormonal homeostasis (Iqbal and Ashraf, 2013). It has been observed that Pb and Zn affected seed germination in Cicer arietinum cv. Aziziye-94 by altering hormonal balance, and exogenous application of GA reverses the effect of heavy metals (Atici et al., 2005). Further, Sharaf et al. (2009) reported that GA abolished the detrimental effects of Cd and Pb on broad bean and lupin plants by regulating activities of proteases, catalases, and peroxidases. However, Rubio et al. (1994) reported that external addition of GA could not overcome the depressing effect of metals (Cd and Ni) on rice seedlings. Transcriptomic analyses also revealed that exogenous addition of GA plays an important role in counteracting the adverse effect of stressors. Sun et al. (2013) demonstrated that GA imparts abiotic stress resistance to Arabidopsis by up-regulating the GAST1 gene (identified as a GA-stimulated transcript) which in turn modulates ROS accumulation. In rice, the OsAOP gene encodes a tonoplast intrinsic protein (TIP) that has been observed to express a response to GA and stress; it is suggested that this gene plays an essential role in the defense in rice against several stresses (Liang et al., 2013). It is well known that sulfur-containing compounds play an important role in plants’ defense against stresses. For Arabidopsis, it has been demonstrated that the expression of adenosine 50 -phosphosulfate reductase, the key enzyme of sulfate assimilation, is increased using GA signaling under stress, while other hormones do not show such an effect; this suggests utilizing GA

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signaling under stress to protect plant metabolism (Koprivova et al., 2008). It has been observed that GA signaling controls seed germination under stress conditions. A membrane-bound NAC transcription factor, NTL8 (negatively affecting seed germination), has been shown to mediate salt regulation of seed germination via the GA pathway, primarily independent of ABA signaling (Kim et al., 2008), suggesting the positive role of GA in regulating seed germination on the basis of prevailing environmental conditions. It has been reported that GA-induced expression of the wheat TaMYB73 gene in Arabidopsis, and its overexpression, also enhanced tolerance against stress (He et al., 2012b). In addition, expression of several stress-responsive genes (e.g., AtCBF3, AtABF3, AtCBF3, and AtABF3) was reported in TaMYB73 overexpressing lines, which further aided in strengthening stress tolerance in Arabidopsis, indicating the role of GA in increasing stress tolerance by enhancing expression of TaMYB73. DELLA proteins, which are well-known repressors of GA responses, have recently been shown to be involved in avoiding stress. Another study showed that stress induces changes in GA metabolism resulting in stabilization of DELLA, which in turn leads to mitotic exit and endoreproduction (Claeys et al., 2012); therefore it protects plants’ metabolism by a stress-avoidance mechanism. These studies clearly indicate that GA plays an important role in protecting plant metabolisms against various stresses; however, this may occur via various routes, suggesting that there is complex GA signaling during plants’ acclimation to stress.

10.7.3 Behavior of cytokinins under stress The name cytokinin is because of its specific effects on cytokinesis. Kinetin and certain other substances show kinetin-like activity, collectively called cytokinins. Cytokinin N6-substituted adenine derivatives have been shown to be involved in the regulation of many aspects of growth and differentiation, including cell division, apical dominance, nutrient metabolism, chloroplast development, senescence, flowering, nodulation, and circadian rhythms (Van Staden and Davey, 1979; Perilli et al., 2010). Cytokinins are usually produced in roots, young fruits, and seeds. They enter the shoot organs via the xylem. Organs that are cut off from a continuous cytokinin supply (e.g., cut shoots) age faster than those that are connected to their roots. In light of the important regulatory role played by cytokinins in modulating development, it seems feasible to also anticipate their involvement in responses to adverse environmental conditions. Like auxins and gibberellins, cytokinins have been shown to play an important role during plant acclimation to stress conditions. Studies have shown that cytokinins are important for the regulation of environmental stress responses and involve intense interactions and crosstalk with other hormones (Jeon et al., 2010; Nishiyama et al., 2011; Ha et al., 2012). Environmental stresses, such as metals, high light, temperature, drought, and high salinity, decrease the production and transport of cytokinins from roots. Exogenous application of cytokinins has been reported to increase the stress-tolerance capacity of plants indicating a beneficial effect of cytokinins in the regulation of plants’ adaptation to environmental stresses. Thus, these findings revealed the potential application of cytokinins in agricultural biotechnology. For Pisum sativum L. seedlings, 10 μM of kinetin has been reported to enhance Mn tolerance and also increase seedlings’ growth by improving ammonium assimilation and the antioxidant defense system (Gangwar et al., 2010). Al-Hakimi (2007) observed that Cd (2550 μM) treatment inhibited the growth rate, chlorophyll content, and net photosynthesis (PN); however, addition of

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kinetin reduced Cd-induced alterations in pea seedlings. Piotrowska-Niczyporuk et al. (2012) showed that heavy metals (Cd, Pb, and Cu) decreased the growth of green algae, Chlorella vulgaris, by enhancing ROS and altering the defense system; however, exogenous application of cytokinins alleviated stress symptoms by reducing metal absorption and stimulating the defense system. In barley, Cd (39.5 mM) decreased seed germination and coleoptile elongation, but exogenous application of kinetin decreased such toxic effects (Munzuroglu and Zengin, 2006). It has been reported that Pb (5 μM) treatment lowered terminal electron transport activity (ETS) by 25% in root tissues of Picea abies (L.) Karst, while zeatin mitigated the lead-induced inhibition of root growth and the ETS activity, indicating that the presence of cytokinin in the rhizosphere could be an important factor affecting Pb toxicity (Vodnik et al., 1999). The study showed that degradation of cytokinin may be one of the prime reasons through which stressors cause toxicity and that exogenous application of cytokinins protects plants against stress. Gemrotová et al. (2013) reported that an inhibitor of cytokinin degradation, INCYDE (2-chloro-6-(3-methoxyphenyl)aminopurine), protected the medicinal plant Bulbine natalensis Baker against the negative effects of Cd and suggested that modulating the cytokinin status with inhibitors of cytokinin perception and/or degradation may be useful in protecting plants against the adverse effects of high Cd levels. Thomas et al. (2005) observed that tobacco plants expressing the cytokinin-synthesizing gene (Ipt) showed enhanced tolerance against Cu stress as indicated by lower lipid peroxidation and increased expression of the metallothionein gene (MT-L2), despite accumulating a higher Cu concentration compared to nontransformed plants. In addition to alleviating excess metal toxicity, cytokinins have been reported to play an important role in plant acclimation under essential metal deficiencies. Rubio-Wilhelmi et al. (2011) reported that tobacco transgenic plants expressing isopentenyltransferase, a gene coding the ratelimiting step in cytokinin synthesis, avoided the alterations of oxidative metabolism and maintained relative growth rate and biomass accumulation under suboptimal nitrogen conditions, suggesting that cytokinin synthesis in transgenic plants may be an effective mechanism to improve nitrogen use efficiency. Further, Nam et al. (2012) demonstrated that cytokinin played a regulatory role in response to potassium ion deficiency in Arabidopsis. These researchers used cytokinin-deficient (CK-deficient) mutants and cytokinin-receptor (CK-receptor) mutants and showed that CK-deficient mutants respond to low potassium levels in terms of ROS accumulation and root hair growth, while CK-receptor mutants lost responsiveness to low potassium levels and did not show ROS accumulation and root hair growth, indicating that cytokinin plays a role in plants’ adaptation to low potassium conditions. Besides heavy metal toxicity, cytokinins have been studied for their efficacy in alleviating the toxicity of other abiotic stresses such as drought, salinity, and temperature. It has been observed that drought decreased growth of Zea mays L., while exogenous addition of cytokinin reversed this effect and enhanced photosynthetic performance of stressed plants through NO signaling (Shao et al., 2010). In Salvia officinalis, exogenous application of kinetin (10 μM) has been reported to reduce salt stress by improving antioxidant composition (Tounekti et al., 2011). Rivero et al. (2010) demonstrated that Nicotiana tabacum SR1 plants that overexpress the PSARK::IPT (i.e., for senescence-associated receptor kinase::isopentenyltransferase) gene showed enhanced tolerance to drought in comparison to the wild types. Further results revealed that transgenic plants showed enhanced expression of several gene-encoding proteins associated with Chl synthesis, light reactions (i.e., photosystem II, the cytochrome b(6)/f complex, photosystem I,


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NADH oxidoreductase, and the ATP complex), the Calvin-Benson cycle, and photorespiration; however, in wild types their expression declined. In rice, it has also been demonstrated that overexpression of the PSARK::IPT gene delayed response to water stress and increased grain yield probably by differentially expressing gene-encoding enzymes associated with hormone synthesis and hormone-regulated pathways (Peleg et al., 2011). In another study, Rivero et al. (2009) observed that tobacco plants overexpressing the PSARK-IPT gene exhibited tolerance against water deficiency and involvement of photorespiration in protection of the photosynthetic process that was concluded during stress. In addition, Merewitz et al. (2012) reported that overexpression of the SAG12-ipt gene (i.e., senescence-activated promoter-isopentenyl transferase) enhanced the drought tolerance of Agrostis stolonifera L. by maintaining the accumulation of metabolites, particularly amino acids (g-aminobutyric acid, proline, glycine and alanine), carbohydrates (sucrose, fructose, maltose, and ribose), and organic acids, which are mainly involved in the Krebs cycle. In Solanum lycopersicum L., it has been reported that Ipt gene expression enhanced root cytokinin biosynthesis and modified both shoot hormonal and ionic status, thus ameliorating salinity-induced decreases in growth and yield (Ghanem et al., 2011). Another study showed that expression of the Ipt gene with two inducible promoters (SAG12 and HSP18) increased or maintained six leaf proteins (i.e., oxygen-evolving enhancer protein 2, putative oxygen evolving complex, Rubisco small subunit, enolase, Hsp90, and glycolate oxidase) and nine root proteins (i.e., nucleotide-sugar dehydratase, NAD-dependent isocitrate dehydrogenase, putative heterogeneous nuclear ribonucleoprotein A2, Fd-GOGAT, ferredoxin-NADP reductase precursor, dDTP-glucose 4-6-dehydratase-like protein, ascorbate peroxidase, and two unknown proteins) in Agrostis stolonifera; this involved imparting heat stress (35 C) tolerance (Xu et al., 2010). Cytokinin is an influential hormone and several genes, which may be involved in the plant acclimation process during stress, have been shown to be regulated by this hormone. Shi et al. (2012) identified 11 Solanum lycopersicum cytokinin response factors (SICRF1SICRF11) that respond to abiotic stress and suggested that they may have a diverse set of roles in stress and hormone regulation in tomato plants. Studies explicitly showed that cytokinins largely contribute to plants’ acclimation process during stress via a complex network of signaling. Although histidine kinase receptors, ATP/ADP-isopentenyltransferase (IPT) and cytokinin oxidase/dehydrogenases (CKXs), are well-known players of cytokinin signaling, further studies are needed to decipher the complex network of cytokinin signaling in order to manage the productivity of plants facing stress.

10.8 Conclusion and future prospects Environmental stresses, such as heavy metals, drought, salts, temperature, and so on, are major factors that limit agricultural productivity. Further, the ever-increasing global population is compelling scientists to seek and develop strategies to enhance food production under such adverse conditions in order to satisfy the increasing demand for food. During the last decade, much progress has been made in understanding molecular mechanisms related to metal acquisition, transport, and defense and have been successfully used to induce the capability of plants to survive under metal stress conditions. In the case of essential metals, an understanding of the complex processes of metal

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uptake, transport, and defense is necessary to enhance metal acquisition under metal-limiting conditions in order to increase productivity; it is also necessary to check their excess accumulation under metal excess conditions. However, for nonessential metals, understanding and identification of their transporters has been used to enhance the metal tolerance capacity of plants and to reduce their accumulation in crop plants. In spite of much progress recognizing the molecular mechanisms of heavy metal toxicity and detoxification in plants, many components of the complex metal-signaling network remain to be identified. Considering the importance of hormones (e.g., auxins, gibberellins, and cytokinins) in many plants’ functioning under physiological and metal stress conditions, further research dealing with endogenous regulation of plant hormone metabolism may contribute much to dealing with such adverse conditions. So far, there are some excellent studies that support the importance of hormones in plants under metal as well as other abiotic stress conditions. For example, the application of exogenous hormones, as well as the introduction of gene(s) of their biosynthetic pathways, seems to initiate various biochemical pathways that enhance plant tolerance against various abiotic stresses. Therefore, elucidation of hormonal metabolisms in plants can contribute to developing physiological, biochemical, and biotechnological strategies against abiotic stresses in order to increase plant yield and crop productivity for the world’s ever-increasing population.

Acknowledgments One of the authors (SG) is thankful to CSIR, New Delhi for providing financial assistance in the form of Research Associateship to carry out research. The authors are thankful to the Head, Department of Plant Science, M.J.P. Rohilkhand University, Bareilly, and the Department of Botany, University of Allahabad, Allahabad, for their kind cooperation. One of the authors (V.P. Singh) wishes to thank Shri Akhilesh Chandra Gupta, Principal, Government R.P.S. P.G. College, Baikunthpur, C.G., for his kind cooperation and sympathetic attitude.

References Agarwal, S.K., 2009. Heavy Metal Pollution. A.P.H. Publishing Corporation, New Delhi. Agrawal, S.B., Mishra, S., 2009. Effects of supplemental ultraviolet-B and cadmium on growth, antioxidants and yield of Pisum sativum L. Ecotoxicol. Environ. Saf. 72, 610618. Al-Hakimi, A.M.A., 2007. Modification of cadmium toxicity in pea seedlings by kinetin. Plant Soil Environ. 53, 129135. Ali, S., Farooq, M.A., Yasmeen, T., Hussain, S., Arif, M.S., Abbas, F., et al., 2013. The influence of silicon on barley growth, photosynthesis and ultra-structure under chromium stress. Ecotoxicol. Environ. Saf. 89, 6672. Alscher, R.G., Erturk, N., Heath, L.S., 2002. Role of superoxide dismutases (SODs) in controlling oxidative stress in plants. J. Exp. Bot. 53, 13311341. Argueso, C.T., Raines, T., Kieber, J.J., 2010. Cytokinin signaling and transcriptional networks. Curr. Opin. Plant Biol. 13, 533539. Arrigoni, O., Dipierro, S., Borraccino, G., 1981. Ascorbate free radical reductase, a key enzyme of the ascorbic acid system. FEBS Lett. 125, 242245.

References

237

Asada, K., 1994. Production and action of active oxygen species in photosynthetic tissue. In: Foyer, C.H., Mullineaux, P.M. (Eds.), Causes of Photooxidative Stress and Amelioration of Defense Systems in Plants. CRC Press, Boca Raton, FL, pp. 77104. ¨ ., A˘gar, G., Battal, P., 2005. Changes in phytohormone contents in chickpea seeds germinating under Atici, O lead or zinc stress. Biol. Plant 49, 215222. Aust, S.D., Marehouse, L.A., Thomas, C.E., 1985. Role of metals in oxygen radical reactions. Free Radic. Biol. Med. 1, 325. Baccouch, S., Chaoui, A., Ferjani, E.E., 2001. Nickel toxicity induces oxidative damage in Zea mays roots. J. Plant Nutr. 24, 10851097. Backor, M., Vaczi, P., Bartak, M., Budova, J., Dzubaj, A., 2007. Uptake, photosynthetic characteristics and membrane lipid peroxidation levels in the lichen photobiont Trebouxia erici exposed to copper and cadmium. Bryologist 110, 100107. Badescu, G.O., Napier, R.M., 2006. Auxin: will it all end in TIRs. Trends Plant Sci. 11, 217223. Balestrasse, K.B., Gardey, L., Gallego, S.M., Tomaro, M.L., 2001. Response of antioxidant defence system in soybean nodules and roots subjected to cadmium stress. Aust. J. Plant Physiol. 28, 497504. Barth, C., Gouzd, Z.A., Steele, H.P., Imperio, R.M., 2010. A mutation in GDP-mannose pyrophosphorylase causes conditional hypersensitivity to ammonium, resulting in Arabidopsis root growth inhibition, altered ammonium metabolism, and hormone homeostasis. J. Exp. Bot. 61, 379394. Basile, A., Sorbo, S., Pisani, T., Paoli, L., Munzi, S., Loppi, S., 2012. Bioacumulation and ultrastructural effects of Cd, Cu, Pb and Zn in the moss Scorpiurum circinatum (Brid.) Fleisch. & Loeske. Environ. Pollut. 166, 208211. Basu, U., Good, A.G., Taylor, G.J., 2001. Transgenic Brassica napus plants overexpressing aluminium-induced mitochondrial manganese superoxide dismutase cDNA are resistant to aluminium. Plant Cell Environ. 24, 12691278. Becana, M., Dalton, D.A., Moran, J.F., Iturbe-Ormaetxe, I., Matamoros, M.A., Rubio, M.C., 2000. Reactive oxygen species and antioxidants in legume root nodules. Physiol. Plant 109, 372381. Bhattacharjee, S., 1997. Membrane lipid peroxidation, free radical scavangers and ethylene evolution in Amaranthus as affected by lead and cadmium. Biol. Plant 40, 131135. Bianco, C., Defez, R., 2009. Medicago truncatula improves salt tolerance when nodulated by an indole-3-acetic acid-overproducing Sinorhizobium meliloti strain. J. Exp. Bot. 60, 30973107. Bienert, G.P., Thorsen, M., Schussler, M.D., Nilsson, H.R., Wagner, A., Tamas, M.J., et al., 2008. A subgroup of plant aquaporins facilitate the bi-directional diffusion of As(OH)3 and Sb(OH)3 across membranes. BMC Biol. 6, 26. Boominathan, R., Doran, P.M., 2002. Ni-induced oxidative stress in roots of the Ni hyperaccumulator, Alyssum bertolonii. New Phytol. 156, 205215. Boˇcová, B., Huttová, J., Liptáková, L., Mistrı´k, I., Ollé, M., Tamás, L., 2012. Impact of short-term cadmium treatment on catalase and ascorbate peroxidase activities in barley root tips. Biol. Plant 56, 724728. Branquinho, C., Brown, D.H., Máguas, C., Catarino, F., 1997. Lead (Pb) uptake and its effects on membrane integrity and chlorophyll fluorescence in different lichen species. Environ. Exp. Bot. 37, 95105. Brocks, J.J., Logan, G.A., Buick, R., Summons, R.E., 1999. Archean molecular fossils and the early rise of eukaryotes. Science 285, 10331036. Cargnelutti, D., Tabaldi, L.A., Spanevello, R.M., Jucoski, G.O., Battisti, V., Redin, M., et al., 2006. Mercury toxicity induces oxidative stress in growing cucumber seedlings. Chemosphere 65, 9991006. ¨ zay, C., Bozda˘g, A., Terzi, H., 2010. Lead contamination reduces Cenkci, S., Ci˘gerci, I.H., Yıldız, M., O chlorophyll biosynthesis and genomic template stability in Brassica rapa L. Environ. Exp. Bot. 67, 467473. Chakrabarti, N., Mukherji, S., 2003. Effect of phytohormone pretreatment on nitrogen metabolism in Vigna radiata under salt stress. Biol. Plant 46, 6366.

238


Chamnongpol, S., Willekens, H., Langebartels, C., Van Montagu, M., Inzé, D., Van Camp, W., 1996. Transgenic tobacco with a reduced catalase activity develops necrotic lesions and induces pathogenesis related expression under high light. Plant J. 10, 491503. Chen, F., Wang, F., Wu, F., Mao, W., Zhang, G., Zhou, M., 2010a. Modulation of exogenous glutathione in antioxidant defense system against Cd stress in the two barley genotypes differing in Cd tolerance. Plant Physiol. Biochem. 48, 663672. Chen, W.W., Yang, J.L., Qin, C., Jin, C.W., Mo, J.H., Ye, T., et al., 2010b. Nitric oxide acts downstream of auxin to trigger root ferric-chelate reductase activity in response to iron deficiency in Arabidopsis. Plant Physiol. 154, 810819. Chen, Z., Gallie, D.R., 2004. The ascorbic acid redox state controls guard cell signaling and stomatal movement. Plant Cell 16, 11431162. Chiang, H.C., Lo, J.C., Yeh, K.C., 2006. Genes associated with heavy metal tolerance and accumulation in Zn/Cd hyperaccumulator Arabidopsis halleri: a genomic survey with cDNA microarray. Environ. Sci. Technol. 40, 67926798. Chou, T.S., Chao, Y.Y., Huang, W.D., Hong, C.Y., Kao, C.H., 2011. Effect of magnesium deficiency on antioxidant status and cadmium toxicity in rice seedlings. J. Plant Physiol. 168, 10211030. Claeys, H., Skirycz, A., Maleux, K., Inzé, D., 2012. DELLA signaling mediates stress-induced cell differentiation in Arabidopsis leaves through modulation of anaphase-promoting complex/cyclosome activity. Plant Physiol. 159, 739747. Clemens, S., 2001. Molecular mechanisms of plant metal tolerance and homeostasis. Planta 212, 475486. Clemens, S., 2006. Toxic metal accumulation, responses to exposure and mechanisms of tolerance in plants. Biochimie 88, 17071719. Cui, Y., Zhao, N., 2011. Oxidative stress and change in plant metabolism of maize (Zea mays L.) growing in contaminated soil with elemental sulfur and toxic effect of zinc. Plant Soil Environ. 57, 3439. Dai, J.Y., Chen, L., Zhao, J.F., Ma, N., 2006. Characteristics of sewage sludge and distribution of heavy metal in plants with amendment of sewage sludge. J. Environ. Sci. 18, 10941100. Davey, J.E., van Staden, J., 1979. Cytokinin activity in Lupinus albus L: IV. Distribution in seeds. Plant Physiol. 63 (5), 873877. Dharmasiri, N., Dharmasiri, S., Estelle, M., 2005. The F-box protein TIR1 is an auxin receptor. Nature 435, 441445. Dho, S., Camusso, W., Mucciarelli, M., Fusconi, A., 2010. Arsenate toxicity on the apices of Pisum sativum L. seedling roots: effects on mitotic activity, chromatin integrity and microtubules. Environ. Exp. Bot. 69, 1723. Dietrich, I.E., Tice, M.M., Newman, D.K., 2006. The co-evolution of life and earth. Curr. Biol. 16, 395400. Dietz, K.J., Bair, M., Kra¨mer, U., 1999. Free radical and reactive oxygen species as mediators of heavy metal toxicity in plants. In: Prasad, M.N.V., Hagemeyer, J. (Eds.), Heavy Metal Stress in Plants from Molecules to Ecosystems. Spinger-Verlag, Berlin, pp. 7379. Dixit, V., Pandey, V., Shyam, R., 2001. Differential antioxidative responses to cadmium in roots and leaves of pea (Pisum sativum L. cv Azad). J. Exp. Bot. 52, 11011109. Dixit, V., Pandey, V., Shyam, R., 2002. Chromium ions inactivate electron transport and enhance superoxide generation in vivo in pea (Pisum sativum L. cv. Azad) root mitochondria. Plant Cell Environ. 25, 687693. Dixon, D.P., Hawkins, T., Hussey, P.J., Edwards, R., 2009. Enzyme activities and subcellular localization of members of the Arabidopsis glutathione transferase superfamily. J. Exp. Bot. 60, 12071218. Du, H., Wu, N., Fu, J., Wang, S., Li, X., Xiao, J., et al., 2012. A GH3 family member, OsGH3-2, modulates auxin and abscisic acid levels and differentially affects drought and cold tolerance in rice. J. Exp. Bot. 63, 64676480. Egamberdieva, D., 2009. Alleviation of salt stress by plant growth regulators and IAA producing bacteria in wheat. Acta Physiol. Plant 31, 861864.

References

239

Elbaz, A., Wei, Y.Y., Meng, Q., Zheng, Q., Yang, Z.M., 2010. Mercury-induced oxidative stress and impact on antioxidant enzymes in Chlamydomonas reinhardtii. Ecotoxicology 19, 12851293. Elobeid, M., Go¨bel, C., Feussner, I., Polle, A., 2012. Cadmium interferes with auxin physiology and lignification in Poplar. J. Exp. Bot. 63, 14131421. Faize, M., Burgos, L., Faize, L., Piqueras, A., Nicolas, E., Barba-Espin, G., et al., 2011. Involvement of cytosolic ascorbate peroxidase and Cu/Zn-superoxide dismutase for improved tolerance against drought stress. J. Exp. Bot. 62, 25992613. Fa¨ssler, E., Evangelou, M.W., Robinson, B.H., Schulin, R., 2010. Effects of indole-3-acetic acid (IAA) on sunflower growth and heavy metal uptake in combination with ethylene diamine disuccinic acid (EDDS). Chemosphere 80, 901907. Fodor, F., 2002. Physiological responses of vascular plants to heavy metals. In: Prasad, M.N.V., Strzalka, K. (Eds.), Physiology and Biochemistry of Metal Toxicity and Tolerance in Plants. Kluwer Academic, Dordrecht, UK, pp. 149177. Fox, T.C., Guerinot, M.L., 1998. Molecular biology of cation transport in plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 49, 669696. Foyer, C.H., Lopez-Delgado, H., Dat, J.F., Scott, I.M., 1997. Hydrogen peroxide and glutathione associated mechanisms of acclamatory stress tolerance and signaling. Physiol. Plant. 100, 241254. Foyer, C.H., Noctor, G., 2005. Redox homeostasis and antioxidant signaling: a metabolic interface between stress perception and physiological responses. Plant Cell 17, 18661875. Foyer, C.H., Noctor, G., 2011. Ascorbate and glutathione: the heart of the redox hub. Plant Physiol. 155, 218. Freeman, J.L., Persans, M.W., Nieman, K., Albrecht, C., Peer, W., Pickering, I.J., et al., 2004. Increased glutathione biosynthesis plays a role in nickel tolerance in Thlaspi nickel hyperaccumulators. Plant Cell 16, 21762191. Gabbrielli, R., Pandolfini, T., Espen, L., Palandri, M.R., 1999. Growth, peroxidase activity and cytological modifications in Pisum sativum seedlings to Ni21 toxicity. J. Plant Physiol. 155, 639645. Gajewska, E., Sklodowska, M., 2008. Differential biochemical responses of wheat shoots and roots to nickel stress: antioxidative reactions and proline accumulation. Plant Growth Regul. 54, 179188. Gajewska, E., Sklodowska, M., 2010. Differential effect of equal copper, cadmium and nickel concentration on biochemical reactions in wheat seedlings. Ecotoxicol. Environ. Saf. 73, 9961003. Gangwar, S., Singh, V.P., 2011. Indole acetic acid differently changes growth and nitrogen metabolism in Pisum sativum L. seedlings under chromium (VI) phytotoxicity: implication of oxidative stress. Sci. Hortic. 129, 321328. Gangwar, S., Singh, V.P., Prasad, S.M., Maurya, J.N., 2010. Modulation of manganese toxicity in Pisum sativum L. seedlings by kinetin. Sci. Hortic. 126, 467474. Gangwar, S., Singh, V.P., Srivastava, P.K., Maurya, J.N., 2011a. Modification of chromium (VI) phytotoxicity by exogenous gibberellic acid application in Pisum sativum (L.) seedlings. Acta Physiol. Plant 33, 13851397. Gangwar, S., Singh, V.P., Prasad, S.M., Maurya, J.N., 2011b. Differential responses of pea seedlings to indole acetic acid under manganese toxicity. Acta Physiol. Plant 33, 451462. Garzoń, T., Gunsé, B., Moreno, A.R., Tomos, A.D., Barcelo´, J., Poschenrieder, C., 2011. Aluminium-induced alteration of ion homeostasis in root tip vacuoles of two maize varieties differing in Al tolerance. Plant Sci. 180, 709715. Gemrotová, M., Kulkarni, M.G., Stirk, W.A., Strnad, M., Van Staden, J., Spıćhal, L., 2013. Seedlings of medicinal plants treated with either a cytokinin antagonist (PI-55) or an inhibitor of cytokinin degradation (INCYDE) are protected against the negative effects of cadmium. Plant Growth Regul. 71, 137145.

240


Gest, N., Gautier, H., Stevens, R., 2013. Ascorbate as seen through plant evolution: the rise of a successful molecule? J. Exp. Bot. 64, 3353. Ghanem, M.E., Albacete, A., Smigocki, A.C., Frébort, I., Pospı´sˇilová, H., Martıńez-Andu´jar, C., et al., 2011. Root-synthesized cytokinins improve shoot growth and fruit yield in salinized tomato (Solanum lycopersicum L.) plants. J. Exp. Bot. 62, 125140. Gill, S.S., Hasanuzzaman, M., Nahar, K., Macovei, A., Tuteja, N., 2013. Importance of nitric oxide in cadmium stress tolerance in crop plants. Plant Physiol. Biochem. 63, 254261. Gondim, F.A., Gomes-Filho, E., Costa, J.H., Mendes Alencar, N.L., Prisco, J.T., 2012. Catalase plays a key role in salt stress acclimation induced by hydrogen peroxide pretreatment in maize. Plant Physiol. Biochem. 56, 6271. Guan, Z.Q., Chai, T.Y., Zhang, Y.X., Xu, J., Wei, W., 2009. Enhancement of Cd tolerance in transgenic tobacco plants overexpressing a Cd-induced catalase cDNA. Chemosphere 76, 623630. Gusman, G.S., Oliveira, J.A., Farnese, F.S., Cambraia, J., 2013. Arsenate and arsenite: the toxic effects on photosynthesis and growth of lettuce plants. Acta Physiol. Plant 35, 12011209. Ha, S., Vankova, R., Yamaguchi-Shinozaki, K., Shinozaki, K., Phan Tran, L.S., 2012. Cytokinins: metabolism and function in plant adaptation to environmental stresses. Trends Plant Sci. 17, 172179. Hadi, F., Bano, A., Fuller, M.P., 2010. The improved phytoextraction of lead (Pb) and the growth of maize (Zea mays L.): the role of plant growth regulators (GA3 and IAA) and EDTA alone and in combinations. Chemosphere 80, 457462. Hall, J.L., 2002. Cellular mechanisms for heavy metal detoxification and tolerance. J. Exp. Bot. 53, 111. Halliwell, B., Gutteridge, J.M.C., 1989. Free Radicals in Biology and Medicine. second ed. Clarendon Press, Oxford. Halliwell, B., Gutteridge, J.M.C., 1999. Free Radicals in Biology and Medicine. third ed. Oxford University Press, Oxford. Hamayun, M., Khan, S.A., Khan, A.L., Shin, J.H., Ahmad, B., Shin, D.H., et al., 2010. Exogenous gibberellic acid reprograms soybean to higher growth and salt stress tolerance. J. Agric. Food Chem. 58, 72267232. He, H., He, L., Gu, M., 2012a. Interactions between nitric oxide and plant hormones in aluminum tolerance. Plant Signal. Behav. 7, 469471. He, Y., Li, W., Lv, J., Jia, Y., Wang, M., Xia, G., 2012b. Ectopic expression of a wheat MYB transcription factor gene, TaMYB73, improves salinity stress tolerance in Arabidopsis thaliana. J. Exp. Bot. 63, 15111522. Hisamatsu, T., Koshioka, M., Kubota, S., Fujime, Y., King, R.W., Mander, L.N., 2000. The role of gibberellin in the control of growth and flowering in Matthiola incana. Physiol. Plant 109, 97105. Hong, C.Y., Chao, Y.Y., Yang, M.Y., Cheng, S.Y., Cho, S.C., Kao, C.H., 2009. NaCl-induced expression of glutathione reductase in roots of rice (Oryza sativa L.) seedlings is mediated through hydrogen peroxide but not abscisic acid. Plant Soil 320, 103115. Hossain, M.A., Asada, K., 1984. Purification of dehydroascorbate reductase from spinach and its characterization as thiol enzyme. Plant Cell Physiol. 25, 8592. Hossain, M.A., Piyatida, P., da Silva, J.A.T., Fujita, M., 2012. Molecular mechanism of heavy metal toxicity and tolerance in plants: central role of glutathione in detoxification of reactive oxygen species and methylglyoxal and in heavy metal chelation. J. Bot. Available from: http://dx.doi.org/10.1155/2012/872875. Hsu, Y.T., Kao, C.H., 2004. Cadmium toxicity is reduced by nitric oxide in rice leaves. Plant Growth Regul. 42, 227238. Huang, C., He, W., Guo, J., Chang, X., Su, P., Zhang, L., 2005. Increased sensitivity to salt stress in an ascorbate-deficient Arabidopsis mutant. J. Exp. Bot. 422, 30413049. Iqbal, M., Ashraf, M., 2013. Gibberellic acid mediated induction of salt tolerance in wheat plants: growth, ionic partitioning, photosynthesis, yield and hormonal homeostasis. Environ. Exp. Bot. 86, 7685.

References

241

Iqbal, N., Nazar, R., Khan, M.I.R., Masood, A., Khan, N.A., 2011. Role of gibberellins in regulation of sourcesink relations under optimal and limiting environmental conditions. Curr. Sci. 100, 9981007. Ishikawa, T., Casini, A.F., Nishikimi, M., 1998. Molecular cloning and functional expression of rat liver glutathione-dependent dehydroascorbate reductase. J. Biol. Chem. 273, 2870828712. Izosimova, A., 2005. Modelling the interaction between calcium and nickel in the soilplant system. FAL Agric. Res. 288, 99. Jeon, J., Kim, N.Y., Kim, S., Kang, N.Y., Novák, O., Ku, S.J., et al., 2010. A subset of cytokinin twocomponent signaling system plays a role in cold temperature stress response in Arabidopsis. J. Biol. Chem. 285, 2337123386. Jiménez, A., Hernández, J.A., del Rıó, L.A., Sevilla, F., 1997. Evidence for the presence of the ascorbateglutathione cycle in mitochondria and peroxisomes of pea leaves. Plant Physiol. 114, 275284. Kalinowska, R., Pawlik-Skowrońska, B., 2010. Response of two terrestrial green microalgae (Chlorophyta, Trebouxiophyceae) isolated from Cu-rich and unpolluted soils to copper stress. Environ. Pollut. 158, 27782785. Kanazawa, S., Sano, S., Koshiba, T., Ushimaru, T., 2000. Changes in antioxidative in cucumber cotyledons during natural senescence: comparison with those during dark-induced senescence. Plant Physiol. 109, 211216. Karpinska, B., Karlsson, M., Schinkel, H., Streller, S., Su¨ss, K.H., Melzer, M., et al., 2001. A novel superoxide dismutase with a high isoelectric point in higher plants. Expression, regulation, and protein localization. Plant Physiol. 126, 16681677. Kim, S.G., Lee, A.K., Yoon, H.K., Park, C.M., 2008. A membrane-bound NAC transcription factor NTL8 regulates gibberellic acid-mediated salt signaling in Arabidopsis seed germination. Plant J. 55, 7788. Koprivova, A., North, K.A., Kopriva, S., 2008. Complex signaling network in regulation of adenosine 50 -phosphosulfate reductase by salt stress in Arabidopsis roots. Plant Physiol. 146, 14081420. Krishnamurthy, A., Rathinasabapathi, B., 2013. Auxin and its transport play a role in plant tolerance to arsenite-induced oxidative stress in Arabidopsis thaliana. Plant Cell Environ. 36, 18381849. Kwon, S.Y., Jeong, Y.J., Lee, H.S., Kim, J.S., Cho, K.Y., Allen, R.D., et al., 2002. Enhanced tolerances of transgenic tobacco plants expressing both superoxide dismutase and ascorbate peroxidase in chloroplasts against methyl viologen-mediated oxidative stress. Plant Cell Environ. 25, 873882. Laspina, N.V., Groppa, M.D., Tomaro, M.L., Benavides, M.P., 2005. Nitric oxide protects sunflower leaves against Cd-induced oxidative stress. Plant Sci. 169, 323330. Latifi, A., Ruiz, M., Zhang, C.C., 2009. Oxidative stress in cyanobacteria. FEMS Microbiol. Rev. 33, 258278. Lee, S.H., Ahsan, N., Lee, K.W., Kim, D.H., Lee, D.G., Kwak, S.S., et al., 2007. Simultaneous overexpression of both Cu/Zn superoxide dismutase and ascorbate peroxidase in transgenic tall fescue plants confers increased tolerance to a wide range of abiotic stresses. J. Plant Physiol. 164, 16261638. Leyser, Q., 2010. The power of auxin in plants. Plant Physiol. 154, 501505. Li, X., Chanroj, S., Wu, Z., Romanovsky, S.M., Harper, J.F., Sze, H., 2008. A distinct endosomal Ca21/Mn21 pump affects root growth through the secretory process. Plant Physiol. 147, 16751689. Li, X., Yang, Y., Jia, L., Chen, H., Wei, X., 2013. Zinc-induced oxidative damage, antioxidant enzyme response and proline metabolism in roots and leaves of wheat plants. Ecotoxicol. Environ. Saf. 89, 150157. Liang, W.H., Li, L., Zhang, F., Liu, Y.X., Li, M.M., Shi, H.H., et al., 2013. Effects of abiotic stress, light, phytochromes and phytohormones on the expression of OsAQP, a rice aquaporin gene. Plant Growth Regul. 69, 2127.

242


Lone, M.I., He, Z., Stoffella, P.J., Yang, X., 2008. Phytoremediation of heavy metal polluted soils and water: progress and perspectives. J. Zhejiang Univ. Sci. B 9, 210220. Mahanty, S., Kaul, T., Pandey, P., Reddy, R.A., Mallikarjuna, G., Reddy, C.S., et al., 2012. Biochemical and molecular analyses of copperzinc superoxide dismutase from a C4 plant Pennisetum glaucum reveals an adaptive role in response to oxidative stress. Gene 505, 309317. Maheshwari, R., Dubey, R.S., 2009. Nickel-induced oxidative stress and the role of antioxidant defence in rice seedlings. Plant Growth Regul. 59, 3749. Mallick, S., Sinam, G., Sinha, S., 2011. Study on arsenate tolerant and sensitive cultivars of Zea mays L.: differential detoxification mechanism and effect on nutrients status. Ecotoxicol. Environ. Saf. 74, 13161324. Martret, B.L., Poage, M., Shiel, K., Nugent, G.D., Dix, P.J., 2011. Tobacco chloroplast transformants expressing genes encoding dehydroascorbate reductase, glutathione reductase, and glutathione-S-transferase, exhibit altered anti-oxidant metabolism and improved abiotic stress tolerance. Plant Biotechnol. J. 9, 661673. Matsuoka, M., 2003. Gibberellin signaling: how do plant cells respond to GA signals? J. Plant Growth Regul. 22, 123125. McBride, M.B., 2003. Toxic metals in sewage sludge-amended soils: has proportion of beneficial use discounted the risks? Adv. Environ. Res. 8, 519. Mehlhorn, H., Lelandais, M., Korth, H.G., Foyer, C.H., 1996. Ascorbate is the natural substrate for plant peroxidases. FEBS Lett. 378, 203206. Mendoza-Co´zatl, D.G., Jobe, T.O., Hauser, F., Schroeder, J.I., 2011. Long-distance transport, vacuolar sequestration, tolerance, and transcriptional responses induced by cadmium and arsenic. Curr. Opin. Plant Biol. 14, 554562. Meng, H., Hua, S., Shamsi, I.H., Jilani, G., Li, Y., Jiang, L., 2009. Cadmium-induced stress on the seed germination and seedling growth of Brassica napus L., and its alleviation through exogenous plant growth regulators. Plant Growth Regul. 58, 4759. Meng, Y., Ma, X., Chen, D., Wu, P., Chen, M., 2010. MicroRNA-mediated signaling involved in plant root development. Biochem. Biophys. Res. Commun. 393, 345349. Merewitz, E.B., Du, H., Yu, W., Liu, Y., Gianfagna, T., Huang, B., 2012. Elevated cytokinin content in ipt transgenic creeping bentgrass promotes drought tolerance through regulating metabolite accumulation. J. Exp. Bot. 63, 13151328. Michael, P.I., Krishnaswamy, M., 2011. The effect of zinc stress combined with high irradiance stress on membrane damage and antioxidative response in bean seedlings. Environ. Exp. Bot. 74, 171177. Mills, R.F., Doherty, M.L., Lopéz-Marqués, R.L., Weimar, T., Dupree, P., et al., 2008. ECA3, a Golgi localized P2A-type ATPase, plays a crucial role in manganese nutrition in Arabidopsis. Plant Physiol. 146, 116128. Molas, J., 2002. Changes of chloroplast ultrastructure and total chlorophyll concentration in cabbage leaves caused by excess of organic Ni(II) complexes. Environ. Exp. Bot. 47, 115126. Mullineaux, P.M., Creissen, G.P., 1997. Glutathione reductase: regulation and role in oxidative stress. In: Scandalios, J. (Ed.), Oxidative Stress and the Molecular Biology of Antioxidant Defenses. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY, pp. 667713. Munzuroglu, O., Zengin, F.K., 2006. Effect of cadmium on germination, coleoptile and root growth of barley seeds in the presence of gibberellic acid and kinetin. J. Environ. Biol. 27, 671677. Myouga, F., Hosoda, C., Umezaw, T., Iizumi, H., Kuromori, T., Motohashid, R., et al., 2008. A heterocomplex of iron superoxide dismutases defends chloroplast nucleoids against oxidative stress and is essential for chloroplast development in Arabidopsis. Plant Cell 20, 31483162. Mu¨ller-Moulá, P., Havaux, M., Niyogi, K.K., 2003. Zeaxanthin deficiency enhances the high light sensitivity of an ascorbate-deficient mutant of Arabidopsis. Plant Physiol. 133, 748760.

References

243

Nagajyoti, P.C., Lee, K.D., Sreekanth, T.V.M., 2010. Heavy metals, occurrence and toxicity for plants: a review. Environ. Chem. Lett. 8, 199216. Nakano, Y., Asada, K., 1998. Hydrogen peroxidase scavenged by ascorbate specific peroxidase in spinach chloroplast. Plant Cell Physiol. 22, 867880. Nam, Y.-J., Tran, L.-S.P., Kojima, M., Sakakibara, H., Nishiyama, R., Shin, R., 2012. Regulatory roles of cytokinins and cytokinin signaling in response to potassium deficiency in Arabidopsis. PLoS ONE 7 (10), e47797. Nelson, N., 1999. Metal-ion transporters and homeostasis. EMBO J. 18, 43614371. Nishiyama, R., Watanabe, Y., Fujita, Y., Le, D.T., Kojima, M., Werner, T., et al., 2011. Analysis of cytokinin mutants and regulation of cytokinin metabolic genes reveals important regulatory roles of cytokinins in drought, salt and abscisic acid responses, and abscisic acid biosynthesis. Plant Cell 23, 21692183. Noctor, G., Foyer, C.H., 1998. Ascorbate and glutathione: keeping active oxygen under control. Annu. Rev. Plant Physiol. Plant Mol. Biol. 49, 249279. Noctor, G., Veljovic-Jovanovic, S., Foyer, C.H., 2000. Peroxide processing in photosynthesis: antioxidant coupling and redox signalling. Philos. Trans. R. Soc. B Biol. Sci. 355, 14651475. Ortiz, D.F., Ruscitti, T., McCue, K.F., Ow, D.W., 1995. Transport of metal-binding peptides by HMT1, a fission yeast ABC-type vacuolar membrane protein. J. Biol. Chem. 270, 47214728. Park, J.E., Park, J.Y., Kim, Y.S., Staswick, P.E., Jeon, J., Yun, J., et al., 2007. GH3-mediated auxin homeostasis links growth regulation with stress adaptation response in Arabidopsis. J. Biol. Chem. 282, 1003610046. Pasternak, T., Potters, G., Caubergs, R., Janse, M.A.K., 2005. Complementary interactions between oxidative stress and auxins control plant growth responses at plant, organ, and cellular level. J. Exp. Bot. 56, 19912001. Peleg, Z., Reguera, M., Tumimbang, E., Walia, H., Blumwald, E., 2011. Cytokinin-mediated source/sink modifications improve drought tolerance and increase grain yield in rice under water-stress. Plant Biotechnol. J. 9, 747758. Perilli, S., Moubayidin, L., Sabatini, S., 2010. The molecular basis of cytokinin function. Curr. Opin. Plant Biol. 13, 2126. Peto, A., Lehotai, N., Lozano-Juste, J., Leoń, J., Tari, I., Erdei, L., et al., 2011. Involvement of nitric oxide and auxin in signal transduction of copper-induced morphological responses in Arabidopsis seedlings. Ann. Bot. 108, 449457. Pilon, M., Abdel-Ghany, S.E., Cohu, C.M., Gogolin, K.A., Ye, H., 2006. Copper cofactor delivery in plant cells. Curr. Opin. Plant Biol. 9, 256263. Pilon, M., Cohu, C.M., Ravet, K., Abdel-Ghany, S.E., Gaymard, F., 2009. Essential transition metal homeostasis in plants. Curr. Opin. Plant Biol. 12, 347357. Pilon-Smits, E.A.H., Zhu, Y.L., Sears, T., Terry, N., 2000. Overexpression of glutathione reductase in Brassica juncea: effects on cadmium accumulation and tolerance. Physiol. Plant 110, 455460. Pinto, E., Sigaud-Kutner, T.C.S., Leitaõ, M.A.S., Okamoto, O.K., Morse, D., Colepicolo, P., 2003. Heavy metal-induced oxidative stress in algae. J. Phycol. 39, 10081018. ˙ Piotrowska-Niczyporuk, A., Bajguz, A., Zambrzycka, E., Godlewska-Zyłkiewicz, B., 2012. Phytohormones as regulators of heavy metal biosorption and toxicity in green alga Chlorella vulgaris (Chlorophyceae). Plant Physiol. Biochem. 52, 5265. Porter, J.R., Sheridan, R.P., 1981. Inhibition of nitrogen fixation in Alfalfa by arsenate, heavy metals, fluoride, and simulated acid rain. Plant Physiol. 68, 143148. Prasad, S.M., Zeeshan, M., 2005. UV-B radiation and cadmium induced changes in growth, photosynthesis, and antioxidant enzymes of cyanobacterium Plectonema boryanum. Biol. Plant 49, 229236. Prasad, S.M., Dwivedi, R., Zeeshan, M., 2005. Growth, photosynthetic electron transport, and antioxidant responses of young soybean seedlings to simultaneous exposure of nickel and UV-B stress. Photosynthetica 43, 177185.

244


Puig, S., Penãrrubia, L., 2009. Placing metal micronutrients in context: transport and distribution in plants. Curr. Opin. Plant Biol. 12, 299306. Purdy, D., Park, S.F., 1994. Cloning, nucleotide sequence and characterization of a gene encoding O22 dismutase from Campylobacter jejuni and Campylobacter coli. Microbiology 140, 12031208. Qin, F., Kodaira, K.S., Maruyama, K., Mizoi, J., Phan Tran, L.S., Fujita, Y., et al., 2011. SPINDLY, a negative regulator of gibberellic acid signaling, is involved in the plant abiotic stress response. Plant Physiol. 157, 19001913. Quint, M., Gray, W.M., 2006. Auxin signaling. Curr. Opin. Plant Biol. 9, 448453. Ratkevicius, N., Correa, J.A., Moenne, A., 2003. Copper accumulation, synthesis of ascorbate and activation of ascorbate peroxidase in Enteromorpha compressa (L.) Grev. (Chlorophyta) from heavy metal-enriched environments in northern Chile. Plant Cell Environ. 26, 15991608. Rea, P.A., Li, Z.S., Lu, Y.P., Drozdowicz, Y.M., Martinoia, E., 1998. From vacuolar GS-X pumps to multispecific ABC transporters. Annu. Rev. Plant Physiol. Plant Mol. Biol. 49, 727760. ` lvarez, R., Ortega-Villasante, C., A ` lvarez-Fernández, A., del Campo, F.F., Hernández, L.E., 2006. Rellán-A Stress responses of Zea mays to cadmium and mercury. Plant Soil 279, 4150. Rendon, J.L., Pardo, J.P., Mendoza-Hernandez, G., Rojo-Dominguez, A., Hernandez-Arana, A., 1995. Denaturing behavior of glutathione reductase from cyanobacterium Spirulina maxima in guanidine hydrochloride. Arch. Biochem. Biophys. 318, 264270. Requejo, R., Tena, M., 2005. Proteome analysis of maize roots reveals that oxidative stress is a main contributing factor to plant arsenic toxicity. Phytochemistry 66, 15191528. Rivero, R.M., Shulaev, V., Blumwald, E., 2009. Cytokinin-dependent photorespiration and the protection of photosynthesis during water deficit. Plant Physiol. 150, 15301540. Rivero, R.M., Gimeno, J., Van Deynze, A., Walia, H., Blumwald, E., 2010. Enhanced cytokinin synthesis in tobacco plants expressing PSARK::IPT prevents the degradation of photosynthetic protein complexes during drought. Plant Cell Physiol. 51, 19291941. Rodriguez, E., Santos, C., Azevedo, R., Moutinho-Pereira, J., Correia, C., Dias, M.C., 2012. Chromium (VI) induces toxicity at different photosynthetic levels in pea. Plant Physiol. Biochem. 53, 94100. Rouhier, N., Lemaire, S.D., Jacquot, J.P., 2008. The role of glutathione in photosynthetic organisms: emerging functions for glutaredoxins and glutathionylation. Annu. Rev. Plant Biol. 59, 143166. Rubio, M.I., Escrig, I., Martıńez-Cortina, C., Lo´pez-Benet, F.J., Sanz, A., 1994. Cadmium and nickel accumulation in rice plants. Effects on mineral nutrition and possible interactions of abscisic and gibberellic acids. Plant Growth Regul. 14, 151157. Rubio-Wilhelmi, M.M., Sanchez-Rodriguez, E., Rosales, M.A., Begonã, B., Riosa, J.J., Romero, L., et al., 2011. Effect of cytokinins on oxidative stress in tobacco plants under nitrogen deficiency. Environ. Exp. Bot. 72, 167173. Salin, M.L., 1988. Toxic oxygen species and protective systems of the chloroplast. Physiol. Plant 72, 681689. Salt, D.E., Rauser, W.E., 1995. Mg ATP-dependent transport of phytochelatins across the tonoplast of oat roots. Plant Physiol. 107, 12931301. Salt, D.E., Wagner, G.J., 1993. Cadmium transport across tonoplast of vesicles from oat roots. J. Biol. Chem. 268, 1229712302. Sancenon, V., Puig, S., Mira, H., Thiele, D.J., Penarrubia, L., 2003. Identification of a copper transporter family in Arabidopsis thaliana. Plant Mol. Biol. 51, 577587. Schickler, H., Caspi, H., 1999. Response of antioxidative enzymes to nickel and cadmium stress in hyperaccumulator plants of the genus Alyssum. Physiol. Plant 105, 3944. Schwechheimer, C., 2008. Understanding gibberellic acid signaling—are we there yet? Curr. Opin. Plant Biol. 11, 915.

References

245

Schu¨tzendu¨bel, A., Polle, A., 2002. Plant responses to abiotic stresses: heavy metal-induced oxidative stress and protection by mycorrhization. J. Exp. Bot. 53, 13511365. Semane, B., Dupae, J., Cuypers, A., Jean-Paul, N., Tuomainen, M., Tervahauta, A., et al., 2010. Leaf proteome responses of Arabidopsis thaliana exposed to mild cadmium stress. J. Plant Physiol. 167, 247254. Shah, K., Kumar, R.G., Verma, S., Dubey, R.S., 2001. Effect of cadmium on lipid peroxidation, superoxide anion generation and activities of antioxidant enzymes in growing rice seedlings. Plant Sci. 161, 11351144. Shakya, K., Chettri, M.K., Sawidis, T., 2008. Impact of heavy metals (copper, zinc, and lead) on the chlorophyll content of some mosses. Arch. Environ. Contam. Toxicol. 54, 412421. Shanker, A.K., Pathmanabhan, G., 2004. Speciation dependent antioxidative response in roots and leaves of sorghum (Sorghum bicolor (L.) Moench cv CO 27) under Cr(III) and Cr(VI) stress. Plant Soil 265, 141151. Shanker, A.K., Djanaguiraman, M., Sudhagar, R., Chandrashekar, C.N., Pathmanabhan, G., 2004. Differential antioxidative response of ascorbate glutathione pathway enzymes and metabolites in chromium speciation stress in green gram roots. Plant Sci. 166, 10351043. Shanmugam, V., Tsednee, M., Yeh, K.C., 2012. Zinc tolerance induced by iron 1 reveals the importance of glutathione in the cross-homeostasis between zinc and iron in Arabidopsis thaliana. Plant J. 69, 10061017. Shao, R., Wang, K., Shangguan, Z., 2010. Cytokinin-induced photosynthetic adaptability of Zea mays L. to drought stress associated with nitric oxide signal: probed by ESR spectroscopy and fast OJIP fluorescence rise. J. Plant Physiol. 167, 472479. Sharaf, A.E.M.M., Farghal, I.I., Sofy, M.R., 2009. Role of gibberellic acid in abolishing the detrimental effects of Cd and Pb on broad bean and Lupin plants. Res. J. Agric. Biol. Sci. 5, 668673. Sharma, P., Dubey, R.S., 2005. Lead toxicity in plants. Braz. J. Plant Physiol. 17, 3552. Sharma, R.K., Agrawal, M., Marshall, F.M., 2008. Heavy metal (Cu, Zn, Cd and Pb) contamination of vegetables in urban India: a case study in Varanasi. Environ. Pollut. 154, 254263. Shi, X., Gupta, S., Rashotte, A.M., 2012. Solanum lycopersicum cytokinin response factor (SlCRF) genes: characterization of CRF domain-containing ERF genes in tomato. J. Exp. Bot. 63, 973982. Shigeoka, S., Ishikawa, T., Tamoi, M., Miyagawa, Y., Takeda, T., Yabuta, Y., et al., 2002. Regulation and function of ascorbate peroxidase isoenzymes. J. Exp. Bot. 53, 13051319. Shri, M., Kumar, S., Chakrabarty, D., Trivedi, P.K., Mallick, S., Misra, P., et al., 2009. Effect of arsenic on growth, oxidative stress, and antioxidant system in rice seedlings. Ecotoxicol. Environ. Saf. 72, 11021110. Siddiqui, M.H., Al-Whaibi, M.H., Basalah, M.O., 2011. Interactive effect of calcium and gibberellin on nickel tolerance in relation to antioxidant systems in Triticum aestivum L. Protoplasma 248, 503511. Singh, A., Prasad, S.M., 2011. Reduction of heavy metal load in food chain: technology assessment. Rev. Environ. Sci. Biotechnol. 10, 199214. Singh, A., Sharma, R.K., Agrawal, M., Marshall, F.M., 2010. Health risk assessment of heavy metals via dietary intake of foodstuffs from the wastewater irrigated site of a dry tropical area of India. Food Chem. Toxicol. 48, 611619. Singh, H.P., Batish, D.R., Kohli, R.K., Arora, K., 2007. Arsenic-induced root growth inhibition in mung bean (Phaseolus aureus Roxb.) is due to oxidative stress resulting from enhanced lipid peroxidation. Plant Growth Regul. 53, 6573. Singh, H.P., Batish, D.R., Kaur, G., Arora, K., Kohli, R.K., 2008. Nitric oxide (as sodium nitroprusside) supplementation ameliorates Cd toxicity in hydroponically grown wheat roots. Environ. Exp. Bot. 63, 158167. Singh, N., Ma, L.Q., Vu, J.C., Raj, A., 2009. Effects of arsenic on nitrate metabolism in arsenic hyperaccumulating and nonhyperaccumulating ferns. Environ. Pollut. 157, 23002305.

246


Singh, R.P., Agrawal, M., 2010. Variations in heavy metal accumulation, growth and yield of rice plants grown at different sewage sludge amendment rates. Ecotoxicol. Environ. Saf. 73, 632641. Singh, V.P., Tripathi, D.K., Kumar, D., Chauhan, D.K., 2011. Influence of exogenous silicon addition on aluminium tolerance in rice seedlings. Biol. Trace Elem. Res. 144, 12601274. Singh, R., Srivastava, P.K., Singh, V.P., Dubey, G., Prasad, S.M., 2012a. Light intensity determines the extent of mercury toxicity in the cyanobacterium Nostoc muscorum. Acta Physiol. Plant 34, 11191131. Singh, V.P., Srivastava, P.K., Prasad, S.M., 2012b. Impact of low and high fluence rates of UV-B radiation on growth and oxidative stress in Phormidium foveolarum and Nostoc muscorum under copper toxicity: differential display of antioxidants system. Acta Physiol. Plant 34, 22252239. Sinha, S., Saxena, R., Singh, S., 2005. Chromium induced lipid peroxidation in the plants of Pistia stratiotes L: role of antioxidants and antioxidant enzymes. Chemosphere 58, 595604. Smirnoff, N., 1993. The role of active oxygen in the response of plants to water deficit and desiccation. New Phytol. 125, 2758. Srivastava, G., Kumar, S., Dubey, G., Mishra, V., Prasad, S.M., 2012. Nickel and ultraviolet-B stresses induce differential growth and photosynthetic responses in Pisum sativum L. seedlings. Biol. Trace Elem. Res. 149, 8696. Srivastava, S., Srivastava, A.K., Suprasanna, P., D’Souza, S.E., 2013. Identification and profiling of arsenic stress-induced microRNAs in Brassica juncea. J. Exp. Bot. 64, 303315. Sun, S., Wang, H., Yu, H., Zhong, C., Zhang, X., Peng, J., et al., 2013. GASA14 regulates leaf expansion and abiotic stress resistance by modulating reactive oxygen species accumulation. J. Exp. Bot. 64, 16371647. Takeshima, Y., Takatsugu, N., Sugiura, M., Hagiwara, H., 1994. High-level expression of human O2 dismutase in the cyanobacterium Anacystis nidulans 6301. Proc. Nat. Acad. Sci. USA 91, 96859689. Talke, I.N., Hanikenne, M., Kra¨mer, U., 2006. Zinc-dependent global transcriptional control, transcriptional deregulation, and higher gene copy number for genes in metal homeostasis of the hyperaccumulator Arabidopsis halleri. Plant Physiol. 142, 148167. Temmerman, L.D., Ruttens, A., Waegeneers, N., 2012. Impact of atmospheric deposition of As, Cd and Pb on their concentration in carrot and celeriac. Environ. Pollut. 166, 187195. Thomas, J.C., Perron, M., LaRosa, P.C., Smigocki, A.C., 2005. Cytokinin and the regulation of a tobacco metallothionein-like gene during copper stress. Physiol. Plant 123, 262271. Thounaojam, T.C., Panda, P., Mazumdar, P., Kumar, D., Sharma, G.D., Sahoo, L., et al., 2012. Excess copper induced oxidative stress and response of antioxidants in rice. Plant Physiol. Biochem. 53, 3339. Tounekti, T., Hernández, I., Mu¨ller, M., Khemira, H., Munné-Bosch, S., 2011. Kinetin applications alleviate salt stress and improve the antioxidant composition of leaf extracts in Salvia officinalis. Plant Physiol. Biochem. 49, 11651176. Tseng, M.J., Liu, C.W., Yiu, J.C., 2007. Enhanced tolerance to sulfur dioxide and salt stress of transgenic Chinese cabbage plants expressing both superoxide dismutase and catalase in chloroplasts. Plant Physiol. Biochem. 45, 822833. Tuna, A.L., Kaya, C., Dikilitas, M., Higgs, D., 2008. The combined effects of gibberellic acid and salinity on some antioxidant enzyme activities, plant growth parameters and nutritional status in maize plants. Environ. Exp. Bot. 62, 19. Vanhoudt, N., Vandenhove, H., Horemans, N., Wannijn, J., Bujanic, A., Vangronsveld, J., et al., 2010. Study of oxidative stress related responses induced in Arabidopsis thaliana following mixed exposure to uranium and cadmium. Plant Physiol. Biochem. 48, 879886. Veljovic-Jovanovic, S.D., Pignocchi, C., Noctor, G., Foyer, C.H., 2001. Low ascorbic acid in the vtc-1 mutant of Arabidopsis is associated with decreased growth and intracellular redistribution of the antioxidant system. Plant Physiol. 127, 426435.

References

247

Verbruggen, N., Hermans, C., Schat, H., 2009. Mechanisms to cope with arsenic or cadmium excess in plants. Curr. Opin. Plant Biol. 12, 364372. Vernoux, T., Wilson, R.C., Seeley, K.A., Reichheld, J.P., Muroy, S., Brown, S., et al., 2000. The root meristemless1/cadmium sensitive2 gene defines a glutathione-dependent pathway involved in initiation and maintenance of cell division during postembryonic root development. Plant Cell 12, 97110. Vodnik, D., Gaberscik, A., Gogala, N., 1999. Lead phytotoxicity in Norway spruce (Picea abies (L.) Karst.): the effect of Pb and zeatin-riboside on root respiratory potential. Phyton (Horn, Austria) 39, 155159. Wang, C., Tian, Y., Wang, X., Geng, J., Jiang, J., Yu, H., et al., 2010. Lead-contaminated soil induced oxidative stress, defense response and its indicative biomarkers in roots of Vicia faba seedlings. Ecotoxicology 19, 11301139. Wang, J., Zhang, H., Allen, R.D., 1999. Overexpression of an Arabidopsis peroxisomal ascorbate peroxidase gene in tobacco increases protection against oxidative stress. Plant Cell Physiol. 40, 725732. Washko, P.W., Welch, R.W., Dhariwal, K.R., Wang, Y., Levine, M., 1992. Ascorbic acid and dehydro-ascorbic acid analyses in biological samples. Anal. Biochem. 204, 114. Wilkinson, S., Kudoyarova, G.R., Veselov, D.S., Arkhipova, T.N., Davies, W.J., 2012. Plant hormone interactions: innovative targets for crop breeding and management. J. Exp. Bot. 63, 34993509. Willekens, H., Chamnongpol, S., Davey, M., Schraudner, M., Langebartels, C., Van Montagu, M., et al., 1997. Catalase is a sink for H2O2 and is indispensable for stress defence in C3 plants. EMBO J. 16, 48064816. Wu, F.B., Zhang, G.P., Dominy, P., Wu, H.X., Bachir, D.M.L., 2007. Differences in yield components and kernel Cd accumulation in response to Cd toxicity in four barley genotypes. Chemosphere 70, 8392. Xia, J., Yamaji, N., Kasai, T., Ma, J.F., 2010. Plasma membrane-localized transporter for aluminum in rice. Proc. Natl. Acad. Sci. USA 107, 1838118385. Xu, Q.M., Chen, H., 2011. Antioxidant responses of rice seedlings to Ce41 under hydroponic cultures. Ecotoxicol. Environ. Saf. 74, 16931699. Xu, Y., Gianfagna, T., Huang, B., 2010. Proteomic changes associated with expression of a gene (ipt) controlling cytokinin synthesis for improving heat tolerance in a perennial grass species. J. Exp. Bot. 61, 32733289. Yadav, S.K., 2010. Heavy metals toxicity in plants: an overview on the role of glutathione and phytochelatins in heavy metal stress tolerance of plants. S. Afr. J. Bot. 76, 167179. Yamaguchi, K., Mori, H., Nishimura, M., 1995. A novel isoenzyme of ascorbate peroxidase localized on glyoxysomal and leaf peroxisomal membranes in pumpkin. Plant Cell Physiol. 36, 11571162. Yan, D.Y., Lo, I.M., 2013. Removal effectiveness and mechanisms of naphthalene and heavy metals from artificially contaminated soil by iron chelate-activated persulfate. Environ. Pollut. 178, 1522. Ye, W.L., Wood, B.A., Stroud, J.L., Andralojc, P.J., Raab, A., McGrath, S.P., et al., 2010. Arsenic speciation in phloem and xylem exudates of castor bean. Plant Physiol. 154, 15051513. Yin, L., Wang, S., Eltayeb, A.E., Uddin, M.I., Yamamoto, Y., Tsuji, W., et al., 2010. Overexpression of dehydroascorbate reductase, but not monodehydroascorbate reductase, confers tolerance to aluminum stress in transgenic tobacco. Planta 231, 609621. Yoshimura, K., Yabuta, Y., Ishikawa, T., Shigeoka, S., 2000. Expression of spinach ascorbate peroxidase isoenzymes in response to oxidative stresses. Plant Physiol. 123, 223234. Zhang, F.Q., Wang, Y.S., Lou, Z.P., Dong, J.D., 2007. Effect of heavy metal stress on antioxidative enzymes and lipid peroxidation in leaves and roots of two mangrove plant seedlings (Kandelia candel and Bruguiera gymnorrhiza). Chemosphere 67, 4450. Zhang, W.H., Tyerman, S.D., 1999. Inhibition of water channels by HgCl2 in intact wheat root cells. Plant Physiol. 120, 849857.

248


Zheng, L., Peer, T., Seybold, V., Lu¨tz-Meindl, U., 2012. Pb-induced ultrastructural alterations and subcellular localization of Pb in two species of Lespedeza by TEM-coupled electron energy loss spectroscopy. Environ. Exp. Bot. 77, 196206. Zhou, Z.S., Huang, S.Q., Guo, K., Mehta, S.K., Zhang, P.C., Yang, Z.M., 2007. Metabolic adaptations to mercury-induced oxidative stress in roots of Medicago sativa L. J. Inorg. Biochem. 101, 19. Zhu, X.F., Jiang, T., Wang, Z.W., Lei, G.J., Shi, Y.Z., Li, G.X., et al., 2012. Gibberellic acid alleviates cadmium toxicity by reducing nitric oxide accumulation and expression of IRT1 in Arabidopsis thaliana. J. Hazard. Mater. 239-240, 302307. Zhu, Y.L., Pilon-Smits, E.A.H., Jouanin, L., Terry, N., 1999a. Overexpression of glutathione synthetase in Indian mustard enhances cadmium accumulation and tolerance. Plant Physiol. 119 (1), 73180. Zhu, Y.L., Pilon-Smits, E.A.H., Tarun, A.S., Weber, S.U., Jouanin, L., Terry, N., 1999b. Cadmium tolerance and accumulation in Indian mustard is enhanced by overexpressing γ-glutamylcysteine synthetase. Plant Physiol. 121, 11691177.

CHAPTER

Reactive Nitrogen Species and the Role of NO in Abiotic Stress

11

´ ´ Jan Sumaira, Nad’a Wilhelmova, ´ Daniela Pavlı´kova´ and Jiˇrina Szakov ´ Dagmar Prochazkov a, a´

11.1 Introduction In 1772 Joseph Priestley characterized nitric oxide (NO) as a colorless, nonflammable, odorless, and toxic gas. After the industrial revolution, this compound was studied solely as a component of air pollution because NO is involved in ozone layer destruction and in acid rain (Corpas et al., 2008a). The interest of biologists gained special momentum when this molecule was identified as a potent endogenous vasodilator (Schmidt and Walter, 1994). With the finding that NO has many functions in mammalian cells, such as regulation of vascular tone, neuronal signaling, or immune response to infection (Knowles and Moncada, 1994), various studies have reported its presence in the plant kingdom as well. Nitric oxide produced by plants was first observed by Klepper (1979) in soybean plants treated with photosynthetic inhibitor herbicides or other chemicals, as well as under dark and anoxic conditions. Mounting evidence has proved NO to be involved in many plant physiological and metabolic processes, including adaptation to environmental stresses (Uchida et al., 2002). Because of its participation in numerous biotic and abiotic responses, NO has been proposed even as a general stress molecule (Gould et al., 2003).

11.2 The reactive nitrogen species Nitric oxide may react with superoxide radicals forming peroxynitrite (ONOO2) (Kissner et al., 1997). ONOO2 also may be produced by the enzyme nitrate reductase (NR) in the presence of oxygen and NAD(P)H (Yamasaki and Sakihama, 2000). ONOO2 is a powerful oxidant that can react with DNA, lipids, and proteins under physiological conditions, resulting in cellular damage and cytotoxicity (Radi, 2004; Szabo´ et al., 2007). This molecule may protonate, as a result of which peroxynitrous acid is formed, a source of nitrogen dioxide (NO2) and hydroxyl radicals (Wendehenne et al., 2001). NO can perform important post-translational protein modifications also through nitration and S-nitrosylation. Nitration is a general chemical process for the introduction of a nitro group NO2 into a chemical compound. Although there are several amino acids that are preferentially nitrated, such as tyrosine, tryptophan, cysteine, and methionine, most studies done consider tyrosine nitration. This process consists of the addition of a nitro group to one of two equivalent orthocarbons of the aromatic P. Ahmad (Ed): Emerging Technologies and Management of Crop Stress Tolerance, Volume 2. DOI: http://dx.doi.org/10.1016/B978-0-12-800875-1.00011-9 © 2014 Elsevier Inc. All rights reserved.

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ring of tyrosine residues (Corpas et al., 2009). Tyrosine nitration has been shown to be competent to change the function of a protein in the following ways: (1) gain of function, as well as no effect on function; and (2) inhibition of function, which is a much more common result of protein tyrosine nitration (Radi, 2004). In plants, the latest data hint that nitrotyrosine may serve as a marker of nitrosative stress during abiotic stress in the same way as protein carbonylation or lipid peroxidation does (e.g., Wilhelmová et al., 2006; Valderrama et al., 2007; Corpas et al., 2008a; Chaki et al., 2009). S-nitrosylation refers to the binding of an NO group to an SH group in a cysteine residue; it plays a significant role in NO-mediated signaling (Stamler et al., 2001). Proteins exhibit a striking differential susceptibility to S-nitrosylation; however, in this respect, their overall content of cysteines is not important (Wang et al., 2006). In plants, many proteins are S-nitrosylated under physiological or stress conditions. These observations led to the first insights into S-nitrosylationdependent regulation of protein function (Lindermayr and Durner, 2009). In plant systems, S-nitrosylation of proteins was found to contribute to gene regulation (Serpa et al., 2007; Ferrarini et al., 2008; Palmieri et al., 2008; Tada et al., 2008) and modulates phytohormonal signaling (Melotto et al., 2006) and cell death (Hara et al., 2005; Belenghi et al., 2007; Holtgrefe et al., 2008). The remarkable specificity of S-nitrosylation is conferred by different factors such as the subcellular compartmentalization of NO sources and the target protein (Hess et al., 2005). S-nitrosoglutathione is a nitric oxide-derived molecule generated by the interaction of NO with reduced glutathione (GSH) during S-nitrosylation, or by a process of transnitrosation from other nitrosothiols (RSNOs) with GSH (Corpas et al., 2013). The reaction appears to take place either through the formation of N2O3 or the addition of NO to a glutathionyl radical formed during this reaction (Broniowska et al., 2013). RSNOs, especially GSNO, may serve both as an intracellular NO deposit and as a transporter for NO throughout the cell (Singh et al., 1996a,b). The formation of RSNOs indicates the reaction of nitrosonium with a thiol group present in free cysteine, peptides, or proteins (Carver et al., 2005; Dahm et al., 2006; Sun et al., 2006; Chaki et al., 2009). These compounds carry out important biological reactions such as NO release, transnitrosation, S-thiolation, as well as direct actions (Hogg, 2000; Stamler et al., 2001). Under physiological conditions, RSNOs are considered to provide protection against cellular damage induced by oxidative and nitrosative stress (Liu et al., 2004; Sun et al., 2006; Valderrama et al., 2007; Chaki et al., 2009). The enzyme GSNO reductase (GSNOR) can regulate the cellular level of GSNO and therefore NO content via the NADH-dependent reduction of GSNO to oxidized glutathione (GSSG) and NH3, and in this way, the content of overall RSNO (Liu et al., 2001; Lamotte et al., 2005). In microbes and in mammal cells, GSNOR may play a dual role: (1) turning off GSNO-derived NO signaling and (2) cellular protection against nitrosative stress by controlling excess S-nitrosylation (Liu et al., 2001; Sakamoto et al., 2002).

11.3 Drought stress From the point of view of plant productivity, it is especially important to address drought stress. It causes several interlinked physiological consequences that are deleterious to plant cells, organs, and/or tissues. One of them is the overproduction of the reactive oxygen species (ROS), including superoxide anion, hydrogen peroxide, singlet oxygen, and hydroxyl radicals.

11.4 Waterlogging stress

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Drought promoted NO production in pea, beat, tobacco, rice, cucumber, and grapevine plants (Gould et al., 2003; Kolbert et al., 2005; Arasimowicz-Jelonek et al., 2009; Patakas et al., 2010; Xiong et al., 2012). Hao et al. (2008) noted that both NO synthase (NOS)-like activity and the rate of NO release increased substantially under dehydration stress. They suggested that NO dependence on NOS-like activity serves as a signaling component in the induction of protective responses and is associated with drought tolerance in maize seedlings. On the contrary, the activation state and maximal extractable activity of the important NO producer, NR, declined rapidly in response to drought (Foyer et al., 1998). Similarly, NR activity was significantly higher under an optimal water regime than in drought stress conditions (Kroëk et al., 2008). Correlation among signal molecules of abscisic acid (ABA), H2O2, and NO was confirmed by several reports. It has been shown that NO selectively activates intracellular Ca21 channels in broad bean (Vicia faba) guard cells via a cGMP/cADPR-dependent signaling pathway, disentangling the participation of NO as a signaling molecule in the ABA-induced stomatal closure (Durner et al., 1998; Garcıá-Mata and Lamattina, 2003). In Arabidopsis guard cells, NR-mediated NO synthesis was sensitive to ABA treatment, and was required for stomatal closure induced by ABA (Desikan et al., 2004). In addition, ABA synthesis in wheat roots in response to water deficiency was much higher in the presence of NO donors and ROS, which suggests synergistic action of ROS and NO (Zhao et al., 2001). As a confirmation of this fact, the increase of ABA accumulation was blocked after the addition of ROS scavengers and NOS inhibitor. The accumulation of NO also proved to be necessary in bean stomata during ABA-induced stomata closure (Garcıá-Mata and Lamattina, 2003). Exogenously applied NO donor sodium nitroprusside (SNP) reduced water loss from detached wheat leaves and decreased transpiration rate, ion leakage, and induced stomatal closure, while a specific NO scavenger suppressed all these NO actions (Garcıá-Mata and Lamattina, 2001). Liao et al. (2012) showed that SNP improved the photosynthetic performance of leaves and alleviated the negative effects of drought on carbohydrate and nitrogen accumulation in marigold (Tagetes erecta L.). Exogenously applied NO improved drought tolerance in cucumber, maize, and rice. It has been suggested that increased antioxidant protection, which scavenges ROS, facilitated better cellular membrane stability and maintained photosynthesis and water status (Hao et al., 2008; Arasimowicz-Jelonek et al., 2009; Farooq et al., 2009). Accumulation of proline is one of the well-known adaptive responses of plants against drought stress. Exogenous application of NO alleviated osmotic stress by decreasing oxidative damage and by stimulation of proline accumulation in wheat (Tan et al., 2008). On the contrary, Xiong et al. (2012) demonstrated that although drought stress induces a simultaneous accumulation of NO and proline, NO is expendable for accumulation of proline in rice leaves. Therefore, they excluded the eventuality that NO plays a downstream role for ABA in drought-induced proline accumulation in rice leaves.

11.4 Waterlogging stress In nature, plants are often exposed to transient or permanent waterlogging. Waterlogging, designated also as flooding, drastically influences a majority of the soil physicochemical properties, most of all soil redox potential, pH and O2 levels. Thus, conditions of hypoxia (the reduction of O2 below the optimal level) or anoxia (the complete lack of O2) are commonly encountered by plant

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roots. These O2 restrictive conditions significantly influence plant development, growth, and survival (Parent et al., 2008). Waterlogging substantially promotes NO production (Sui et al., 2010). Within 12 days of waterlogging, NO production, NR, and NOS activities increased first, then decreased subsequently in Malus hupehensis roots. Similarly, Sairam et al. (2012) reported increased NO production and NR activity in V. luteola during flooding. Hypoxic stress activated NR leading to an increase of NO synthesis and higher NO emission from plant tissues (Perazzolli et al., 2006). In plant roots, two different types of NR are known: one is located in the cytosol (cNR) and the other is attached to the plasma membrane that faces the apoplast (Sto¨hr and Ullrich, 1997; Sto¨hr and Ma¨ck, 2001). In barley (Hordeum vulgare) roots, a 2.5fold activation of cNR occurred under hypoxia (Botrel and Kaiser, 1997). In root cultures of Arabidopsis, two NR genes were induced under hypoxia: NR1 gene showed mild induction after 0.5 to 4 h of hypoxia and strong induction after 20 h, while NR2 gene was strongly activated in 2 to 4 h and even more after 20 h of low oxygen conditions (Klok et al., 2002). Nitric oxide is known to be an effective inhibitor of cytochrome oxidase in the mitochondrial electron transport chain and may further reduce cell respiration and energy production (Zottini et al., 2002). The hemeproteins with the highest avidity (e.g., hexacoordinate hemoglobins) retain oxygen even under anoxic conditions, resulting in their being extremely effective NO scavengers but essentially incapable of producing NO (Igamberdiev et al., 2010). A class 1 nonsymbiotic hemoglobin (nsHbs) from Arabidopsis, barley, and alfalfa are known to detoxify NO to nitrate in an NAD(P)Hdependent manner (Seregélyes et al., 2000; Igamberdiev and Hill, 2004; Perazzolli et al., 2004). Indeed, NO accumulation, stimulated by hypoxia, was significantly suppressed in Arabidopsis plants expressing Arabidopsis class-1 nsHb in alfalfa (Medicago sativa) root cultures overexpressing barley class-1 nsHb and in maize (Zea mays) cell lines expressing the same barley nsHb (Dordas et al., 2003b; Dordas et al., 2004; Perazzolli et al., 2004). On the other hand, the transgenic lines suppressed for nsHbs expression showed increased NO concentrations (Dordas et al., 2003b; Dordas et al., 2004; Perazzolli et al., 2004). This sequence of reactions, in which NO is oxidized to nitrate, is referred to as the Hb/NO cycle (Dordas et al., 2003a). Arabidopsis class-1 nsHb is also able to metabolize GSNO through production of S-nitrosohemoglobin (Perazzolli et al., 2004). Interestingly, NO is considered to be an attractive candidate for involvement in aerenchyma formation, which is a common solution for plants exposed to waterlogging. Depending on the NO concentration and other factors, nitric oxide is able to either accelerate or inhibit apoptosis (Kim et al., 2001). The effect may be either direct, through cell necrosis, or through regulatory pathways, and it may be selective in relation to the cells that do respond (Sairam et al., 2008).

11.5 High temperature stress High temperature is an important limiting factor of crop productivity. Heat stress induces increased ROS production, oxidative stress, lipid peroxidation, enzyme inactivation, membrane injury, protein degradation, pigment bleaching, and DNA strand disruption in cells (Suzuki and Mittler, 2006). Hasanuzzaman et al. (2013) suggested that ABA may impart thermotolerance by raising the level of NO. High temperature treatment of lucerne cells resulted in an increase of NO synthesis

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(Leshem, 2001; Neill et al., 2003). Most probably the observed effects were related to the antioxidant action of NO, which elevates negative effects caused by the intensification of peroxidative metabolism under thermal stress (Neill et al., 2002). On the contrary, heat inhibited NO accumulation in cultured guard cell protoplasts of Nicotiana glauca (tree tobacco) (Beard et al., 2012). Uchida et al. (2002) showed that pretreatment with low levels of NO induced not only ROSscavenging enzyme activities but also expression of transcripts for oxidative stress-related gene encoding sucrose-phosphate synthase, Δ1pyrroline-5-carboxylate synthase, and the small heat shock protein 26 in rice seedlings. They suggested that NO can increase heat tolerance by acting as a signal molecule. Bouchard and Yamasaki (2008, 2009) suggested that heat stress-stimulated NO production could play a role in the induction of cell death by mediating an increase in caspase-like activity in Symbiodinium microadriaticum. Application of two nitric oxide donors, SNP and S-nitroso-N-acetylpenicillamine (SNAP), significantly mitigated heat stress-induced ion leakage, growth suppression, and cell viability decrease in calluses of two ecotypes of reed (Phragmites communis Trin.). H2O2 and malondialdehyde contents were decreased and the activities of superoxide dismutase (SOD), catalase (CAT), ascorbate peroxidase (APX), and peroxidase (POD) increased in both ecotypes (Song et al., 2006).

11.6 Low temperature stress A low temperature (cold stress) causes many changes in biochemical and physiological processes and ROS-homeostasis in plants (Xin and Browse, 1998; Suzuki and Mittler, 2006; Zhao et al., 2009; Siddiqui et al., 2011). Low temperature stimulated an increase of NOS and S-nitrosoglutathione reductase (GSNOR) activities. This was accompanied by an increase in the contents of NO and S-nitrosothiols, and also by an intensification of the immunoreactivity with an antibody against NO2-tyrosine (Corpas et al., 2008b). Cold acclimation induced an increase in NO production in leaves of both wild-type (WT) and mutant nitric oxide associated 1/resistant to inhibition with fosmidomycin 1 (1 AtNOA1/RIF1) A. thaliana, while the NO level in NR-defective double mutant (nia1nia2) leaves was lower compared to WT plants, although little change occurred during acclimation. Cold acclimation stimulated NR activity and induced up-regulation of NIA1 gene expression and reduced the quantity of NOA1/RIF1 protein and inhibited NOS activity. These results indicated that up-regulation of NRdependent NO synthesis underpins cold acclimation-induced NO production. Seedlings of nia1nia2 were less tolerant to freezing than WT plants. Treatment with NR inhibitor, NO scavenger, or NO donor showed that the NR-dependent NO level was positively correlated with tolerance to freezing. Further, cold acclimation up- and down-regulated expression of Δ1-pyrroline-5-carboxylate synthetase1 and proline dehydrogenase genes, respectively, resulting in enhanced accumulation of proline in WT plants. The stimulation of proline accumulation by cold acclimation was reduced by NR inhibitor and NO scavenger, while proline accumulation by cold acclimation was not affected by the NOS inhibitor. In contrast to WT plants, cold acclimation up-regulated proline dehydrogenase gene expression in nia1nia2 plants, leading to less accumulation of proline in them. These findings demonstrated that NRdependent NO production plays an important role in cold acclimation and induced an increase in freezing tolerance by modulating proline accumulation in Arabidopsis (Zhao et al., 2009).

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11.7 Salinity stress Salinity is one of the important abiotic stresses affecting plant productivity due to the alterations produced in photosynthesis and respiration, and in the metabolism of proteins and nucleic acids (Hasegawa et al., 2000). The primary effects of high salinity consist of hyperosmotic stress and ion disequilibrium that produce secondary effects such as oxidative stress (Hasegawa et al., 2000; Zhu, 2001). Increase of endogenous NO under salinity stress has been observed, for example, in tobacco leaf cell suspensions and in cotton calli (Gould et al., 2003; Vital et al., 2008). Survival of more green leaf tissue of rice seedlings under salinity stress occurred when treated with SNP; this also resulted in a higher quantum yield for photosystem (PS) II, an increase in activity of antioxidant enzymes, and the expression of specific stress-resistant genes (Uchida et al., 2002). The same NO donor promoted seed germination and root growth of yellow lupine seedlings (Kopyra and Gwo´z´ d´z, 2003) and increased the growth and dry weight of maize seedlings (Zhang et al., 2006). It has been shown that nitric oxide can serve as a signal in inducing salt resistance by increasing the cellular K:Na ratio, which is dependent on the increased plasma membrane H1-ATPase activity in calluses from reed (Phragmites communis) plants (Zhao et al., 2004) and from Populus euphratica (Zhang et al., 2007) and in maize seedlings (Zhang et al., 2006). In olive leaves, salinity stress induced the production of NO, S-nitrosoglutathione, and S-nitrosothiols, and a rise in tyrosine-nitrated proteins mainly in the vascular tissues (Valderrama et al., 2007). Thus, vascular tissues may play an important function in the redistribution of NO-derived forms during nitrosative stress and in signaling-related processes (Valderrama et al., 2007). Arabidopsis mutant Atnoa1 with an impaired in vivo NO synthase activity was more sensitive to NaCl stress compared to wild type (Guo et al., 2003; Zhao et al., 2007). When grown under NaCl stress, the WT Arabidopsis plants exhibited a higher survival rate than Atnoa1 plants and the latter plants had higher levels of hydrogen peroxide than wild-type plants (Zhao et al., 2007). In Atnoa1 plants, salt stress has been mitigated by SNP treatment, while the inhibition of nitric oxide accumulation in the WT plants produced the opposite effect (Zhao et al., 2007). Vital et al. (2008) studied the roles of superoxide and NO in the NaCl-induced up-regulation on antioxidant enzyme activities in NaCl-tolerant cotton calli. The direct addition of NO gas produced no change in the activities of CAT and GR and caused a significant decrease in APX activity when compared to the controls. When the calli was treated with SNP in the absence of NaCI stress, APX and GR activities decreased significantly and CAT activity was only slightly higher than the control. Treatment with SNP in the presence of NaCl stress resulted in a significant decrease in APX activity, and GR and APX activities were not significantly different from those observed with the NaCl treatment alone. These results suggested that NO may play a role in switching “off ” the response after other mechanisms in the cascade of events responsible for NaCl tolerance have been activated (Vital et al., 2008). Recently, Boldizsár et al. (2013) reported that modification of NO levels affected salt-induced, glutathione-dependent redox changes and simultaneously the free amino acid composition and the level of several free amino acids.

11.8 Heavy metal stress Agricultural soils in many parts of the world are contaminated by heavy metals such as Cd, Cu, Zn, Ni, Co, Cr, Pb, and As (Yadav, 2010). Among the heavy metals Fe, Mo, and Mn are important as

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micronutrients; Zn, Ni, Cu, V, Co, W, and Cr are toxic elements with high or low importance as trace elements. As, Hg, Ag, Sb, Cd, Pb, and U have no known function as nutrients and seem to be more or less toxic to plants (Goldbold and Huttermann, 1985; Nies, 1999; Saxena and Shekhawat, 2013). Several reports have suggested the following mechanisms by which NO helps plants resist heavy metal stress. (1) NO can indirectly scavenge ROS induced by heavy metals. Thus, NO might be involved in increasing the antioxidant content and antioxidative enzyme activity in plants (Hsu and Kao, 2004). (2) NO can affect root cell wall components, therefore nitric oxide may increase heavy metal accumulation in root cell walls and decrease its concentrations in the soluble fraction of plant leaves (Xiong et al., 2010). (3) NO could function as a signaling molecule in the cascade of events leading to changes in gene expression (Pagnussat et al., 2002, 2003; Garcıá-Mata and Lamattina, 2003; Wilson et al., 2008; Xiong et al., 2012).

11.8.1 Cadmium Cadmium (Cd) is one of the most toxic elements with a long biological half-life. Its presence as a pollutant in agricultural soil is mainly due to anthropogenic activities (De Michele et al., 2009). The main symptoms, in addition to others, of Cd-induced toxicity in plants are: chlorosis, altered chloroplast ultrastructure, photosynthesis inhibition, inactivation of enzymes in CO2 fixation, and induced lipid peroxidation (Gill et al., 2013). Early studies have shown that Cd inhibited NR activity in pea shoots (Hernández et al., 1997), which may result in decreased NO production. Cd induced a significant lowering of nitric oxide in the vascular tissues of pea (Barrosso et al., 2006). On the other hand, NO increased in the roots of Brassica juncea L. and Pisum sativum L. (Bartha et al., 2005) and treatment with Cd for four weeks produced a 2.4-fold increase in NO (Mahmood et al., 2009). Similarly, CdCl2 treatment of A. thaliana cell suspension cultures was accompanied by a rapid increase in NO and phytochelatin synthesis, which continued to be high as long as the cells remained viable. In addition, inhibition of NO synthesis resulted in partial prevention of hydrogen peroxide increase, expression of the marker senescence-associated gene12, and mortality, indicating that NO is actually required for Cd21-induced cell death. NO also modulated the extent of phytochelatin content, and possibly their function, by S-nitrosylation (De Michele et al., 2009). NO was also reported to be responsible for the Cd-induced growth inhibition of Arabidopsis primary roots, as well as to contribute to Cd21 toxicity by favoring Cd21 versus Ca21 uptake and by initiating a cellular pathway resembling those activated on Fe deprivation (Besson-Bard et al., 2009). Nitric oxide production under Cd stress seems to be time and concentration dependent. Treatment with 100 mM Cd for 24 h significantly decreased the NO content in the crown roots of 7-day-old rice seedlings but in the crown roots of 4-week-old rice plantlets under 0.2 mM Cd stress, the NO levels increased rapidly in the first half-hour and then began to decrease. Four h later, the NO level dropped even lower than in the control, and 24 h later, it reached its nadir (Xiong et al., 2009). Soybean cells treated with two concentrations of Cd21 showed a dose-dependent and rapid production of NO, which may suggest that NO functions as a signal molecule involved in mitigation of the heavy metal stress (Kopyra et al., 2006). Pretreatment with SNP improved Cd tolerance in Medicago truncatula roots by reducing oxidative damage, maintaining the auxin equilibrium, and increasing the accumulation of proline and glutathione (Xu et al., 2010a). When sunflower (Helianthus annuus) plants were pretreated with SNP, Cd-induced chlorophyll decay was evidently reduced: chlorophyll content remained in 88%

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of those shown by control plants (Laspina et al., 2005). In tomato plants, SNP promoted ROSscavenging enzymes, reduced accumulation of H2O2, and induced the activity of H1-ATPase and H1-pyrophosphatase in plasma membrane or tonoplast (Cui et al., 2010). Nitric oxide treatment also significantly elevated the depressed APX activity in barley seedlings during 10 and 15 days of CdCl2 treatment (Chen et al., 2010). In sunflower leaves treated with 0.5 mm Cd, APX activity increased even more—163% after application of exogenous NO (Laspina et al., 2005). NO stimulated SOD activity in Lupinus roots grown with Cd, which in roots preincubated with SNP was significantly higher (Kopyra and Gwo´z´ d´z, 2003). NO also increased the content of low-molecular antioxidant ascorbate in Cd-treated rice leaves (Hsu and Kao, 2004). Similarly, exogenous NO increased glutathione peroxidase (GPX) activity in sunflower leaves treated with Cd (Laspina et al., 2005). In contrast, a decrease in GPX and CAT activities were observed when Cd-stressed wheat roots were treated with NO (Singh et al., 2008).

11.8.2 Copper Nitric oxide increased in the adventitious roots of Panax ginseng exposed to Cu for 24 h (Tewari et al., 2008). Zhang et al. (2008) investigated the effects of various Cu concentrations and treatment times on NO concentration in Chlamydomonas reinhardtii. Their results indicated that the amount of NO increases with the duration and concentration of Cu exposure. It has been demonstrated that the addition of SNP in combination with Cu lowered the inhibition levels of carbon fixation, O2 evolution, maximum quantum yield of PSII, and significantly reduced the oxidative burst in NH41grown Chlorella (Singh et al., 2004). Tewari et al. (2008) suggested that reduction of excess Cu-induced toxicity by SNP is most likely mediated through the modulation in the activities of antioxidant enzymes involved in H2O2 detoxification (CAT, POD, APX) and in the maintenance of cellular redox couples (GR), as well as the contents of molecular antioxidants (particularly nonprotein thiol, ascorbate, and its redox status). An exogenous NO supply also improved the activity of SOD, an enzyme responsible for O22 dismutation, and NADPH oxidase, an enzyme responsible for O22 generation, in excess Cu supplied adventitious roots of Panax ginseng (Tewari et al., 2008). Hu et al. (2007) reported that NO pretreatment improved wheat seed germination and alleviated oxidative stress under Cu toxicity by increasing the activities of SOD and CAT and by decreasing the lipoxygenase activity and malondialdehyde synthesis. Singh et al. (2004) proposed that the protective effect of NO could consist of suppression of superoxide production and subsequently by suppression of hydroxyl production from superoxide and peroxynitrite.

11.8.3 Arsenic Under arsenic stress conditions, plants are subjected to different types of changes, which include element uptake and transport, metabolism, and gene expression (Catarecha et al., 2007; Verbruggen et al., 2009; Zhao et al., 2009; Guo et al., 2012; Leterrier et al., 2012). In tall fescue, the application of 100 mM SNP reduced arsenic-induced oxidative damage in leaves (Jin et al., 2010). In Arabidopsis under As treatment, NO content increased in roots and this increase was accompanied by a rise in protein tyrosine nitration in leaves (Leterrier et al., 2012), which is regarded as a marker of nitrosative stress (Corpas et al., 2008a).

11.10 Exposure to high light conditions

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S-nitrosoglutathione (GSNO) is formed by the S-nitrosylation reaction of NO with GSH. GSNO may have great physiological importance for plants since it is thought to function as a mobile reservoir of NO bioactivity (Durner and Klessig, 1999). In Arabidopsis under As conditions, GSNO content decreased. This may be due to the rise in GSNOR activity because this enzyme catalyzes the NADH-dependent reduction in GSNO to GSSG and NH3 and is thus a key player in the NO metabolism under physiological and stress conditions (Leterrier et al., 2012). Pretreatment with SNP dramatically ameliorated the As-induced decrease in the root and coleoptile lengths of rice. Nitric oxide not only exhibited ROS scavenging activity but also partially reversed the As-induced increase in the activities of the antioxidant enzymes SOD, APX, GR, and CAT (Singh et al., 2009). In tall fescue, the application of 100 mM SNP alleviated arsenic-induced electrolyte leakage and contents of malondialdehyde, hydrogen peroxide, and superoxide radical and increased activities of SOD, CAT, and POD (Jin et al., 2010).

11.8.4 Zinc Zinc, as a microelement, is essential and involved in numerous physiological processes, but at high concentrations is toxic. In roots of Solanum nigrum, Zn-induced NO production promoted an increase in ROS content by modulating the activities of NADPH oxidase (NOX) and antioxidant enzymes. Afterward, programmed cell death (PCD) was observed in primary root tips. Zn-induced NO production also influenced the number of lateral roots and root hair growth and thus modulated root system architecture and activity. These results demonstrated that NO-mediated plant responses increased Zn tolerance through morphological and physiological changes in the roots. The suplementation with NO scavengers, 2-phenyl-4,4,5,5,-tetramethylimidazoline-1-oxyl 3-oxide (PTIO), or animal NOS inhibitor L-NAME forestalled the rhizosphere acidification in response to surplus Zn, suggesting that Zn-induced NO production improves H1-ATPase activity and root system activity; therefore, it is advantageous for the plants’ response to long-term Zn toxicity. Thus, NO production and the subsequent PCD in root tips exposed to excess Zn are favorable for the S. nigrum seedling response to long-term Zn toxicity by modulating root system architecture and subsequent adaptation to Zn stress (Xu et al., 2010b).

11.9 Air pollutants Interestingly, during the 1970s, attention with regard to NO was focused on its participation in air pollution because nitric oxide contributes to acid rain and the depletion of the ozone layer. Both aspects have harmful effects on plants, the environment, and human health. For that reason, this molecule was considered “toxic” (Corpas, 2011). Air pollution studies with plants have shown that NO inhibits photosynthetic CO2 assimilation (Hill and Bennett, 1970; Bruggink et al., 1988; Takahashi and Yamasaki, 2002).

11.10 Exposure to high light conditions Light is essential for plant growth and development, but when plants are subjected to excessive light, photoinhibition occurs and ROS production increases (Asada, 2006). These events often result

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in photooxidative damages, thus light can be one of the most deleterious environmental factors (Xu et al., 2010c). For example, NO emission by NR was higher under light conditions than in the dark in sunflower plants (Rockel et al., 2002). In pea leaves, high-intensity light did not result in significant changes in NO content although NOS-like activity was significantly enhanced. High light intensity did not change GSNOR activity, but it did increase the content of RSNOs and tyrosine nitration (Corpas et al., 2008b). In the thylakoid membranes of A. thaliana, leaves adapted to growth light and subsequently, when exposed to high light, changes in the nitration level of 23 tyrosine residues in five PSI and nine PSII proteins were determined. The majority of them showed a lower nitration level in PSI and PSII complexes and supercomplexes under high light conditions, as compared to growth light. On the contrary, the nitration level significantly increased in assembled/disassembled PSI and PSII subcomplexes under high light conditions (Galetskiy et al., 2011). SNP treatment of tall fescue (Festuca arundinacea) leaves under high light stress resulted in mitigated light-induced electrolyte leakage, and in lower malondialdehyde, carbonyl, H2O2, and superoxide radical contents. At the same time, activities of SOD, CAT, and APX increased (Xu et al., 2010c).

11.11 UV-B radiation Plants, as sessile organisms that absorb sunlight to grow and develop, are inevitably exposed to ultraviolet (UV) radiation (200400 nm) that represents almost 7% of the electromagnetic radiation emitted from the Sun. The majority of UV-B radiation (280320 nm) is absorbed by stratospheric ozone but a minor proportion is transmitted to the Earth’s surface (Frohnmeyer and Staiger, 2003; Tossi et al., 2012). High doses of UV-B light induce the production of ROS, causing damage to proteins, lipids, and DNA; it also affects the plant cells’ integrity, morphology, and physiology (Frohnmeyer and Staiger, 2003; Tossi et al., 2009). Too much exposure of plants to UV-B radiation leads to an increase of ion leakage, loss of chlorophyll, and decreases the maximum efficiency of PSII photochemistry (Fv/Fm) and the quantum yield of PSII electron transport; it also increases H2O2 and thylakoid membrane protein oxidation. The endogenous NO level increased 2-fold in UV-B irradiated maize (Zea mays) leaves (Tossi et al., 2011). Xue et al. (2006) showed that UV-B radiation significantly induced NOS activity and promoted NO release as well. Similarly, NO and H2O2 contents were increased in bean (Phaseolus vulgaris) leaves. After treatment with an inhibitor of NOS (Nω-nitro-l-arginine), nitric oxide release was blocked. Application of CAT not only effectively eliminated H2O2 in the leaves but also inhibited the activity of NOS and the emission of NO. In contrast, treatment with exogenous H2O2 increased both NOS activity and NO content. Zhang and Zhao (2008) suggested that NO production was mediated by H2O2 through higher NOS activity. NR activity of silver birch leaves irradiated with UV-B significantly increased, indicating that activity is inducible by UV-B. Further, treatment of the leaves with NR inhibitor tungstate abolished UV-B-triggered NO generation, which suggests that NR may be essential for UV-B-triggered NO. Moreover, UV-B-induced NIA1 (gene encoding NR) expression coincides with UV-B-triggered NO generation and NR activity (Zhang et al., 2011). SNP pretreatment of A. thaliana seedlings recovered the UV-B inhibited root growth as compared to PTIO pretreatment. It has been shown that 24 h after UV-B irradiation the organization of

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microtubules in root epidermal cells of SNP-pretreated A. thaliana seedlings was partially recovered; with c-PTIO-pretreated ones, the organization of microtubules was not distinctly improved. Krasylenko et al. (2012) proposed that the enhanced NO levels can protect microtubule organization as well as microtubule related processes of root growth and development against disrupting effects of UV-B. Pretreatments with SNP prevented chlorophyll loss and ion leakage in UV-B-treated soybean plants (Santa-Cruz et al., 2010). SNP also permitted the survival of more green leaf tissue, preventing chlorophyll content reduction and a higher quantum yield of PSII than in nontreated controls under UV-B stress; this suggested that NO has a protective effect on chloroplast membrane in maize leaves (Kim et al., 2001). In addition, treatment with SNP decreased chlorophyll loss, abated Fv/Fm decrease, and alleviated the increase in carbonyl groups in thylakoid membrane proteins after bean UV-B irradiation (Phaseolus vulgaris) (Shi et al., 2005). SNP application also significantly increased proline content in an algal culture of Spirulina platensis (Xue et al., 2006). The important factor in plant protection against UV-B radiation is represented by flavonoidubiquitous plant secondary products that are best known as the characteristic red, blue, and purple anthocyanin pigments of plant tissues (Winkel-Shirley, 2001; Ryan et al., 2002). Given that NO is involved in secondary metabolite production, it is therefore deduced that NR should play a role in UV-B-induced flavonoid accumulation. This was confirmed by the fact that the pretreatment of silver birch leaves with NR inhibitors abolished UV-B-induced flavonoid accumulation (Zhang et al., 2011). The involvement of nitric oxide in the up-regulation of the gene encoding chalcone synthase in response to UV-B exposure was shown by spraying A. thaliana plants with PTIO or L-NAME. Both prevented the induction of chalcone synthase expression, indicating that up-regulation of chalcone synthase by UV-B requires NO (Mackerness et al., 2001). Nitric oxide donor SNP up-regulated the expression of three transcription factors involved in the phenylpropanoid (as flavonoids and synapate esters) biosynthesis pathway and, consequently, the expression of chalcone synthase and chalcone isomerase. The activation of this signaling pathway resulted in an increase of flavonoid and anthocyanin content (Tossi et al., 2011). In addition, maize leaves pretreated with the specific NO scavenger, cPTIO, do not accumulate NO and flavonoids in response to UV-B (Tossi et al., 2011).

11.12 Conclusion and future prospects It is obvious that NO, a simple molecule, plays a significant role in a wide spectrum of plant responses to various abiotic stresses. With progress in the genomic and more recently proteomic access, it will be possible to define not only the NO-regulated genes but also downstream targets of nitric oxide. The identification of proteins as potential targets for nitration and S-nitrosylation in plants under various abiotic stresses will contribute to advances in the regulatory functions of NO in plants.

Acknowledgments This work was supported by the Grant Agency of the Czech Republic, Grant No. P501/11/1239.

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References Arasimowicz-Jelonek, M., Floryszak-Wieczorek, J., Kubiˇs, J., 2009. Interaction between polyamine and nitric oxide signaling in adaptive responses to drought in cucumber. J. Plant Growth Regul. 28, 177186. Asada, K., 2006. Production and scavenging of reactive oxygen species in chloroplasts and their functions. Plant Physiol. 141, 391396. Barrosso, J.B., Corpas, F.J., Carreras, A., Rodrı´guez-Serrano, M., Esteban, F.J., Fernández-Ocanã, A., et al., 2006. Localization of S-nitrosoglutathione and expression of S-nitrosoglutathione reductase in pea plants under cadmium stress. J. Exp. Bot. 57, 17851793. Bartha, B., Kolbert, Z., Erdei, L., 2005. Nitric oxide production induced by heavy metals in Brassica juncea L. Czern. and Pisum sativum L. Acta Biol. Szeged. 49, 912. Beard, R.A., Anderson, D.J., Bufford, J.L., Tallman, G., 2012. Heat reduces nitric oxide production required for auxin-mediated gene expression and fate determination in Nicotiana glauca guard cell protoplasts. Plant Physiol. 159, 16081623. Belenghi, B., Romero-Puertas, M.C., Vercammen, D., Brackenier, A., Inze, D., Delledonne, M., et al., 2007. Metacaspase activity of Arabidopsis thaliana is regulated by S-nitrosylation of a critical cysteine residue. J. Biol. Chem. 282, 13521358. Besson-Bard, A., Gravot, A., Richaud, P., Auroy, P., Duc, C., Gaymard, F., et al., 2009. Nitric oxide contributes to cadmium toxicity in Arabidopsis by promoting cadmium accumulation in roots and by up-regulation genes related to iron uptake. Plant Physiol. 149, 13021315. ´ ., Simon-Sarkadi, L., Szirtes, K., Soltéy, A., Szalai, G., Keyster, M., et al., 2013. Nitric oxide Boldizsár, A affects salt-induced changes in free amino acid levels in maize. J. Plant Physiol. 170, 10201027. Botrel, A., Kaiser, W.M., 1997. Nitrate reductase activation state in barley roots in relation to the energy and carbohydrate status. Planta 201, 496501. Bouchard, J.N., Yamasaki, H., 2008. Heat stress stimulates nitric oxide production in Symbiodinium microadriaticum: a possible linkage between nitric oxide and the coral bleaching phenomenon. Plant Cell Physiol. 49, 641652. Bouchard, J.N., Yamasaki, H., 2009. Implicaton of nitric oxide in the heat-stress-induced cell death of the symbiotic alga Symbiodinium microadriaticum. Mar. Biol. 156, 22092220. Broniowska, K.A., Diers, A.R., Hogg, N., 2013. S-Nitrosoglutathione. Biochim. Biophys. Acta 1830, 31733181. Bruggink, G.T., Wolting, H.G., Dassen, J.H.A., Bus, V.G.M., 1988. The effect of nitric oxide fumigation at two CO2 concentrations on net photosynthesis and stomatal resistence of tomato (Lycopersicon lycopersicum L. cv. Abunda). New Phytol. 110, 185191. Carver, J., Doctor, A., Zaman, K., Gaston, B., 2005. S-nitrosothiol formation. Methods Enzymol. 396, 95105. Catarecha, P., Segura, M.D., Franco-Zorrilla, J.M., Garcıá-Ponce, B., Lanza, M., Solano, R., et al., 2007. A mutant of the Arabidopsis phosphate transporter PHT1;1 displays enhanced arsenic accumulation. Plant Cell 19, 11231133. Chaki, M., Fernández-Ocanã, A.M., Valderrama, R., Carreras, A., Esteban, F.J., Luque, F., et al., 2009. Involvement of reactive nitrogen and oxygen species (RNS and ROS) in sunflower-mildew interaction. Plant Cell Physiol. 50, 265279. Chen, F., Wang, F., Sun, H., Cai, Y., Mao, W., Zhang, G., et al., 2010. Genotype dependent effect of exogenous nitric oxide on Cd-induced changes in antioxidative metabolism. Growth Regul. 29, 394408. Corpas, F.J., 2011. The two sides of nitric oxide (NO). How a pollutant becomes a good friend for plants and animals. EnviroNews 17.

References

261

Corpas, F.J., del Rıó, L.A., Barroso, J.B., 2008a. Post-translational modifications mediated by reactive nitrogen species. Plant Signal. Behav. 3, 301303. Corpas, F.J., Chaki, M., Fernández-Ocanã, A., Valderrama, R., Palma, J.M., Carreras, A., et al., 2008b. Metabolism of reactive nitrogen species in pea plants under abiotic stress conditions. Plant Cell Physiol. 49, 17111722. Corpas, F.J., Chaki, M., Leterrier, M., Barroso, J.B., 2009. Protein tyrosine nitration. A new challenge in plants. Plant Signal. Behav. 10, 920923. Corpas, F.J., Alché, J.D., Barroso, J.B., 2013. Current overview of S-nitrosoglutathione (GSNO) in higher plants. Trends Plant Sci. 4, 13. Cui, X.M., Zhang, Y.K., Wu, X.B., Liu, C.S., 2010. The investigation of the alleviated effect of copper toxicity by exogenous nitric oxide in tomato plants. Plant Soil Environ. 56, 274281. Dahm, C.C., Moore, K., Murphy, M.P., 2006. Persistent S-nitrosilation of complex I and the other mitochondrial membrane proteins by nitrosothiols but not nitric oxide of peroxinitrite: implication for the interaction of nitric oxide with mitochondria. J. Biol. Chem. 281, 1005610065. De Michele, R., Vurro, E., Rigo, C., Costa, A., Elviri, L., Di Valentino, M., et al., 2009. Nitric oxide is involved in cadmium-induced programmed cell death in Arabidopsis suspension cultures. Plant Physiol. 150, 217228. Desikan, R., Cheung, M.-K., Bright, J., Henson, D., Hancock, J.T., Neill, S.J., 2004. ABA, hydrogen peroxide and nitric oxide signalling in stomatal guard cells. J. Exp. Bot. 55, 205212. Dordas, C., Hasinoff, B.B., Igamberdiev, A.U., Manach, N., Rivoal, J., Hill, R.D., 2003a. Expression of stressinduced hemoglobin affects NO levels produced by alfalfa root cultures under hypoxic stress. Plant J. 35, 763770. Dordas, C., Rivoal, J., Hill, R.D., 2003b. Plant hemoglobins, nitric oxide and hypoxic stress. Ann. Bot. 91, 173178. Dordas, C., Hasinoff, B.B., Rivoal, J., Hill, R.D., 2004. Class-I hemoglobins, nitrate and NO levels in anoxic maize cell-suspension cultures. Planta 219, 6672. Durner, J., Klessig, D.F., 1999. Nitric oxide as a signal in plants. Curr. Opin. Plant Biol. 2, 369374. Durner, J., Wendenhenne, D., Klessig, D.F., 1998. Defence gene induction in tobacco by nitric oxide, cyclic GMP, and cyclic ADP-ribose. Proc. Natl. Acad. Sci. USA 95, 1032810333. Farooq, M., Wahid, A., Kobayashi, N., Fujita, D., Basr, S.M.A., 2009. Plant drought stress: effects, mechanisms and management. Agron. Sustain. Dev. 29, 185212. Ferrarini, A., De Stefano, M., Baudouin, E., Pucciariello, C., Polverari, A., Puppo, A., et al., 2008. Expression of Medicago truncatula genes responsive to nitric oxide in pathogenic and symbiotic conditions. Mol. Plant Microbe Inter. 21, 781790. Foyer, C.H., Valadier, M.H., Migge, A., Becker, T.W., 1998. Drought-induced effects on nitrate reductase activity and mRNA and on the coordination of nitrogen and carbon metabolism in maize leaves. Plant Physiol. 117, 283292. Frohnmeyer, H., Staiger, D., 2003. Ultraviolet-B radiation-mediated responses in plants. Balancing damage and protection. Plant Physiol. 133, 14201428. Galetskiy, D., Lohscheide, J.N., Kononikhin, A.S., Popov, I.A., Nikolaev, E.N., Adamska, I., 2011. Phosphorylation and nitration levels of photosynthetic proteins are conversely regulated by light stress. Plant Mol. Biol. 77, 461473. Garcıá-Mata, C., Lamattina, L., 2001. Nitric oxide induces stomatal closure and enhances the adaptive plant responses against drought stress. Plant Physiol. 126, 11961204. Garcıá-Mata, C., Lamattina, L., 2003. Abscisic acid, nitric oxide and stomatal closure—is nitrate reductase one of the missing links? Trends Plant Sci. 8, 2026.

262


Gill, S.S., Hasanuzzaman, M., Nahar, K., Macovei, A., Tuteja, N., 2013. Importance of nitric oxide in cadmium stress tolerance in crop plants. Plant Physiol. Biochem. 63, 254261. Goldbold, D.L., Huttermann, A., 1985. Effect of zinc, cadmium and mercury on root elongation of Picea abies (Karst) seedlings and the significance of these metals to forest die-back. Environ. Pollut. 38, 375381. Gould, K.S., Lamotte, O., Klinguer, A., Pugin, A., Wendehenne, D., 2003. Nitric oxide production in tobacco leaf cells: a generalized stress response? Plant Cell Environ. 26, 18511862. Guo, F.Q., Okamoto, M., Crawford, N.M., 2003. Identification of a plant nitric oxide synthase gene involved in hormonal signaling. Science 302, 100103. Guo, J., Xu, W., Ma, M., 2012. The assembly of metals chelation by thiols and vacuolar compartmentalization conferred increased tolerance to and accumulation of cadmium and arsenic in transgenic Arabidopsis thaliana. J. Hazard. Mater. 199200, 309313. Hao, G., Xing, Y., Zhang, J., 2008. Role of nitric oxide dependence on nitric oxide synthase-like activity in the water stress signaling of maize seedling. J. Integr. Plant Biol. 50, 435442. Hara, M.R., Agrawal, N., Kim, S.F., Cascio, M.B., Fujimuro, M., Ozeki, Y., et al., 2005. S-nitrosylated GAPDH initiates apoptotic cell death by nuclear translocation following Siah1 binding. Nat. Cell Biol. 7, 665674. Hasanuzzaman, M., Nahar, K., Alam, M.M., Roychowdhury, R., Fujita, M., 2013. Physiological, biochemical, and molecular mechanisms of heat stress tolerance in plants. Int. J. Mol. Sci. 14, 96439684. Hasegawa, P.M., Bressan, R.A., Zhu, J.-K., Bohnert, H.J., 2000. Plant cellular and molecular responses to high salinity. Annu. Rev. Plant Physiol. Plant Mol. Biol. 51, 463499. Hernández, L.E., Garate, A., Carpena-Rviz, R., 1997. Effect of cadmium on the uptake, distribution and assimilation of nitrate in Pisum sativum. Plant Soil 189, 97106. Hess, D.T., Matsumoto, A., Kim, S.O., Marshall, H.E., Stamler, J.S., 2005. Protein S-nitrosylation: purview and parameters. Nat. Rev. Mol. Cell Biol. 6, 150166. Hill, A.C., Bennett, J.H., 1970. Inhibition of apparent photosynthesis by nitrogen oxides. Atmos. Environ. 4, 341348. Hogg, N., 2000. Biological chemistry and clinical potential of S-nitrosothiols. Free Radic. Biol. Med. 28, 14781486. Holtgrefe, S., Gohlke, J., Starmann, J., Druce, S., Klocke, S., Altmann, B., et al., 2008. Regulation of plant cytosolic glyceraldehyde 3-phosphate dehydrogenase isoforms by thiol modifications. Physiol. Plant 133, 211228. Hsu, Y.T., Kao, C.H., 2004. Cd toxicity is reduced by nitric oxide in rice leaves. Plant Growth Regul. 42, 227238. Hu, K.D., Hu, L.Y., Li, Y.H., Zhang, F.Q., Zhang, H., 2007. Protective roles of nitric oxide on germination and antioxidant metabolism in wheat seeds under copper stress. Plant Growth Regul. 53, 173183. Igamberdiev, A.U., Hill, R.D., 2004. Nitrate, NO and haemoglobin in plant adaptation to hypoxia: an alternative to classic fermentation pathway. J. Exp. Bot. 55, 24732482. Igamberdiev, A.U., Bykova, N.V., Shah, J.K., Hill, R.D., 2010. Anoxic nitric oxide cycling in plants: participating reactions and possible mechanisms. Physiol. Plant 138, 393404. Jin, J.W., Xu, Y.F., Huang, Y.F., 2010. Protective effect of nitric oxide against arsenic-induced oxidative damage in tall fescue leaves. Afr. J. Biotech. 9, 16191627. Kim, P.K., Zamora, R., Petrosko, P., Billiar, T.R., 2001. The regulatory role of nitric oxide in apoptosis. Int. Immunopharmacol. 1, 14211441. Kissner, R., Nauser, T., Bugnon, P., Lye, P.G., Koppenol, W.H., 1997. Formation and properties of peroxynitrite as studied by laser flash photolysis. Chem. Res. Toxicol. 10, 12851292. Klepper, L.A., 1979. Nitric oxide (NO) and nitrogen dioxide emissions from herbicide-treated soybean plants. Atmos. Environ. 13, 537542.

References

263

Klok, E.J., Wilson, I.W., Wilson, D., Chapman, S.C., Ewing, R.M., Somerville, S.C., et al., 2002. Expression profile analysis of the low-oxygen response in Arabidopsis root cultures. Plant Cell 14, 24812494. Knowles, R.G., Moncada, S., 1994. Nitric oxide synthases in mammals. Biochem. J. 298, 249258. Kolbert, Y., Bartha, B., Erdei, L., 2005. Generation of nitric oxide in roots of Pisum sativum, Triticum aestivum and Petroselium crispum plants under osmotic and drought stress. Acta Biol. Szegend. 49, 1316. Kopyra, M., Gwo´z´ d´z, E.A., 2003. Nitric oxide stimulates seed germination and counteracts the inhibitory effect of heavy metals and salinity on root growth of Lupinus luteus. Plant Physiol. Biochem. 41, 10111017. Kopyra, M., Stachoń-Wilk, M., Gwo´z´ d´z, E.A., 2006. Effects of exogenous nitric oxide on the antioxidant capacity of cadmium-treated soybean cell suspension. Acta Physiol. Plant 28, 525536. Krasylenko, Y.A., Yemets, A.I., Sheremet, Y.A., Blume, Y.B., 2012. Nitric oxide as a critical factor for perception of UV-B irradiation by microtubules in Arabidopsis. Plant Physiol. 145, 505515. Kroëk, M., Slamka, P., Olˇsovská, K., Brestiˇc, M., Benˇc´ıková, M., 2008. Reduction of drought stress effect in spring barley (Hordeum vulgare L.) by nitrogen fertilization. Plant Soil Environ. 54, 713. Lamotte, O., Courtois, C., Barnavon, L., Pugin, A., Wendehenne, D., 2005. Nitric oxide in plants: the biosynthesis and cell signalling properties of a fascinating molecule. Planta 221, 14. Laspina, N.V., Groppa, M.D., Tomaro, M.L., Benavides, M.P., 2005. Nitric oxide protect sunflower leaves against Cd-induced oxidative stress. Plant Sci. 169, 323330. Leshem, Y.Y., 2001. Nitric Oxide in Plants. Kluwer Academic Publishers, London, UK. Leterrier, M., Airaki, M., Palma, J.M., Chaki, M., Barroso, J.B., Corpas, F.J., 2012. Arsenic triggers the nitric oxide (NO) and S-nitrosoglutathione (GSNO) metabolism in Arabidopsis. Environ. Pollut. 166, 136143. Liao, W.B., Huang, G.B., Yu, J.H., Zhang, M.L., 2012. Nitric oxide and hydrogen peroxide alleviate drought stress in marigold explants and promote its adventitious root development. Plant Physiol. Biochem. 58, 615. Lindermayr, C., Durner, J., 2009. S-Nitrosylation in plants: pattern and function. J. Proteomics 73, 19. Liu, L., Hausladen, A., Zeng, M., Que, L., Heitman, J., Stamler, J.S., 2001. A metabolic enzyme for S-nitrosothiols conserved from bacteria to humans. Nature 410, 490494. Liu, L., Zeng, M., Zhang, J., Hanes, M.A., Ahearn, G., McMahon, T.J., et al., 2004. Essential roles of S-nitrosothiols in vascular homeostasis and endotoxic shock. Cell 116, 617628. Mackerness, S.A.-H., John, C.F., Jordan, B., Thomas, B., 2001. Early signalling components in ultraviolet-B responses: distinct roles for different reactive oxygen species and nitric oxide. FEBS Lett. 489, 237242. Mahmood, T., Gupta, K.J., Kaiser, W.M., 2009. Cadmium stress stimulates nitric oxide production by wheat roots. Pak. J. Bot. 41, 12851290. Melotto, M., Underwood, W., Koczan, J., Nomura, K., He, S.Y., 2006. Plant stomata function in innate immunity against bacterial invasion. Cell 126, 969980. Neill, S.J., Desikan, R., Clarke, A., Hurst, R.D., Hancock, J.T., 2002. Hydrogen peroxide and nitric oxide as signalling molecules in plants. J. Exp. Bot. 53, 12371247. Neill, S.J., Desikan, R., Hancock, J.T., 2003. Nitric oxide signalling in plants. New Phytol. 159, 1135. Nies, D.H., 1999. Microbial heavy-metal resistence. Appl. Microbiol. Biotechnol. 51, 730750. Pagnussat, G., Simontacchi, M., Puntarulo, S., Lamattina, L., 2002. Nitric oxide is required for root organogenesis. Plant Physiol. 129, 954956. Pagnussat, G.C., Lanteri, M.L., Lamattina, L., 2003. Nitric oxide and cyclic GMP are messengers in the indole acetic acid-induced adventitious rooting process. Plant Physiol. 132, 12411248. Palmieri, M.C., Sell, S., Huang, X., Scherf, M., Werner, T., Durner, J., et al., 2008. Nitric oxide-responsive genes and promoters in Arabidopsis thaliana: a bioinformatics approach. J. Exp. Bot. 59, 177186. Parent, C., Capelli, N., Berger, A., Crevecoeur, M., Dat, J.F., 2008. An overview of plant responses to soil waterlogging. Plant Stress 2, 2027.

264


Patakas, A.A., Zotos, A., Beis, A.S., 2010. Production, localisation and possible roles of nitric oxide in drought stressed grapevines. Aust. J. Grape Wine Res. 16, 203209. Perazzolli, M., Dominici, P., Romero-Puertas, M.C., Zago, E.D., Zeier, J., Sonoda, M., et al., 2004. Arabidopsis non-symbiotic haemoglogin AHb1 modulates nitric oxide bioactivity. Plant Cell 16, 110. Perazzolli, M., Romero-Puertas, M.C., Delledonne, M., 2006. Modulation of nitric oxide bioactivity by plant haemoglobins. J. Exp. Bot. 57, 479488. Radi, R., 2004. Nitric oxide, oxidants, and protein tyrosine nitratin. Proc. Natl. Acad. Sci. USA 101, 40034008. Rockel, P., Strube, F., Rockel, A., Wildt, J., Kaiser, W.M., 2002. Regulation of nitric (NO) production by plant nitrate reductase in vivo and in vitro. J. Exp. Bot. 53, 103110. Ryan, K.G., Swinny, E.F., Markham, K.R., Winefield, C., 2002. Flavonoid gene expression and UV photoprotection in transgenic and mutant Petunia leaves. Phytochemistry 59, 2332. Sairam, R.K., Kumutha, D., Ezhilmathi, K., Desmukh, P.S., Srivastava, G.C., 2008. Physiology and biochemistry of waterlogging tolerance in plants. Biol. Plant 52, 401412. Sairam, R.K., Dharmar, K., Chinnusamy, V., Lekshmy, S., Joshi, R., Bhattacharya, P., 2012. The role of nonsymbiotic haemeglobin and nitric oxide homeostasis in waterlogging tolerance in Vigna species. Biol. Plant 56, 528536. Sakamoto, A., Ueda, M., Morikawa, H., 2002. Arabidopsis glutathione-dependent formaldehyde dehydrogenase is an S-nitrosoglutathione reductase. FEBS Lett. 515, 2024. Santa-Cruz, D., Pacienza, N., Polizio, A., Balestrasse, K., Tomaro, M., Yannarelli, G., 2010. Nitric oxide synthase-like dependent NO production enhances heme oxygenase up-regulation in ultraviolet-B-irradiated soybean plants. Phytochemistry 71, 17001707. Saxena, I., Shekhawat, G.S., 2013. Nitric oxide (NO) in alleviation of heavy metal induced phytotoxicity and its role in protein nitration. Nitric Oxide 32, 1320. Schmidt, H.W., Walter, U., 1994. NO at work. Cell 78, 919925. Seregélyes, C., Mustardy, L., Ayaydin, F., Sass, L., Kovacs, L., Endre, G., et al., 2000. Nuclear localization of a hypoxia-inducible novel non-symbiotic hemoglobin in cultured alfalfa cells. FEBS Lett. 482, 125130. Serpa, V., Vernal, J., Lamattina, L., Grotewold, E., Cassia, R., Terenzi, H., 2007. Inhibition of AtMYB2 DNA-binding by nitric oxide involves cysteine S-nitrosylation. Biochem. Biophys. Res. Commun. 361, 10481053. Shi, S., Wang, G., Wang, Y., Zhang, L., Zhang, L., 2005. Protective effect of nitric oxide against oxidative stress under ultraviolet-B radiation. Nitric Oxide 13, 19. Siddiqui, M.H., Al-Whaibi, M.H., Basalah, M.O., 2011. Role of nitric oxide in tolerance of plants to abiotic stress. Protoplasma 248 (3), 447455. Singh, A.K., Sharma, L., Mallick, N., 2004. Antioxidative role of nitric oxide on copper toxicity to a chlorophycean alga Chlorella. Ecotoxicol. Environ. Saf. 59, 223227. Singh, H.P., Batish, D.R., Kaur, G., Arora, K., Kohli, R.H., 2008. Nitric oxide (as sodium nitroprusside) supplementation ameliorates Cd toxicity in hydroponically grown wheat roots. Environ. Exp. Bot. 63, 158167. Singh, H.P., Kaur, S., Batish, D.R., Sharma, V.P., Sharma, N., Kohli, R.K., 2009. Nitric oxide alleviates arsenic toxicity by reducing oxidative damage in the roots of Orysa sativa (Rice). Nitric Oxide 20, 289297. Singh, R.J., Hogg, N., Joseph, J., Kalyanaraman, B., 1996a. Mechanisms of nitric oxide release from S-nitrosothiols. J. Biol. Chem. 271, 1859618603. Singh, S.P., Wishnok, J.S., Keshive, M., Dee, W.M., Tannenbaum, S.R., 1996b. The chemistry of the S-nitrosoglutathione/glutathione system. Proc. Natl. Acad. Sci. USA 93, 1442814433. Song, L., Ding, W., Zhao, M.G., Sun, B.T., Zhang, L.X., 2006. Nitric oxide protects against oxidative stress under heat stress in the calluses from two ecotypes of reed. Plant Sci. 171, 449458.

References

265

Stamler, J.S., Lamas, S., Fang, F.C., 2001. Nitrosylation: the prototypic redox-based signaling mechanism. Cell 106, 675683. Sto¨hr, C., Ma¨ck, G., 2001. Diurnal changes in nitrogen metabolism of tobacco roots. J. Exp. Bot. 52, 12831289. Sto¨hr, C., Ullrich, W.R., 1997. A succinate-oxidizing nitrate reductase is located at the plasma membrane of plant roots. Planta 203, 129132. Sui, J., Yang, H.Q., Zhang, X.R., Jiang, Q.Q., Ran, K., Sun, X.L., et al., 2010. Nitric oxide production in Malus hupehensis roots under waterlogging and the effects of exogenous NaNO3 on this production. Ying Yong Sheng Tai Xue Bao 21, 13951399. Sun, J., Steenbergen, C., Murphy, E., 2006. S-Nitrosylation. NO-related redox signalling to protect against oxidative stress. Antioxid Redox Signal. 8, 16931705. Suzuki, N., Mittler, R., 2006. Reactive oxygen species and temperature stresses: a delicate balance between signaling and destruction. Physiol. Plant 126, 4551. Szabo´, C., Ischiropoulos, H., Radi, R., 2007. Peroxinitrite: biochemistry, pathophysiology and development of therapeutics. Nat. Rev. Drug Discov. 6, 662680. Tada, Y., Spoel, S.H., Pajerowska-Mukhtar, K., Mou, Z., Song, J., Wang, C., et al., 2008. Plant immunity requires conformational changes of NPR1 via S-nitrosylation and thioredoxins. Science 321, 952956. Takahashi, S., Yamasaki, H., 2002. Reversible inhibition of photophosphorylation in chloroplasts by nitric oxide. FEBS Lett. 512, 145148. Tan, J., Zhao, H., Hong, J., Han, Y., Li, H., Zhao, W., 2008. Effects of exogenous nitric oxide on photosynthesis, antioxidant capacity and proline accumulation in wheat seedlings subjected to osmotic stress. World J. Agric. Sci. 4, 307313. Tewari, R.K., Hahn, E.J., Paek, K.Y., 2008. Modulation of cooper toxicity-induced oxidative damage by nitric oxide supply in the adventitious roots of Panan ginseng. Plant Cell Rep. 27, 563573. Tossi, V., Lamattina, L., Cassia, R., 2009. An increase in the concentration of abscisic acid is critical for nitric oxide-mediated plant adaptive responses to UV-B irradiation. New Phytol. 181, 871879. Tossi, V., Amenta, M., Lamattina, L., Cassia, R., 2011. Nitric oxide enhances plant ultraviolet-B protection up-regulating gene expression of the phenylpropanoid biosynthetic pathway. Plant Cell Environ. 34, 909921. Tossi, V., Lombardo, C., Cassia, R., Lamattina, L., 2012. Nitric oxide and flavonoids are systematically induced by UV-B in maize leaves. Plant Sci. 193-194, 103109. Uchida, A., Jagendorf, A.T., Hibino, T., Takabe, T., 2002. Effects of hydrogen peroxide and nitric oxide on both salt and heat tolerance in rice. Plant Sci. 163, 515523. Valderrama, R., Corpas, F.J., Carreras, A., Fernández-Ocanã, A., Chaki, M., Luque, F., 2007. Nitrosative stress in plants. FEBS Lett. 581, 453461. Verbruggen, N., Hermans, C., Schat, H., 2009. Mechanisms to cope with arsenic or cadmium excess in plants. Curr. Opin. Plant Biol. 12, 364372. Vital, S.A., Fowler, R.W., Virgen, A., Gossett, D.R., Banks, S.W., Rodriguez, J., 2008. Opposing roles for superoxide and nitric oxide in the NaCl stress-induced upregulation of antioxidant enzyme activity in cotton callus tissue. Environ. Exp. Bot. 62, 6068. Wang, G., Moniri, N.H., Ozawa, K., Stamler, J.S., Daaka, Y., 2006. Nitric oxide regulates endocytosis by S-nitrosylation of dynamin. Proc. Natl. Acad. Sci. USA 31, 12951300. Wendehenne, D., Pugin, A., Klessig, D.F., Durner, J., 2001. Nitric oxide: comparative synthesis and signalling in animal and plant cells. Trends Plant Sci. 46, 177183. Wilhelmová, N., Wilhelm, J., Fuksová, H., My´tinová, Z., Procházková, D., Schwippelová, Z., et al., 2006. The effect of plant cytokinin hormones on the production of ethylene, nitric oxide, and protein nitrotyrosine in ageing tobacco leaves. Biofactors 27, 203211.

266


Wilson, I.D., Neill, S.J., Hancock, J.T., 2008. Nitric oxide synthesis and signalling in plants. Plant Cell Environ. 31, 622631. Winkel-Shirley, B., 2001. Flavonoid biosynthesis. A colourful model for genetics, biochemistry, cell biology, and biotechnology. Plant Physiol. 126, 485493. Xin, Z., Browse, J., 1998. Eskimol mutants of Arabidopsis are constitutively freezing-tolerant. Proc. Natl. Acad. Sci. USA 95, 77907804. Xiong, J., Fu, G., Tao, L., Zhu, C., 2010. Roles of nitric oxide in alleviating heavy metal toxicity in plants. Arch. Biochem. Biophys. 497, 1320. Xiong, J., Zhang, L., Fu, G., Yang, Y., Zhu, C., Tao, L., 2012. Drought-induced proline accumulation is uninvolved with increased nitric oxide, which alleviates drought stress by decreasing transpiration in rice. J. Plant Res. 125, 155164. Xu, J., Wang, W., Yin, H., Liu, X., Sun, H., Mi, Q., 2010a. Exogenous nitric oxide improves antioxidative capacity and reduces auxin degradation in roots of Medicago truncatula seedlings under cadmium stress. Plant Soil 326, 321330. Xu, J., Yin, H., Li, Y., Liu, X., 2010b. Nitric oxide is associated with long-term zinc tolerance in Solanum nigrum. Plant Physiol. 154, 13191334. Xu, Y., Sun, X., Jin, J., Zhou, H., 2010c. Protective effects of nitric oxide on light-induced oxidative damage in leaves of tall fescue. J. Plant Physiol. 167, 512518. Xue, L.G., Li, S.W., Xu, S.J., An, L.Z., Wang, X.L., 2006. Alleviate effects of nitric oxide on the biological damage of Spirulena platensis induced by enhanced ultraviolet-B. Wei Sheng Wu Xue Bao 46, 561564. Yadav, S.K., 2010. Heavy metals toxicity in plants: an overview on the role of glutathione and phytochelatins in heavy metal stress tolerance of plants. S. Afr. J. Bot. 76, 167179. Yamasaki, H., Sakihoma, Y., 2000. Simulataneous production of nitric oxide and peroxynitrite by plant nitrate reductase: in vitro evidence for the NR-dependent formation of active nitrogen species. FEBS Lett. 468, 8992. Zhang, F., Wang, Y., Yang, Y., Wu, H., Wang, D., Liu, J., 2007. Involvement of hydrogen peroxide and nitric oxide in salt resistence in the calluses from Populus euphratica. Plant Cell Environ. 30, 775785. Zhang, L., Zhao, L., 2008. Production of nitric oxide under ultraviolet-B irradiation is mediated by hydrogen peroxide through activation of nitric oxide synthase. J. Plant Biol. 51, 395400. Zhang, L.P., Mehta, S.K., Liu, Z.P., Yang, Z.M., 2008. Cooper induced proline synthesis is associated with nitric oxide generation in Chlamydomonas reihardtii. Plant Cell Physiol. 49, 411419. Zhang, M., Dong, J.F., Jin, H.H., Sun, L.N., Xu, M.J., 2011. UV-B-induced flavonoid accumulation in Betula pendula leaves is dependent upon nitrate reductase-mediated nitric oxide signaling. Tree Physiol. 31, 798807. Zhang, Y., Wang, L., Liu, Y., Zhang, Q., Wei, Q., Zhang, W., 2006. Nitric oxide enhances salt tolerance in maize seedlings through increasing activities of proton-pump and Na1/H1 antiport in the tonoplast. Planta 224, 545555. Zhao, L., Zhang, F., Guo, J., Yang, Y., Li, B., Zhang, L., 2004. Nitric oxide functions as a signal in salt resistence in the calluses from two ecotypes of reed. Plant Physiol. 134, 849857. Zhao, M.G., Tian, Q.Y., Zhang, W.H., 2007. Nitric oxide synthase-dependent nitric oxide production is associated with salt tolerance in Arabidopsis. Plant Physiol. 144, 206217. Zhao, M.G., Chen, L., Zhang, L.L., Zhang, W.H., 2009. Nitric reductase dependent nitric oxide production is involved in cold acclimation and freezing tolerance in Arabidopsis. Plant Physiol. 151, 755767. Zhao, R.X., Zhang, Q.B., Wu, X.Y., Wang, Y., 2001. The effects of drought on epidermal cells and stomatal density of wheat leaves. Inner Mongolia Agric. Sci. Technol. 6, 67. Zhu, J.K., 2001. Plant salt tolerance. Trends Plant Sci. 6, 835840. Zottini, M., Formentin, E., Scattolin, M., Carimi, F., Lo Schiavo, F., Terzi, M., 2002. Nitric oxide affects plant mitochondrial functionality in vivo. FEBS Lett. 515, 7578.

CHAPTER

Role of Tocopherol (Vitamin E) in Plants: Abiotic Stress Tolerance and Beyond

12

Mirza Hasanuzzaman, Kamrun Nahar and Masayuki Fujita

12.1 Introduction As a result of their sessile nature, plants are always subjected to various environmental adversities or abiotic stresses such as salinity, drought, extreme temperatures, metal toxicity, waterlogging, UV-B radiation, ozone, and so on. These are responsible for hampering the growth, physiology, and productivity of plants and thus are a challenge for global food security (Hasanuzzaman et al., 2009, 2010, 2011a,b, 2012ac, 2013a,b; 2014). Various abiotic stresses have been noted to reduce crop yield as much as 50% (Rodrı´guez et al., 2005; Acquaah, 2007). Oxidative stress caused by reactive oxygen species (ROS), such as superoxide (O2 2 ), hydrogen peroxide (H2O2), hydroxyl radical (OH•), and singlet oxygen (1O2), is common in all abiotic stresses that can cause severe damage to cells (Gill and Tuteja, 2010). By nature, plants possess an antioxidant defense system bearing nonenzymatic antioxidants such as ascorbate (AsA), glutathione (GSH), tocopherol (Toc), alkaloids, nonprotein amino acids, and others; this is in addition to antioxidant enzymes such as superoxide dismutase (SOD), catalase (CAT), ascorbate peroxidase (APX), monodehydroascorbate reductase (MDHAR), dehydroascorbate reductase (DHAR), glutathione reductase (GR), glutathione peroxidase (GPX), glutathione S-transferase (GST), and peroxidases (POX). They are located in different cell organelles and work together to keep the ROS level below a toxic limit and thus control oxidative damage (Mittler et al., 2007; Gill and Tuteja, 2010). Tocopherol exists in four different forms: alpha (α), beta (β), gamma (γ), and delta (δ). Among the antioxidants, Toc has turned out to be a universal constituent of all higher plants (Threlfall, 1971; Kamal-Eldin and Appelqvist, 1996). Unlike other antioxidants, Toc is exclusively synthesized in photosynthesizing organisms such as higher plants and algae (Hussain et al., 2013). Tocopherol biosynthesis in plants mainly occurs in the plastid (Mendes and Kell, 1997). There are two converging pathways of Toc biosynthesis that are governed by a number of enzymes. However, the accumulation of Toc greatly varies in different plant species and different plant parts as well. Several reports indicated that stress-tolerant plants exhibit an enhanced level of Toc, whereas sensitive ones show decreased levels of Toc under stressful conditions leading to oxidative damage (Smirnoff, 1993; Munné-Bosch and Alegre, 2002; Munné-Bosch, 2005). Several plant studies provided evidence that elevated levels of Toc can confer tolerance to several abiotic stresses including salinity (Ouyang et al., 2011; Farouk, 2011), drought (Cela et al., 2011; Espinoza et al., 2013); P. Ahmad (Ed): Emerging Technologies and Management of Crop Stress Tolerance, Volume 2. DOI: http://dx.doi.org/10.1016/B978-0-12-800875-1.00012-0 © 2014 Elsevier Inc. All rights reserved.

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CHAPTER 12 Role of Tocopherol (Vitamin E) in Plants

temperature extremes (Kanayama et al., 2013; Kumar et al., 2013), metal toxicity (Yusuf et al., 2010; Sanita` di Toppi et al., 2012), elevated ozone (Guo et al., 2009), and UV radiation (Munné-Bosch and Alegre, 2002). Tocopherols play vital roles in maintaining redox homeostasis. Protection of chloroplast toward a sound photosynthesis process is another vital role of Toc. In photosynthetic membranes they scavenge ROS (mainly 1O2 and OH•) and reduce lipid peroxyl radicals (LOO•) to their corresponding hydroperoxides (Maeda et al., 2005). It was evident that Toc biosynthesis increased under stressful conditions and provided better protection against oxidative stress by limiting ROS generation (Shao et al., 2008; Semchuk et al., 2009; Lushchak and Semchuk, 2012). Tocopherols were also found to positively affect seed germination and plant growth and development (Horvath et al., 2006). Their function seems to be interlinked with phytohormone functions (Munné-Bosch, 2007). Through participating in signal cascade, Toc conveys abiotic and biotic stress signals to facilitate better development and stress tolerance (Sattler et al., 2004). Environmental stress, its magnitude, and plant species are factors for the regulation of endogenous Toc. In spite of having differences, research studies on gene response and expression revealed that elevated levels of Toc conferred better stress tolerance to plants (Munné-Bosch, 2005; Semchuk et al., 2011). In addition to the relationship between endogenous Toc and stress tolerance, many studies already have proved exogenous Toc to be a successful protectant against different abiotic stresses (DeLong and Steffen, 1998; Guo et al., 2009; Skłodowska et al., 2009; Ellouzi et al., 2013; Espinoza et al., 2013). In this chapter, the roles of Toc in plants’ life process, especially under different abiotic stresses, are reviewed and discussed in the context of available literature.

12.2 Chemistry and types of tocopherol Tocopherol (Toc) is a chemical compound having vitamin E activity. Due to its activity, it was given the name “tocopherol” from the Greek words tokos (childbirth or offspring), and pherin (to bear or to carry), meaning in sum “to carry a pregnancy” with the ending -ol signifying its phenolic nature. This name was given because its activity was first identified from a dietary fertility factor in rats. The structure of vitamin E was first elucidated by Fernholz (1938). Vitamin E is a chain of organic compounds having methylated phenols. Another group of compounds related to Toc—tocotrienols—also have vitamin E activity. These (tocopherols and tocotrienols) are fat-soluble antioxidants that have diverse roles in plants and animals. Tocopherol exists in four different forms that occur in alpha (α), beta (β), gamma (γ), and delta (δ) forms. The differences among α-, β-, γ-, and δ-Toc are only due to the position and number of the methyl (2CH3) substitution(s) on the aromatic (chromanol) ring (Figure 12.1). For the chromanoxy radical (TO•) of each Toc, the OH group is replaced by the radical, O•, as shown in Figure 12.2. All features have a chromanol ring, with a hydroxyl group (2OH) that can donate a hydrogen atom (H•) to reduce free radicals and a hydrophobic side chain; this allows for penetration into biological membranes. Besides the chromanol ring, Toc has a fully saturated 16-carbon phytol tail that contains three trans-double bonds in their side chain. They have three chiral centers at carbon 2, 40 , and 80 and the naturally occurring isomers have the R-configuration

12.2 Chemistry and types of tocopherol

269

FIGURE 12.1 Chemical structure of four homologues of tocopherol.

FIGURE 12.2 Chromanoxy radical (TO•) of α-, β-, γ-, and δ-tocopherol. For α-tocopherol, R1 and R2 are replaced by CH3 and CH3; for β-tocopherol, R1 and R2 are replaced by CH3 and H; for γ-tocopherol, R1 and R2 are replaced by H and CH3; and for δ-tocopherol, R1 and R2 are replaced by H and H.

at all three positions. Toc is amphipatic in nature but differs in some biochemical properties with respect to its isoprenoid side chain. Some basic properties of the four tocopherols are presented in Table 12.1. Note specifically that the aOH group of C-6 of the chromanol ring is important in terms of the antioxidant role of Toc because it can donate H• to terminate the radical chain in the autoxidation reaction.

270


Table 12.1 Basic Chemical Properties of Four Types of Tocopherol Types

IUPAC Name

α-tocopherol

(2R)-2,5,7,8-tetramethyl-2-[(4R,8R)(4,8,12-trimethyltridecyl)]-6-chromanol (2R)-2,5,8-trimethyl-2-[(4R,8R)(4,8,12-trimethyltridecyl)]-3,4-dihydrochromen-6-ol (2R)-2,7,8-trimethyl-2-[(4R,8R)4,8,12-trimethyltridecyl]-6-chromanol (2R)-2,8-dimethyl-2-[(4R,8R)4,8,12-trimethyltridecyl]-6-chromanol

β- tocopherol γ-tocopherol δ- tocopherol

Molecular Formula

Molecular Mass (g mol21)

C29H50O2

430.71

C28H48O2

416.68

C28H48O2 C27H46O2

402.65

International Union of Pure and Applied Chemistry.

12.3 Tocopherol biosynthesis and accumulation in plants The synthesis of vitamin E (vit-E) was first reported by Karrer and his colleagues (1938), and the mechanisms or pathways of Toc biosynthesis were revealed more than 30 years ago (Grusak and DellaPenna, 1999). Unlike other antioxidants, Toc is exclusively synthesized in photosynthesizing organisms—higher plants and algae (Hussain et al., 2013). Tocopherol biosynthesis in plants mainly occurs in the plastid, and the enzymes required for Toc biosynthesis are largely associated with the plastidial envelope (Mendes and Kell, 1997). There are two converging pathways involved in Toc biosynthesis: the shikimate pathway and the methylerythrotol phosphate (MEP) pathway. The shikimate and MEP pathways are localized in cytosol and plastid, respectively. These two pathways bring the head group and the side chain building block together. In particular, the shikimate pathway is responsible for forming the aromatic ring, while the MEP pathway constructs the phytyldiphosphate (PDP) for the Toc tail, as shown in Figure 12.3. The shikimate pathway of aromatic amino acid synthesis is responsible for the derivation of the hydroquinone ring of Toc where homogentisate acts as a precursor that is formed by oxygenation of the tyrosine metabolite (p-hydroxyphenylpyruvate, HPP) by the action of p-hydroxyphenylpyruvate dehydrogenase (HPPD). A shikimate pathway consists of several steps (at least 7), where the intermediate ones come from glycolysis (phosphoenolpyruvate), and the pentose phosphate pathway (erythrose 4-phosphate) is converted into chorismate (see Figure 12.3). In these steps, several enzymes are involved but their specific role in Toc biosynthesis is still unknown (Lushchak and Semchuk, 2012). Some of the steps are inhibited by exogenous toxicants (e.g., herbicide). For example, glyphosate is a widely used herbicide that targets the enzyme 5-enolpyruvylshikimate 3-phosphate (EPSP) synthase (Herrmann, 1995; Sun et al., 2005); thus, it inhibits the formation of chorismate—the end product of the shikimate pathway—that is responsible for the synthesis of many metabolites including Toc. The first intermediate of Toc is HPP, which is derived from prephenate directly by the action of prephenate dehydrogense (PDH) or via arogenate and tyrosine. In higher plants, HPP is produced from tyrosine, which is catalyzed by tyrosine aminotransferase (TAT), which is influenced by various factors (e.g., jasmonic acid, octadecanoids, and

12.3 Tocopherol biosynthesis and accumulation in plants

271

FIGURE 12.3 Tocopherol biosynthesis in plants. Additional details can be found in the text.

caronatine) (Lopukhina et al., 2001; Sandorf and Holla¨nder-Czytko, 2002). Exogenous application of these chemicals resulted in enhanced production of Toc due to elevated enzymatic activities (Lopukhina et al., 2001; Sandorf and Holla¨nder-Czytko, 2002). This HPP is then oxygenated to homogentisate (HGA) by the activity of HPP dioxigenase—the end product that merges with the end product (phytol diphosphate) from the MEP pathway. Several steps are involved in the formation of PDP through the MEP pathway (Lushchak and Semchuk, 2012). The end product, PDP, is derived from the precursor molecules; that is, isopentenyl diphosphate (IPP) and its isomer dimethylallyl diphosphate (DMAPP) (see Figure 12.3). However, IPP is reported to be the end product of the MEP pathway in higher plants (Lichtenthaler, 2000). Further, this end product produces C20-intermediate geranylgeranyl diphosphate (GGDP) (Munné-Bosch and Alegre, 2002); it also acts as a precursor for the biosynthesis of carotenoids (CAR), tocotrienols, chl, and PDP (Ischebeck et al., 2006). As a result of the multistep reaction localized in the plastid envelope membrane, GGDP is converted into PDP, which is catalyzed by geranylgeranyl reductase (GGR) (Keller et al., 1998). It has

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been observed that the decreased activity of GGR resulted in reduced chl and Toc content in plants because of geranylgeranylated chl (Grabes et al., 2001; Tanaka et al., 1999). In higher plants, PDP also comes from the free phytol produced of the chl catabolism by chlorophyllase (CHL); this finding is supported by several reports (Valentin et al., 2006; Ischebeck et al., 2006; Lushchak and Semchuk, 2012). It is important to note that phytol is not directly used as a precursor for Toc biosynthesis. Rather, it has to be phosphorylated into phytol-phosphate (PP) and PDP by the activity of phytol kinase and phytol-phosphate kinase (PKK) (Ischebeck et al., 2006). The final process of Toc biosynthesis is the condensation of HGA with PDP, which is catalyzed by homogentisate phytyltransferase (HPT), yielding 2-methyl-6-phytyl-1,4-benzoquinone (MPBQ). MPBQ is then methylated into 2,3-dimethyl-6-phytyl-1,4-benzoquinone (DMPBQ) by the activity of MPBQ methyltransferase (MPBQ MT) (see Figure 12.3). Inspite of an inability to donate electrons, MPBQ and DMPBQ are redox active quinones, and thus bear the possibility of taking part in the same role as Toc (Leibler and Burr, 2000). MPBQ and DMPBQ produce γ- and δ-Toc, respectively, by the activity of a common enzyme, Toc cyclase (TC). These γ- and δ-tocopherols further methylate to produce α- and β-Toc, respectively, which are catalyzed by γ-Toc methyltransferase (γ-TMT) (see Figure 12.3). The biosynthesis of Toc is influenced by different factors such as plant age, the organs and organelles of plants, and other regulatory compounds (e.g., hormones) (Cella et al., 2009b). The biosynthesis of Toc is also influenced by phytohormones such as abscisic acid (ABA), salicylic acid (SA), and jasmonic acid (JA). Jasmonic acid has been reported to regulate Toc biosynthesis genes in Arabidopsis and barley (Falk et al., 2002; Sandorf and Holla¨nder-Czytko, 2002). Munné-Bosch and Alegre (2003) observed that enhanced endogenous SA can improve the synthesis of α-Toc in drought-stressed Phillyrea angustifolia. Abscisic acid was found to regulate the genes responsible for HPPD, which in turn resulted in increased biosynthesis of Toc (Munné-Bosch et al., 2007). The accumulation of Toc greatly varied in a number of plant species and different plant parts as well. The average range of Toc content is 100 to 500 mg kg21 fresh weight of normal plants with some exceptions. Oil-yielding plants (e.g., soybean, coconut, mustard/canola, sunflower, corn) are found to contain a higher amount of Toc in their tissues (Eitenmiller, 1997). The total Toc content is the highest in seed compared to other plant parts. Table 12.2 indicates the amount of α-Toc in different plant species. In seeds, Toc is normally localized in plastids; however, in some cases it was also observed in cytoplasmic lipid bodies (White et al., 2006). Generally, α-Toc is the major form of Toc in leaves, while seeds of many plants contain γ-Toc. Other forms of Toc viz. β-δ-Toc are uncommon in plants (Tan, 1989; Demurin et al., 1996; Abbasi et al., 2007; Hussain et al., 2013).

12.4 The role of tocopherol in plant growth and physiology Tocopherols play diversified roles in plant growth and physiological processes. The performance of Calendula officinalis L. plants was evaluated considering different growth and physiological parameters. Foliar spray of α-Toc (0, 50, 100 mg L21) improved vegetative growth and the flowering parameters of Calendula officinalis. The α-Toc at 100 mg L21 increased leaf area (9.48%) and fresh and dry weight of aerial parts (19.58% and 22.24%, respectively). The highest seed yield was obtained by using the same dose of α-Toc (Soltani et al., 2012). Plant height, number of branches and leaves, stem

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Table 12.2 α-Tocopherol Content in Different Cultivated Plant Species Source

Plant Organs

Usable Products

α-Toc Content (g kg21)

Wheat Sunflower Sunflower Almond Safflower Canola Walnut Peanut Palm Olive Soybean Maize Oat Coconut Asparagus Spinach Spinach Tomato Carrot Tobacco Tobacco Ficus elastic Lettuce Lettuce Maple Pine Juniper

Kernel Seed Seed Kernel Kernel Seed Fruit Seed Kernel Seed Kernel Seed Seed Seed/fruit Shoot Leaf Leaf Fruit Root Leaf Leaf Leaf Leaf Leaf Leaf Leaf Leaf

Germ Oil Kernel Oil Oil Oil Oil Edible nut Oil Oil Oil Entire grain Kernel Oil Young shoot Raw leaf Cooked leaf Raw fruit Taproot Young leaf Old leaf Fresh leaf Outer leaf Inner leaf Matured leaf Matured leaf Matured leaf

1500 610 351 392 450 270 200 172 150 120 116 20 15 10 15 20 21 9 6 57 180 301 16 9 435 118 145

´ Source: Adapted from Szymanska and Kruk (2008) and Hussain et al. (2013).

diameter, leaf area, and fresh and dry weight of Hibiscus rosa-sineses L. were significantly improved by application of α-Toc (El-Quesni et al., 2009). Application of α-Toc improved growth in Helianthus annus cultivars. It was also supposed to affect protein synthesis, senescence, and photosynthetic products, which concomitantly increased seed yield (Sadak et al., 2010). El-Bassiouny et al. (2005) noted increased growth parameters and seed yield of faba bean by use of α-Toc. The α-Toc is the most common form of Toc found in photosynthetic tissue. Presenting in the chloroplasts, it helps in quenching 1O2 or scavenging LOO• and the concomitant alleviation of oxidative damage in chloroplast (Munné-Bosch, 2007). The α-Toc increases membrane rigidity when provided with adequate fluidity and membrane function (Munné-Bosch, 2007). Besides protecting

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the photosynthetic membrane, exogenous Toc application improved the photosynthetic pigment content of several plant species. In H. rosa-sineses, chl a, chl b, and CAR were improved by different levels of α-Toc (0, 50, and 100 mg kg21) (El-Quesni et al., 2009). In Calendula officinalis L., Toc was also effective in improving chl and CAR content (Soltani et al., 2012). Faba bean plants also had increased chl a, b, and CAR content with Toc application (El-Bassiouny et al., 2005). Nonphotosynthetic tissues can have different forms of Toc. The seeds mostly contain γ-Toc, whereas flowers preferentially accumulate α-Toc. Several studies, however, described that the floral organs (e.g., sepals, carpels, petals, stamens) have different forms of Toc (Abbasi et al., 2007). Irrespective of form, Toc plays vital roles in development, signal transduction, interacting, or controlling phytohormonal regulation, senescence, and so on (Arrom and Munné-Bosch, 2010). Tocopherols have been demonstrated as important signaling molecules in several studies. The forms and levels of Toc are altered depending on plant growth stage and those perform different metabolic functions. Studies with Brassica napus, Nicotiana tabacum, and Arabidopsis thaliana of wild type and mutant revealed that the seeds of these plants have high γ-Toc content. The rates of germination in these plants were inversely correlated with the γ-Toc content of seeds. The γ-Toc, by reducing the level of nitric oxide (NO), prolonged the early development process (Desel et al., 2007). In germinating seeds and in the seedling development stage of Hordeum vulgare L. γ-Toc could control NO content and subsequent signals (Desel and Krupinska, 2005). The roles of γ-Toc were dominant during young leaves’ growth of Phaseolus coccineus (Szymańska and Kruk, 2008). It is recognized that tocopherol plays a role in plants’ nutrient translocation, accumulation, and vascular systems and in carbohydrate translocation in various plant parts through phloem (Porfirova et al., 2002; Hofius et al., 2004). Tocopherol-deficient maize and potato mutant showed ultrastructural modification and callose occlusion in plasmodesmata of the bundle sheath cell of leaf veins (Russin et al., 1996; Botha et al., 2000). Excess sugar accumulation and increased anthocyanins of source leaves with reduced growth were also characteristic features of these mutants (Russin et al., 1996; Provencher et al., 2001; Hofius et al., 2004). Soluble sugars, nitrogen, phosphorus, and potassium contents in H. rosa-sineses were enhanced significantly by α-Toc compared with untreated plants (El-Quesni et al., 2009). Sadak et al. (2010) reported that α-Toc stimulated total carbohydrate accumulation in H. annus plants. Tocopherol levels within plants are often thought to relate to aging and senescence. The levels of α- and γ-Toc were found to be higher in aged leaves of A. thaliana plants (Holla¨nder-Czytko et al., 2005). In Lilium flowers, Toc content increased as the tepal senescence increased (Arrom and Munné-Bosch, 2010). At senescence, plants are faced with severe oxidative stress that results in a rise in radicals from fatty acids; increasing Toc during senescence might be a strategy to reduce that stress. Moreover, α- and γ-Toc present in the chloroplastic membranes play vital roles in sustaining photosynthesis that may have a role in improving plant performance during senescence (Holla¨nder-Czytko et al., 2005).

12.5 Tocopherol and abiotic stress tolerance Tocopherol is an antioxidant and thus has a clear role in plants’ tolerance to abiotic stress. However, the Toc-induced stress protection is largely dependent on plant species, stress intensity, and plant

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physiological state (Munné-Bosch, 2005). The alteration of Toc concentration and its role in regulating stress tolerance are discussed in the sections that follow. Several reports indicate that stresstolerant plants exhibit an enhanced level of Toc, whereas sensitive ones showed a decreased level of Toc under stressful conditions leading to oxidative damage (Smirnoff, 1993; Munné-Bosch and Alegre, 2002; Munné-Bosch, 2005). The alteration of α-Toc in plants under stressful conditions takes places in two phases. In the first, Toc synthesis increases to eliminate ROS, leading to better protection by avoiding oxidative damage. In the second phase, net Toc loss occurs due to severe stress because of the higher degradation of Toc that exceeds its synthesis. If α-Toc scarcity cannot be reimbursed by rapid biosynthesis of supplementation from exogenous application of Toc, lipid peroxidation increases and as a consequence cell death occurs. It is important to note that in stresstolerant plants, the first phase is evident exclusively, whereas the second phase is typically evident in stress-sensitive ones (Munné-Bosch, 2005).

12.5.1 Salinity Salinity is considered a major abiotic stress that causes disruption of major physiological processes such as photosynthesis, respiration, water and nutrient uptake, antioxidant systems, toxic metabolite and ROS generation, and lipid peroxidation; all of these are responsible for hampering plant growth and development, as well as productivity (Mahajan and Tuteja, 2005; Hasanuzzaman et al., 2009, 2011a,b, 2013a,b). Because salt stress is frequent in many natural growing environments, plants try to develop several adaptive features to survive and sustain themselves (Ashraf and Harris, 2004). How these kinds of survival mechanisms are regulated by Toc was studied in a number of research works; some of which are presented here. Lycopersicon esculentum Mill plants were subjected to NaCl stress (50 and 150 mM). Salt stress increased the lipid peroxidation level, degraded chl, and altered antioxidant metabolism. A rise in Toc level in both doses of salt stress were significant, although the pattern was different in the second and fifth day of stress. Elevated GPX, GST levels were correlated to the antioxidant function of Toc during the early stage stress period, whereas its rise in the late phase was supposed to play a role in the senescence signaling pathway or recovery and recycling of the compounds required for sustaining plants’ normal behavior under stress (Skłodowska et al., 2009). Overexpression of γ-TMT—the gene for regulating conversion of γ-Toc to α-Toc—in Brassica juncea leaves increased resistance to salt stress (Yusuf et al., 2010). Spraying α-Toc in Triticum aestivum under salt stress significantly enhanced antioxidant enzyme activities and accumulates AsA, phenol, and CAR. This helped to reduce hydrogen peroxide and lipid peroxidation levels and improve membrane permeability. Reduced sodium and chloride levels and accumulation of calcium, potassium, and magnesium were also observed with α-Toc spray. Altogether this resulted in delayed senescence or conferred salt tolerance (Farouk, 2011). Several other studies also proved the positive roles of Toc toward salt stress tolerance compared to wild type, transgenic tobacco plants with low Toc that were more sensitive to salt stress. Conversely, those accumulating γ-Toc instead of α-Toc showed a higher resistance to osmotic and oxidative stress induced by salinity (Abbasi et al., 2007). Rice mutants deficient in α- and γ-Toc or their biosynthesis gene have less resistance to salt stress and overexpression of the same geneenhanced salt tolerance (Ouyang et al., 2011). In halophyte Cakile maritime, the α-Toc level was higher than in the glycophyte A. thaliana under a saline growing environment (Ellouzi et al., 2011).

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The positive roles of Toc in developing salt stress tolerance were observed in A. thaliana mutants. Tocopherols have a role in controlling the efficiency of PSII photochemistry, oxidative stress, Na1/K1 homeostasis, and hormonal balance in those rendered salt tolerant. The mutants’ lack of α-Toc and γ-Toc showed more salt sensitivity compared to the mutants lacking α-Toc only. A significant rise of H2O2 and malondialdehyde (MDA) levels with reduced shoot and root growth was prominent under salt stress and stress effects were higher in mutants that lack both α- and γ-Toc. Without these, ABA, JA, and the ethylene precursor, 1-aminocyclopropane-1-carboxylic acid, were higher in content in mutants that lack both α-Toc and γ-Toc compared to mutants lacking α-Toc (Ellouzi et al., 2013).

12.5.2 Drought Water deficiency or drought stress is one of the major causes for crop loss worldwide (Hasanuzzaman and Fujita, 2011, 2012; Alam et al., 2013; Hasanuzzaman et al., 2014), and it has been estimated that global crop production losses may be up to 30% by 2025 compared to current yields because of drought stress (Zhang, 2011). Due to its capacity to quench ROS, Toc can play a role in drought-stressed plants by dissipating excess excitation energy during photooxidative stress (Hernández et al., 2012; Espinoza et al., 2013). In addition, because Toc modulates the level of ROS and therefore the extent of lipid peroxidation, it also modulates the accumulation of polyunsaturated fatty acids (PUFA) oxidation products (oxylipins) and plays a key signaling function during drought and other stress factors (Sattler et al., 2006; Munné-Bosch et al., 2007; Cela et al., 2011). Different plant studies have indicated the positive relationship between Toc biosynthesis/accumulation and water stress (Munné-Bosch et al., 1999; Munné-Bosch and Alegre, 2003). Several reports have shown there is a remarkable elevation of α-Toc under water-deficit conditions in pea (Tanaka et al., 1990; Moran et al., 1994), wheat and cereals (Price et al., 1989; Bartoli et al., 1999), rosemary (Munné-Bosch et al., 1999), and lavender (Munné-Bosch and Alegre, 2001). Liu et al. (2008) observed that transgenic tobacco plants overexpressing the vte1 gene enhanced α-Toc synthesis resulting in better protection to water deficiency; this was also associated with upregulated antioxidant defense such as decreased lipid peroxidation, electrolyte leakage, and H2O2 levels. However, severe drought stress (30% PEG) resulted in a loss of α-Toc in rice chloroplast (Boo and Jung, 1999). In a recent report, Kumar et al. (2013) observed that α-Toc-enriched transgenic B. juncea plants constitutively overexpressing the γ-TMT gene showed enhanced tolerance to drought stress (200 mM manitol) compared to wild-type plants. Transgenic plants showed enhanced activities of SOD, CAT, APX, and GR and decreased the levels of MDA, H2O2, and electrolyte leakage compared to wild type. Hernández et al. (2004) observed a time-dependent pattern of α-Toc accumulation in Cistus clusii grown under drought stress. After a 30-d drought, no changes in α-Toc content were observed, while a 3.3-fold increase in α-Toc was observed after a 50-d drought. They also observed unchanged levels of α-Toc quinine under drought stress, indicating that there is a relationship between Toc and CAR in the control of the 1O2 level in drought-stressed C. clusii plants (Hernández et al., 2004). Different varietal responses toward Toc production under drought stress were observed by Jaleel et al. (2008). While comparing two cultivars (rosea and alba) of Catharanthus roseus, they observed that rosea showed a higher level of α-Toc compared to alba under drought conditions.

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Cela et al. (2009) investigated the effect of drought on α- and γ-Toc levels in Aptenia cordifolia (a xerophyte). Although α-Toc levels remained unchanged, the γ-Toc level increased significantly after a 4-d water shortage, which gave a maximum value after a 10-d stress and was supposed to help prevent leaf desiccation (Cela et al., 2009). Successful efforts to improve plant performance against drought through engineering Toc level and composition have been reported in the literature. In their investigation with Arabidopsis plants Cela et al. (2011) observed a 3.6- and 13.5-fold increase in the level of α- and γ-Toc, respectively, under water deficiency. However, some important genes (e.g., VTE2, VTE1, and VTE4) responsible for Toc biosynthesis did not change significantly (Cela et al., 2011). Espinoza et al. (2013) reported that tobacco seedlings overexpressing VTE2.1, which encodes the enzyme HPT, can catalyze the prenylation step in Toc biosynthesis under drought stress. The elevated level of α-Toc may enhance the photosynthetic efficiency and lower lipid peroxidation leading to better oxidative protection.

12.5.3 Extreme temperature Rising global temperatures seem to be stressful for crops all over the world, where tropical plants are more affected (Wahid et al., 2007). High-temperature stress affects plants in diverse ways at their different growth stages. One of the primary effects of rising temperature at cellular and subcellular levels is the denaturation of proteins that results in membrane damage (Liu and Huang, 2000; Kepova et al., 2005; Hasanuzzaman et al., 2013c). Inactivation of enzymes of mitochondria, chloroplasts, or other organelles cause disruption of biochemical and physiological processes (Howarth, 2005). At organizational levels, impaired photosynthesis, transpiration, nutrient transport, metabolism, translocation (Oukarroum et al., 2012), tissue chlorosis and necrosis, reduced plant growth, and senescence are frequently observed under high-temperature stress (Vollenweider and Gunhardt-Goerg, 2005; Wahid et al., 2007). Low temperature is another harmful extreme that adversely affects plants. This is a stress not only in countries with very low temperatures but also a stress for tropical countries’ plants during the winter season (Farooq et al., 2009). The effects of low temperatures, which cause substantial damage to plants, have been studied for a long time for many economically important crops at different growth stages. This stress is a matter of concern for sustaining plant growth and productivity (Nahar et al., 2009a,b; Zhou-fei et al., 2009). The tocopherol inflections in relation to temperature extremes, both high and low, have been studied in several plant species, and they reveal the positive role of Toc with regard to extreme temperature stress tolerance (Kanayama et al., 2013). Triticum aestivum seedlings were subjected to different levels of high temperature stress (25, 30, and 35 C) for 7 days. Seedlings’ performances were studied in the absence or presence of α-Toc (5 μM). Temperature stress resulted in injury to the plants: inhibition of shoot and root growth, reduced leaf water content, disruption of membrane properties, oxidative damage, impaired stomatal conductance, reduced chl content, and photochemical efficiency. The endogenous α-Toc level increased with a rise in temperature (except for the highest); this may be due to an improved internal antioxidant system. Moreover, exogenous application of α-Toc elevated its endogenous levels, which improved growth, chl content, and photochemical efficiency and reduced membrane damage. The α-Toc also improved the antioxidant defense capability as evidenced by increased activities of SOD, CAT, APX, GR, and the content of AsA, GSH, and a concomitant reduction in MDA and H2O2 content (Kumar et al., 2013). In H. annuus L., 35 C or higher temperatures elevated the level

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of Toc. By studying different substages of reproductive development, it was found that the Toc content was highest in the most sensitive substages. Thus, increasing the Toc level in sensitive growth stages initiates its protective function under high temperature stress. An increase in Toc level was also correlated with superior oil quality (Dong et al., 2007). The level of α-Toc varies according to plant type, and it is correlated with chilling tolerance. Its level increased at low temperatures in chilling-tolerant cereal leaves (Streb et al., 1999); on the other hand, its level decreased in chilling-sensitive maize (Sattler et al., 2004). At low temperature stress, Toc protects photosynthetic membranes from photooxidative stress (Maeda et al., 2006; Matringe et al., 2008). Due to cold injury induced by 10 C, oxidative stress occurred in Medicago sativa L. cv. sewa leaves. The increase of lipid peroxidation or MDA and elevated H2O2 accumulation were the sign of stress. The injury symptoms were reduced at the recovery period due to the redox properties of α-Toc, which showed their function by sequestrating free radicals. The α-Toc also provided antioxidant protection against this stress. Activities of SOD, CAT, APX, and GR increased significantly; those were correlated to higher α-Toc levels and restricted ROS (Bafeel and Ibrahim, 2008). In the Arabidopsis thaliana mutant lacking Toc biosynthetic activity, chilling stress of 4 C substantially damaged phloem loading and increased oxidative stress; however, its biosynthetic mutant showed the opposite response under low temperatures. Its phloem loading and cell wall development were better, and the photooxidative damage and photoinhibition were lower compared to the deficient mutant (Maeda et al., 2006). This finding supports the role of Toc at the gene level.

12.5.4 Metal toxicity Metal toxicity can alter biochemical and physiological events including oxidative stress (Hasanuzzaman and Fujita, 2012; Hasanuzzaman et al., 2012b; Hasanuzzaman and Fujita, 2013). The long-term effect of low doses, or a short spell of high doses of heavy metal, is enough for eventual death of the plant. Several reports demonstrated the role of Toc in metal stress tolerance. Artetxe et al. (2002) observed elevated levels of Toc in duckweed exposed to zinc (Zn) and cadmium (Cd). Similar increases of α-Toc also have been observed in lead (Pb)-treated lupin (Rucińska-Sobkowiak and Pukacki, 2006). In wheat seedlings, 50 and 100 mM nickel (Ni) for 9 d resulted in a 38% and 60% increase in Toc content in shoots (Gajewska and Skłodowska, 2007). The exposure of A. thaliana to copper (Cu) and Cd ions caused a 6- and 5-fold increase in Toc content, respectively (Collin et al., 2008). Vit-E-deficient mutant showed sensitivity to Cd21 and Cu21 (75 μM), whereas the wild type showed better growth (Collin et al., 2008). In contrast, the α-Toc level decreased under As stress (Munné-Bosch and Alegre, 2002). In a recent report, Kumar et al (2013) observed that α-Toc-enriched transgenic B. juncea plants constitutively overexpressing the γ-TMT gene showed enhanced tolerance to Cd stress (20 mM CdCl2) compared to wild-type plants. Transgenic plants showed enhanced activities of SOD, CAT, APX, and GR and decreased the levels of MDA, H2O2, and electrolyte leakage compared to wild type. However, AsA and GSH contents were lower in transgenic plants. Enhanced Toc content associated with up-regulation of the VTE3 gene was reported in the C. reinhardtii (green alga) exposed to 50 mM Cu (Luis et al., 2006). According to Yusuf et al. (2010), B. juncea plants grown under CdCl2 (20 mM) showed 1.5- and 9.3-fold increases in α- and γ-Toc, respectively. In vitro cultured carrot plants showed differential trends in Toc synthesis when exposed to Cd (36 μM) for 2, 4, 7, and 14 d (Sanita` di Toppi et al., 2012). After a 2-d Cd stress, no change in α-Toc was observed, while at 4, 7, and 14 d, the level of α-Toc significantly increased.

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12.5.5 Ozone Ozone (O3) is a strong oxidant. By entering the leaf mesophyll tissue, O3 leads to generation of ROS (through steps of reactions) that create various complexities within plants. Necrosis, oxidative damage, growth reduction, anomalous vegetative and reproductive development, and reduced crop productivity are the common effects of O3 stress (Pellinen et al., 2002). In several reports, Toc has been found to confer plant tolerance to elevated O3. Mutants of Nicotiana tabacum overexpressing Toc cyclase (catalyzes the penultimate step of Toc synthesis) and its wild type were assessed for their responses to O3. In response to 300 nmol L21 O3 for 4 h, the wild type showed leaf necrosis. The transgenic lines showed limited injury as well as an increased photosynthetic rate compared to wild type due to maintenance of the structural integrity of the photosynthetic machineries. The transgenic line also had reduced H2O2, MDA levels with reduced ion leakage (Guo et al., 2009). Enhanced α- or γ-Toc was supposed to provide tolerance against O3 stress in Fagus sylvatica (Haberer et al., 2008).

12.5.6 UV radiation Due to global climate change, the stratosphereric O3 layer is being destroyed, which allows the infiltration of more ultraviolet (UV) radiation to the Earth. The increase in solar ultraviolet-B radiation has become a great concern because a 1% loss of O3 leads to a 2% increase in UV radiation (Mpoloka, 2008). Plants exhibit various anomalous responses to UV-B radiation, which has damaging effects on plant growth, physiology, and yield and also causes oxidative stress (He et al., 2003; Zhang et al., 2003; Mpoloka 2008). The α-Toc has been mentioned as a protectant from UV-radiation stress in some studies, especially in animal cells; however, evidence of its effect on plant cells is scarce indeed. At least one report noted that UV-B stress in plants is correlated with Toc content (Munné-Bosch and Alegre, 2002). The α-Toc of thylakoid membrane scavenges ROS and lipid alkyl and peroxyl radicals and maintains the structure and function of membranes (Fryer, 1992; Hess, 1993). UV-B-induced oxidative stress was resolved by incorporating α-Toc into phosphatidylcholine liposomes (Pelle et al., 1990). Leaves’ thylakoid membranes of Spinacia oleracea L. cv. Meridian were irradiated at 1.8 kJ m22 h21 of biologically effective UV-B radiation for 180 min. A significant increase of lipid peroxidation was evident by the UV-B stress that was increased with time. During increasing lipid peroxidation levels, the endogenous α-Toc was increased; this helped to scavenge ROS and to reduce the lipid peroxidation induced by oxidative damage. Elevated levels of α-Toc conferred antioxidant protection of thylakoid membrane lipids at the same time α-Toc was degraded over time (DeLong and Steffen, 1998).

12.6 The antioxidative role of tocopherol in plants Tocopherol is a lipid-soluble nonenzymatic antioxidant. In cooperation with other antioxidants (e.g., AsA), it (mainly α-Toc) effectively eliminates ROS production (mainly 1O2 and OH•). It was evident that Toc biosynthesis increased under stressful conditions and provided better protection against oxidative stress by limiting ROS generation (Shao et al., 2008; Semchuk et al., 2009;

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FIGURE 12.4 Initiation (A), propagation (B), and termination (C) of the autoxidation chain reaction. Additional details can be found in the text. Source: Adapted from Schneider (2005) with permission from Wiley.

Lushchak and Semchuk, 2012). Tocopherol is present in high amounts in the thylakoid membrane in chloroplast, also a major site of ROS production. Because both ROS production and Toc biosynthesis are localized at the same site, it is possible that the enrichment of α-Toc in chloroplast membranes can be related to the ability of Toc to scavenge ROS-like 1O2 and LOO•, protecting the photosynthetic apparatus from oxidative stress and lipid peroxidation (Munné-Bosch, 2007; Lushchak and Semchuk, 2012), as shown in Figures 12.4 and 12.5. Apart from the formation of Toc, the enzymes MPBQ and DMPBQ showed antioxidant activity by donating two electrons (Leibler and Burr, 2000). Basically, the main role of Toc as an antioxidant is to stabilize the membrane structure involved in the reaction with polyunsaturated fatty acyl chains (Sattler et al., 2003). One of the most widely investigated parameters during oxidative stress in plants is lipid peroxidation (Blokhina et al., 2003), which is initiated by generation of alkyl radical (L•) from PUFA during oxidative stress (Lushchak and Semchuk, 2012). One of the major roles of Toc is reacting with L•; this is a major product during lipid peroxidation (Burton and Ingold, 1981). Among the Toc, α-Toc has the highest antioxidant potential because it has the highest Vit-E activity as well (DellaPenna and Pogson, 2006). The reason for α-Toc being an efficient antioxidant is due to its extremely fast reaction capability with LOO•. In addition, it eliminates the radical properties of the oxidizing fatty acid, thus protecting the subsequent radical reactions that end with a nonradical and nondestructive product. The initiation, propagation, and termination of the autoxidation chain reaction are shown in Figure 12.4B (Schneider, 2005); the author’s study described a three-step reaction toward

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FIGURE 12.5 Coordination role of tocopherol and other antioxidant in ROS detoxification. Additional details can be found in the text.

successful conversion of PUFA to a nonradical product. In the first step, the initial hydrogen abstraction from the bis-allylic methylene of a PUFA (L-H) can be accomplished by various stress factors (X). After that a fast reaction of L• and molecular oxygen (O2) occurs. However, the next slower radical reaction appears to form LOO•—the primary target for the antioxidant reaction. Finally, α-Toc donates the hydrogen from the 6-OH group to the LOO• to form a stable hydroperoxide (L-OOH) and a tocopheroxyl radical (TO•), a faster reaction than the previous reaction in terms of rate for the LOO• (see Figure 12.4C). Other reactions resulting in chain termination are the reaction of the TO• with a LOO• or the dimerization of two LOO•. Both reactions yield nonradical products (Schneider, 2005). The antioxidant activity of Toc as free radical scavengers is associated with the ability to donate its phenolic hydrogen to a lipid-free radical and with the specific requirements of the molecules (Szarka et al., 2012). In particular, Toc has a wider ability to quench 1O2, a countable ROS, and it was reported that one molecule of α-Toc has the capacity to dismutase up to 120 molecules of 1O2 (Fahrenholtz et al., 1974). Transgenic A. thaliana overexpressing Toc synthesis genes provided higher biosynthesis of α-Toc, which showed less accumulation of O2 2 and H2O2 compared to nontransgenic plants (Sattler et al., 2006). During the process of scavenging 1O2, irreversible production of quinones and epoxides occurs, while during the conversion of LOO•, TO• is produced; this can be recycled back to α-Toc in the AsAGSH cycle. Thus, Toc becomes a coordinated part of the AsAGSH cycle as well maintaining a redox state in chloroplast (Munné-Bosch, 2005); see Figure 12.5. Although not

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fully revealed, the interactions between Toc, free radicals, and plant hormones (JA, SA, Eth) show the complex processes of cell signaling and gene regulation toward stress tolerance, directly or indirectly (see Figure 12.5). The interrelated role of AsA and GSH with the ROS-eliminating capability of Toc gives the concept of triad, resulting in the recycling of TO• to Toc (Smirnoff, 2007). During the conversion of LOO• to LOH, CAR also plays a coordinated role, and the same as Toc, CAR reacts with the LOO• produced as a consequence of lipid peroxidation (Smirnoff, 2007).

12.7 Conclusion and future prospects In spite of being a well-known antioxidant, which provides protection against abiotic stress conditions, there are many gaps in grasping the basic mechanisms through which Toc confers abiotic stress tolerance, so its overall effects in plants should be explored. The exact mechanism of the mode of action of Toc is still poorly understood, especially because it may differ in the various species and may also depend on environmental factors. The signaling role of Toc may be more complex; however, being an intricate signaling network controlled by ROS, antioxidants, and phytohormones, Toc is a good candidate to influence cell signaling toward stress tolerance. Other antioxidants (e.g., AsA and GSH) are interlinked with Toc for the control of ROS. In some studies, exogenous application of Toc showed an enhanced level of endogenous Toc and enhanced stress tolerance. Therefore, finding appropriate doses and methods of Toc application as a protectant is a subject for further study. In recent years, some attempts have been made to tailor the genes responsible for Toc biosynthesis under stressful conditions. Complete elucidation of these processes will help in developing abiotic stress tolerance and providing Toc-enriched food for human beings.

Acknowledgments We wish to thank Mr. Md. Mahabub Alam and Mr. Anisur Rahman at the Laboratory of Plant Stress Responses, Faculty of Agriculture, Kagawa University in Japan for their vital assistance during the preparation of the manuscript. We thankfully acknowledge Mr. Md. Iqbal Hosen at the Key Laboratory of Biodiversity and Biogeography, Kunming Institute of Botany, Chinese Academy of Sciences in Yunnan, China, for providing several supporting papers on aspects of this chapter. We apologize to all researchers for those parts of their work that were not cited in here because of the page limitation.

References Abbasi, A.R., Hajirezaei, M., Hofius, D., Sonnewald, U., Voll, L.M., 2007. Specific roles of α- and γ-tocopherol in abiotic stress responses of transgenic tobacco. Plant Physiol. 143, 17201738. Acquaah, G., 2007. Principles of Plant Genetics and Breeding. Blackwell Publishing, Oxford, p. 385. Alam, M.M., Hasanuzzaman, M., Nahar, K., Fujita, M., 2013. Exogenous salicylic acid ameliorates short-term drought stress in mustard (Brassica juncea L.) seedlings by up-regulating the antioxidant defense and glyoxalase system. Aust. J. Crop Sci. 7, 10531063.

References

283

Arrom, L., Munné-Bosch, S., 2010. Tocopherol composition in flower organs of Lilium and its variations during natural and artificial senescence. Plant Sci. 179, 289295. Artetxe, U., Garcıá-Plazaola, J.I., Hernández, A., Becerril, J.M., 2002. Low light grown duckweed plants are more protected against the toxicity induced by Zn and Cd. Plant Physiol. Biochem. 40, 859863. Ashraf, M., Harris, P.J.C., 2004. Potential biochemical indicators of salinity tolerance in plants. Plant Sci. 166, 316. Bafeel, S.O., Ibrahim, M.M., 2008. Antioxidants and accumulation of α-tocopherol induce chilling tolerance in Medicago sativa. Int. J. Agric. Biol. 10, 593598. Bartoli, C.G., Simontacchi, M., Tambussi, E., Beltrano, J., Montaldi, E., Puntarulo, S., 1999. Drought and watering-dependent oxidative stress: effect on antioxidant content in Triticum aestivum L. leaves. J. Exp. Bot. 50, 375383. Blokhina, O., Virolainen, E., Fagerstedt, K.V., 2003. Antioxidants, oxidative damage and oxygen deprivation stress: a review. Ann. Bot. 91, 179194. Boo, Y.C., Jung, J., 1999. Water deficit-induced oxidative stress and antioxidative defenses in rice plants. J. Plant Physiol. 155, 255261. Botha, C.E.J., Cross, R.H.M., van Bel, A.J.E., Peter, C.I., 2000. Phloem loading in the sucrose-export-defective (SXD-1) mutant maize is limited by callose deposition at plasmodesmata in bundle sheath-vascular parenchyma interface. Protoplasma 214, 6572. Burton, G.W., Ingold, K.H., 1981. Autoxidation of biological molecules. 1. The antioxidant activity of vitamin E and related chain-breaking phenolic antioxidants in vitro. J. Am. Chem. Soc. 103, 64726477. Cela, J., Arrom, L., Munné-Bosch, S., 2009. Diurnal changes in photosystem II photochemistry, photoprotective compounds and stress-related phytohormones in the CAM plant, Aptenia cordifolia. Plant Sci. 177, 404410. Cela, J., Chang, C., Munné-Bosch, S., 2011. Accumulation of γ- rather than α-tocopherol alters ethylene signaling gene expression in the vte4 mutant of Arabidopsis thaliana. Plant Cell Physiol. 52, 13891400. Collin, V.C., Eymery, F., Genty, B., Rey, P., Havaux, M., 2008. Vitamin E is essential for the tolerance of Arabidopsis thaliana to metal-induced oxidative stress. Plant Cell Environ. 31, 244257. DeLong, J.M., Steffen, 1998. Lipid peroxidation and α-tocopherol content in α-tocopherol-supplemented thylakoid membranes during UV-B exposure. Environ. Exp. Bot. 39, 177185. DellaPenna, D., Pogson, B.J., 2006. Vitamin synthesis in plants: tocopherols and carotenoids. Annu. Rev. Plant Biol. 57, 711738. Demurin, Y., Skoric, D., Karlovic, D., 1996. Genetic variability of tocopherol composition in sunflower seeds as a basis of breeding for improved oil quality. Plant Breed. 115, 3336. Desel, C., Krupinska, K., 2005. The impact of tocochromanols on early seedling development and NO release. J. Plant Physiol. 162, 771776. Desel, C., Hubbermann, E.M., Schwarz, K., Krupinska, K., 2007. Nitration of γ-tocopherol in plant tissues. Planta 226, 13111322. Dong, G., Liu, X., Chen, Z., Pan, W., Li, H., Liu, G., 2007. The dynamics of tocopherol and the effect of high temperature in developing sunflower (Helianthus annuus L.) embryo. Food Chem. 102, 138145. Eitenmiller, R.R., 1997. Vitamin E content of fats and oils—nutritional implications. Food Technol. 51, 7881. El-Bassiouny, H.M.S., Gobarah, M.E., Ramadan, A.A., 2005. Effect of antioxidants on growth, yield, savism causative agents in seeds of Vicia faba L. plants grown under reclaimed sandy soils. J. Agric. Pak. 7, 653659. El-Quesni, F.E., Abd EL-Aziz, N., Maga, M.K., 2009. Some studies on the effect of ascorbic acid and α-tocopherol on the growth and some chemical composition of Hibiscus rosa sinensis L. at Nurbaria. Ozean J. Appl. Sci. 2, 159167. Ellouzi, H., Hamed, K.B., Cela, J., Munné-Bosch, S., Abdelly, C., 2011. Early effects of salt stress on the physiological and oxidative status of Cakile maritima (halophyte) and Arabidopsis thaliana (glycophyte). Physiol. Plant 142, 128143.

284


Ellouzi, H., Karim Hamed, B., Cela, J., Mu¨ller, M., Abdelly, C., Munné-Bosch, S., 2013. Increased sensitivity to salt stress in tocopherol-deficient Arabidopsis mutants growing in a hydroponic system. Plant Signal. Behav. 8, e23136. Espinoza, A., Martıń, A.S., Lo´pez-Climent, M., Ruiz-Lara, S., Go´mez-Cadenas, A., Casaretto, J.A., 2013. Engineered drought-induced biosynthesis of α-tocopherol alleviates stress-induced leaf damage in tobacco. J. Plant Physiol. 170, 12851294. Fahrenholtz, S.R., Doleiden, F.H., Trozzolo, A.M., Lamola, A.A., 1974. On the quenching of singlet oxygen by α-tocopherol. Photochem. Photobiol. 20, 505509. Falk, J., Krauss, N., Dahnhardt, D., Krupinska, K., 2002. The senescence associated gene of barley encoding 4-hydroxyphenylpyruvate dioxygenase is expressed during oxidative stress. J. Plant Physiol. 159, 12451253. Farooq, M., Aziz, T., Wahid, A., Lee, D.J., Siddique, K.H.M., 2009. Chilling tolerance in maize: agronomic and physiological approaches. Crop Past. Sci. 60, 501516. Farouk, S., 2011. Ascorbic acid and α-tocopherol minimize salt-induced wheat leaf senescence. J. Stress Physiol. Biochem. 7, 5879. Fernholz, E., 1938. On the constitution of α-tocopherol. J. Am. Chem. Soc. 60, 700705. Fryer, M.J., 1992. The antioxidant effects of thylakoid vitamin E (α-tocopherol). Plant Cell Environ. 15, 381392. Gajewska, E., Skłodowska, M., 2007. Relations between tocopherol, chlorophyll and lipid peroxides contents in shoots of Ni-treated wheat. J. Plant Physiol. 164, 364366. Gill, S.S., Tuteja, N., 2010. Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol. Biochem. 48, 909930. Grabes, T., Grimm, B., Koroleva, O., Jahns, P., 2001. Loss of α-tocopherol in tobacco plants with decreased geranylgeranyl reductase activity does not modify photosynthesis in optimal growth conditions but increases sensitivity to high-light stress. Planta 213, 620628. Grusak, M.A., DellaPenna, D., 1999. Improving the nutrient composition of plants to enhance human nutrition and health. Annu. Rev. Plant Physiol. Plant Mol. Biol. 50, 133161. Guo, J., Li, X.F., Qi, D.M., Chen, S.Y., Li, Z.Q., Nijs, I., et al., 2009. Effects of ozone on wild type and transgenic tobacco. Biol. Plant 53, 670676. Haberer, K., Herbinger, K., Alexou, M., Rennenberg, H., Tausz, M., 2008. Effects of drought and canopy ozone exposure on antioxidants in fine roots of mature European beech (Fagus sylvatica). Tree Physiol. 28, 713719. Hasanuzzaman, M., Fujita, M., 2011. Selenium pretreatment upregulates the antioxidant defense and methylglyoxal detoxification system and confers enhanced tolerance to drought stress in rapeseed seedlings. Biol. Trace Elem. Res. 143, 17581776. Hasanuzzaman, M., Fujita, M., 2012. Heavy metals in the environment: current status, toxic effects on plants and possible phytoremediation. In: Anjum, N.A., Pereira, M.A., Ahmad, I., Duarte, A.C., Umar, S., Khan, N.A. (Eds.), Phytotechnologies: Remediation of Environmental Contaminants. CRC Press, Boca Raton, FL, pp. 773. Hasanuzzaman, M., Fujita, M., 2013. Exogenous sodium nitroprusside alleviates arsenic-induced oxidative stress in wheat (Triticum aestivum L.) seedlings by enhancing antioxidant defense and glyoxalase system. Ecotoxicol. 22, 584596. Hasanuzzaman, M., Fujita, M., Islam, M.N., Ahamed, K.U., Nahar, K., 2009. Performance of four irrigated rice varieties under different levels of salinity stress. Int. J. Integr. Biol. 6, 8590. Hasanuzzaman, M., Hossain, M.A., Fujita, M., 2010. Physiological and biochemical mechanisms of nitric oxide induced abiotic stress tolerance in plants. Am. J. Plant Physiol. 5, 295324. Hasanuzzaman, M., Hossain, M.A., Fujita, M., 2011a. Nitric oxide modulates antioxidant defense and the methylglyoxal detoxification system and reduces salinity-induced damage of wheat seedlings. Plant Biotechnol. Rep. 5, 353365.

References

285

Hasanuzzaman, M., Hossain, M.A., Fujita, M., 2011b. Selenium-induced up-regulation of the antioxidant defense and methylglyoxal detoxification system reduces salinity-induced damage in rapeseed seedlings. Biol. Trace Elem. Res. 143, 17041721. Hasanuzzaman, M., Hossain, M.A., Teixeira da Silva, J.A., Fujita, M., 2012a. Plant responses and tolerance to abiotic oxidative stress: antioxidant defense is a key factor. In: Bandi, V., Shanker, A.K., Shanker, C., Mandapaka, M. (Eds.), Crop Stress and its Management: Perspectives and Strategies. Springer, Berlin, pp. 261316. Hasanuzzaman, M., Hossain, M.A., Fujita, M., 2012b. Exogenous selenium pretreatment protects rapeseed seedlings from cadmium-induced oxidative stress by upregulating the antioxidant defense and methylglyoxal detoxification systems. Biol. Trace Elem. Res. 149, 248261. Hasanuzzaman, M., Nahar, K., Alam, M.M., Fujita, M., 2012c. Exogenous nitric oxide alleviates high temperature induced oxidative stress in wheat (Triticum aestivum) seedlings by modulating the antioxidant defense and glyoxalase system. Aust. J. Crop Sci. 6, 13141323. Hasanuzzaman, M., Nahar, K., Fujita, M., 2013a. Plant response to salt stress and role of exogenous protectants to mitigate salt-induced damages. In: Ahmad, P., Azooz, M.M., Prasad, M.N.V. (Eds.), Ecophysiology and Responses of Plants under Salt Stress. Springer, New York, pp. 2587. Hasanuzzaman, M., Nahar, K., Fujita, M., Ahmad, P., Chandna, R., Prasad, M.N.V., et al., 2013b. Enhancing plant productivity under salt stress—Relevance of poly-omics. In: Ahmad, P., Azooz, M.M., Prasad, M.N.V. (Eds.), Salt Stress in Plants: Omics, Signaling and Responses. Springer, Berlin, pp. 113156. Hasanuzzaman, M., Nahar, K., Fujita, M., 2013c. Extreme temperatures, oxidative stress and antioxidant defense in plants. In: Vahdati, K., Leslie, C. (Eds.), Abiotic Stress—Plant Responses and Applications in Agriculture. InTech, Rijeka, pp. 169205. Hasanuzzaman, M., Nahar, K., Gill, S.S., Fujita, M., 2014. Drought stress responses in plants, oxidative stress and antioxidant defense. In: Gill, S.S., Tuteja, N. (Eds.), Climate Change and Plant Abiotic Stress Tolerance. Wiley, Weinheim, pp. 209249. He, D.L., Wong, C.H., He, Y.H., 2003. The effect of reduction of ultraviolet-B radiance on the content of flavonoid in leaves of wheat. Chin. J. Agromet. 24, 32. Hernández, I., Alegre, L., Munné-Bosch, S., 2004. Drought-induced changes in flavonoids and other low molecular weight antioxidants in Cistus clusii grown under Mediterranean field conditions. Tree Physiol. 24, 13031311. Hernández, I., Cela, J., Alegre, L., Munné-Bosch, S., 2012. Antioxidant defenses against drought stress. In: Aroca, R. (Ed.), Plant Responses to Drought Stress: From Morphological to Molecular Features. Springer, New York, pp. 231258. Herrmann, K., 1995. The Shikimate pathway: early steps in the biosynthesis of aromatic compounds. Plant Cell 7, 907919. Hess, J.L., 1993. Vitamin E, α-tocopherol. In: Alscher, R., Hess, J.L. (Eds.), Antioxidants of Higher Plants. CRC Press, Boca Raton, FL, pp. 111134. Hofius, D., Hajirezaei, M.R., Geiger, M., Tschiersch, H., Melzer, M., Sonnewald, U., 2004. RNAi-mediated tocopherol deficiency impairs photoassimilate export in transgenic potato plants. Plant Physiol. 135, 12561268. Holla¨nder-Czytko, H., Grabowski, J., Sandorf, I., Weckermann, K., Weiler, E.W., 2005. Tocopherol content and activities of tyrosine aminotransferase and cystine lyase in Arabidopsis under stress conditions. J. Plant Physiol. 162, 767770. Horvath, G., Wessjohann, L., Bigirimana, J., Monica, H., Jansen, M., Guisez, Y., et al., 2006. Accumulation of tocopherols and tocotrienols during seed development of gape (Vitis vinifera L. Albert Lavallee). Plant Physiol. Biochem. 44, 724731. Howarth, C.J., 2005. Genetic improvements of tolerance to high temperature. In: Ashraf, M., Harris, P.J. (Eds.), Abiotic Stresses: Plant Resistance through Breeding and Molecular Approaches. Howarth Press Inc., New York, pp. 277300.

286


Hussain, N., Irshad, F., Jabeen, Z., Shamsi, I.H., Li, Z., Jiang, L., 2013. Biosynthesis, structural, and functional attributes of tocopherols in planta; past, present, and future perspectives. J. Agric. Food Chem. 61, 61376149. Ischebeck, T., Zbierzak, A.M., Kanwischer, M., Do¨rmann, P., 2006. A salvage pathway for phytol metabolism in Arabidopsis. J. Biol. Chem. 281, 24702477. Jaleel, C.A., Gopi, R., Manivannan, P., Gomathinayagam, M., Sridharan, R., Panneerselvam, R., 2008. Antioxidant potential and indole alkaloid profile variations with water deficits along different parts of two varieties of Catharanthus roseus. Colloids Surf. B Biointerfaces 62, 312318. Kamal-Eldin, A., Appelqvist, L., 1996. The chemistry and antioxidant properties of tocopherols and tocotrienols. Lipids 31, 671701. Kanayama, Y., Sato, K., Ikeda, H., Tamura, T., Nishiyama, M., Kanahama, K., 2013. Seasonal changes in abiotic stress tolerance and concentrations of tocopherol, sugar, and ascorbic acid in sea buckthorn leaves and stems. Sci. Hortic. 164, 232237. Karrer, P., Fritzsche, H., Ringier, B.H., Salomon, H., 1938. Synthesis of α-tocopherol (vitamin E). Nature 141, 1057. Keller, Y., Bouvier, F., D’Harlingue, A., Camara, B., 1998. Metabolic compartmentation of plastid prenyllipid biosynthesis: evidence for the involvement of a multifunctional geranylgeranyl reductase. Eur. J. Biochem. 251, 413417. Kepova, K.D., Hozler, R., Stoilova, L.S., Feller, U., 2005. Heat stress effects on ribulose-1,5, bisphosphate carboxylase/oxygenase, Rubisco binding protein and Rubisco activase in wheat leaves. Biol. Plant 49, 521525. Kumar, S., Singh, R., Nayyar, H., 2013. α-Tocopherol application modulates the response of wheat (Triticum aestivum L.) seedlings to elevated temperatures by mitigation of stress injury and enhancement of antioxidants. J. Plant Growth Regul. 32, 307314. Leibler, D.C., Burr, J.A., 2000. Antioxidant reaction of α-tocopherolhydroquinone. Lipids 35, 10451047. Lichtenthaler, H.K., 2000. The non-mevalonate isoprenoid biosynthesis: enzymes, genes and inhibitors. Biochem. Soc. Trans. 28, 787792. Liu, X., Huang, B., 2000. Heat stress injury in relation to membrane lipid peroxidation in creeping bentgrass. Crop Sci. 40, 503510. Liu, X., Hua, X., Guo, J., Qi, D., Wang, L., Liu, Z., et al., 2008. Enhanced tolerance to drought stress in transgenic tobacco plants overexpressing VTE1 for increased tocopherol production from Arabidopsis thaliana. Biotechnol. Lett. 30, 12751280. Lopukhina, A., Dettenberg, M., Weiler, E.W., Holla¨nder-Czytko, H., 2001. Cloning and characterization of a coronatine-regulated tyrosine aminotransferase from Arabidopsis. Plant Physiol. 126, 16781687. Luis, P., Behnke, K., Toepel, J., Wilhelm, C., 2006. Parallel analysis of transcript levels and physiological key parameters allows the identification of stress phase gene markers in Chlamydomonas reinhardtii under copper excess. Plant Cell Environ. 29, 20432054. Lushchak, V.I., Semchuk, N.M., 2012. Tocopherol biosynthesis: chemistry, regulation and effects of environmental factors. Acta Physiol. Plant. 34, 16071628. Maeda, H., Sakuragi, Y., Bryant, D.A., DellaPenna, D., 2005. Tocopherols protect Synechocystis sp. strain PCC 6803 from lipid peroxidation. Plant Physiol. 138, 14221435. Maeda, H., Song, W., Sage, T.L., DellaPenna, D., 2006. Tocopherols play a crucial role in low-temperature adaptation and phloem loading in Arabidopsis. Plant Cell 18, 27102732. Mahajan, S., Tuteja, N., 2005. Cold, salinity and drought stresses: an overview. Arch. Biochem. Biophys. 444, 139158. Matringe, M., Ksas, B., Rey, P., Havaux, M., 2008. Tocotrienols, the unsaturated forms of vitamin E, can function as antioxidants and lipid protectors in tobacco leaves. Plant Physiol. 147, 764778.

References

287

Mendes, P., Kell, D., 1997. Making cells work—metabolic engineering for everyone. Trends Biotechnol. 15, 67. Mittler, R., Kim, Y., Song, L., Coutu, J., Coutu, A., Ciftci-Yilmaz, S., et al., 2007. Gain- and loss-of-function mutations in Zat10 enhance the tolerance of plants to abiotic stress. FEBS Lett. 580, 65376542. Moran, J.F., Becana, M., Iturbeormaetxe, I., Frechilla, S., Klucas, R.V., Apariciotejo, P., 1994. Drought induces oxidative stress in pea-plants. Planta 194, 346352. Mpoloka, S.W., 2008. Effects of prolonged UV-B exposure in plants. Afr. J. Biotechnol. 7, 48744883. Munné-Bosch, S., 2005. The role of α-tocopherol in plant stress tolerance. J. Plant Physiol. 162, 743748. Munné-Bosch, S., 2007. α-Tocopherol: a multifaceted molecule in plants. Vitam. Horm. 76, 375392. Munné-Bosch, S., Alegre, L., 2001. Subcellular compartmentation of the diterpene carnosic acid and its derivatives in the leaves of rosemary. J. Plant Physiol. 125, 10941102. Munné-Bosch, S., Alegre, L., 2002. The function of tocopherols and tocotrienols in plants. Crit. Rev. Plant Sci. 21, 3157. Munné-Bosch, S., Alegre, L., 2003. Drought-induced changes in the redox state of alpha-tocopherol, ascorbate, and the diterpene carnosic acid in chloroplasts of Labiatae species differing in carnosic acid contents. Plant Physiol. 131, 18161825. Munné-Bosch, S., Schwarz, K., Alegre, L., 1999. Enhanced formation of α-tocopherol and highly oxidized abietane diterpenes in waterstressed rosemary plants. Plant Physiol. 121, 10471052. Munné-Bosch, S., Weiler, E.W., Alegre, L., Muller, M., Duchting, P., Falk, J., 2007. α-Tocopherol may influence cellular signaling by modulating jasmonic acid levels in plants. Planta 225, 681691. Nahar, K., Hasanuzzaman, M., Majumder, R.R., 2009a. Effect of low temperature stress in transplanted Aman Rice Varieties mediated by different transplanting dates. Acad. J. Plant Sci. 2, 132138. Nahar, K., Biswas, J.K., Shamsuzzaman, A.M.M., Hasanuzzaman, M., Barman, H.N., 2009b. Screening of indica rice (Oryza sativa L.) genotypes against low temperature stress. Bot. Res. Int. 2, 295303. Oukarroum, A., Strasser, R.J., Schansker, G., 2012. Heat stress and photosynthetic electron transport chain of the lichen Parmelina tiliacea (Hoffm.) Ach. in the dry and the wet state: differences and similarities with the heat stress response of higher plants. Photosynth. Res. 111, 303314. Ouyang, S., He, S., Liu, P., Zhang, W., Zhang, J., Chen, S., 2011. The role of tocopherol cyclase in salt stress tolerance of rice (Oryza sativa). Sci. China Life Sci. 54, 181813. Pelle, E., Maes, D., Padulo, G.A., Kim, E.K., Smith, W.P., 1990. An in vitro model to test relative antioxidant potential: ultraviolet-induced lipid peroxidation in liposomes. Arch. Biochem. Biophys. 283, 234240. Pellinen, R.I., Korhonen, M.S., Tauriainen, A.A., Palva, E.T., Kangasj˘arvi, J., 2002. Hydrogen peroxide activates cell death and defense gene expression in birch. Plant Physiol. 130, 549560. Porfirova, S., Bergmuller, E., Tropf, S., Lemke, R., Dormann, P., 2002. Isolation of an Arabidopsis mutant lacking vitamin E and identification of a cyclase essential for all tocopherol biosynthesis. Proc. Natl. Acad. Sci. USA 99, 1249512500. Price, A.H., Atherton, N.M., Hendry, G.A., 1989. Plants under drought-stress generate activated oxygen. Free Radic. Res. Commun. 8, 6166. Provencher, L.M., Miao, L., Sinha, N., Lucas, W.J., 2001. Sucrose export defective1 encodes a novel protein implicated in chloroplast-to-nucleus signaling. Plant Cell 13, 11271141. Rodrı´guez, M., Canales, E., Borrás-Hidalgo, O., 2005. Molecular aspects of abiotic stress in plants. Biotechnol. Appl. 22, 110. Rucińska-Sobkowiak, R., Pukacki, P.M., 2006. Antioxidative defense system in lupin roots exposed to increasing concentrations of lead. Acta Physiol. Plant 28, 357364. Russin, W.A., Evert, R.E., Vanderveer, P.J., Sharkey, T.D., Briggs, S.P., 1996. Modification of a specific class of plasmodesmata and loss of sucrose export ability in a sucrose export defective1 maize mutant. Plant Cell 8, 645658.

288


Sadak, M.S., Rady, M.M., Badr, N.M., Gaballah, M.S., 2010. Increasing sunflower salt tolerance using nicotinamide and α-tocopherol. Int. J. Acad. Res. 2, 263270. Sandorf, I., Holla¨nder-Czytko, H., 2002. Jasmonate is involved in the induction of tyrosine aminotransferase and tocopherol biosynthesis in Arabidopsis thaliana. Planta 216, 173179. Sanita` di Toppi, L., Vurro, E., De Benedictis, M., Falasca, G., Zanella, L., Musetti, R., et al., 2012. A bifasic response to cadmium stress in carrot: early acclimatory mechanisms give way to root collapse further to prolonged metal exposure. Plant Physiol. Biochem. 58, 269279. Sattler, S.E., Cahoon, E.B., Coughlan, S.J., DellaPenna, D., 2003. Characterization of tocopherol cyclases from higher plants and cyanobacteria. Evolutionary implications for tocopherol synthesis and function. Plant Physiol. 132, 21842195. Sattler, S.E., Gilliland, L.U., Magallanes-Lundback, M., Pollard, M., Penna, D.D., 2004. Vitamin E is essential for seed longevity and for preventing lipid peroxidation during germination. Plant Cell 16, 14191432. Sattler, S.E., Me`ne-Saffrané, L., Farmer, E.E., Krischke, M., Mueller, M.J., DellaPenna, D., 2006. Nonenzymatic lipid peroxidation reprograms gene expression and activates defense markers in Arabidopsis tocopherol-deficient mutants. Plant Cell 18, 37063720. Schneider, C., 2005. Chemistry and biology of vitamin E. Mol. Nutr. Food Res. 49, 730. Semchuk, N., Lushchak, O.V., Falk, J., Krupinska, K., Lushchak, V.I., 2009. Inactivation of genes, encoding tocopherol biosynthetic pathway enzymes, results in oxidative stress in outdoor grown Arabidopsis thaliana. Plant Physiol. Biochem. 47, 384390. Semchuk, N.M., Vasylyk, Y.V., Kubrak, O.I., Lushchak, V.I., 2011. Effect of sodium nitroprusside and S-nitrosoglutathione on pigment content and antioxidant system of tocopherol-deficient plants of Arabidopsis thaliana. Ukr. Biokhim. Zh. 83, 6979. Shao, H.B., Chu, L.Y., Lu, Z.H., Kang, C.M., 2008. Primary antioxidant free radical scavenging and redox signaling pathways in higher plant cells. Int. J. Biol. Sci. 4, 814. Skłodowska, M., Gapin, M., Gajewska, E., Gabara, B., 2009. Tocopherol content and enzymatic antioxidant activities in chloroplasts from NaCl-stressed tomato plants. Acta Physiol. Plant. 31, 393400. Smirnoff, N., 1993. The role of active oxygen in the response of plants to water deficit and desiccation. New Phytol. 125, 2758. Smirnoff, N., 2007. Ascorbate, tocopherol and carotenoids: metabolism, pathway engineering and functions. In: Smirnoff, N. (Ed.), Antioxidants and Reactive Oxygen Species in Plants. Blackwell Publishing, Oxford, pp. 5386. Soltani, Y., Saffari, V.R., Moud, A.A.M., Mehrabani, M., 2012. Effect of foliar application of α-tocopherol and pyridoxine on vegetative growth, flowering, and some biochemical constituents of Calendula officinalis L. plants. Afr. J. Biotechnol. 11, 1193111935. Streb, P., Shang, W., Feierabend, J., 1999. Resistance of cold-hardened winter rye leaves (Secale cereale L.) to photo-oxidative stress. Plant Cell Environ. 22, 12111223. Sun, Y.C., Chen, Y.C., Tian, Z.X., Li, F.M., Wang, X.Y., Zhang, J., et al., 2005. Novel AroA with high tolerance to glyphosate, encoded by a gene of Pseudomonas putida 4G-1 isolated from an extremely polluted environment in China. Appl. Environ. Microbiol. 71, 47714776. Szarka, A., Tomasskovics, B., Bánhegyi, G., 2012. The ascorbate-glutathione-α-tocopherol triad in abiotic stress response. Int. J. Mol. Sci. 13, 44584483. Szymańska, R., Kruk, J., 2008. Tocopherol content and isomers’ composition in selected plant species. Plant Physiol. Biochem. 46, 2933. Tan, B., 1989. Palm carotenoids, tocopherols and tocotrienols. J. Am. Oil Chem. Soc. 66, 770776. Tanaka, M., Murai, M., Tokunaga, H., Kimura, T., Okada, S., 1990. Tocopherol succinate reference standard (control 881) of National Institute of Hygienic Sciences. Eisei Shikenjo Hokoku 108, 156158.

References

289

Tanaka, R., Oster, U., Kruse, E., Rudiger, W., Grimm, B., 1999. Reduced activity of geranylgeranyl reductase leads to loss of chlorophyll and tocopherol and to partially geranylgeranylated chlorophyll in transgenic tobacco plants expressing antisense RNA for geranylgeranyl reductase. Plant Physiol. 120, 695704. Threlfall, D.R., 1971. The biosynthesis of vitamin E and K and related compounds. Vitam. Horm. 29, 153200. Valentin, H.E., Lincoln, K., Moshiri, F., Jensen, P.K., Qi, Q., Venkatesh, T.V., et al., 2006. The Arabidopsis vitamin E pathway gene5-1 mutant reveals a critical role for phytol kinase in seed tocopherol biosynthesis. Plant Cell 18, 212224. Vollenweider, P., Gunhardt-Goerg, M.S., 2005. Diagnosis of abiotic and biotic stress factors using the visible symptoms in foliage. Environ. Pollut. 137, 455465. Wahid, A., Gelani, S., Ashraf, M., Foolad, M.R., 2007. Heat tolerance in plants: an overview. Environ. Exp. Bot. 61, 199223. White, D.A., Fisk, I.D., Gray, D.A., 2006. Characterisation of oat (Avena sativa L.) oil bodies and intrinsically associated E-vitamers. J. Cereal Sci. 43, 244249. Yusuf, M.A., Kumar, D., Rajwanshi, R., Strasser, R.J., Tsimilli-Michael, M., Govindjee, et al., 2010. Overexpression of gamma-tocopherol methyl transferase gene in transgenic Brassica juncea plants alleviates abiotic stress: physiological and chlorophyll a fluorescence measurements. Biochim. Biophys. Acta 1797, 14281438. Zhang, J., 2011. China’s success in increasing per capita food production. J. Exp. Bot. 62, 37073711. Zhang, M., An, L., Feng, H., Chen, T., Chen, K., Liu, Y., et al., 2003. The cascade mechanisms of nitric oxide as second messenger of ultraviolet-B in inhibiting mesocotyl elongation. Photochem. Photobiol. 77, 219225. Zhou-fei, W., Jian-fei, W., Fu-hua, W., Yong-mei, B., Yun-yu, W., Hong-sheng, Z., 2009. Genetic control of germination ability under cold stress in rice. Rice Sci. 16, 173180.


CHAPTER

Land and Water Management Strategies for the Improvement of Crop Production

13

Gabrijel Ondrasek, Zed Rengel, Dragutin Petosic and Vilim Filipovic

13.1 Introduction For successful implementation of various land and water strategies for the improvement of crop production, water status is of crucial importance—that is, the adequate (optimal) supply in the soilplant continuum (rhizosphere). Depending on the climatic and the hydropedological conditions of an agroecosystem, the soilplant water relationship is usually suboptimal during the vegetation period without appropriate waterland management strategies (e.g., absence of irrigation or drainage systems), particularly for rain-fed cropping. Thus, agricultural crop production is usually limited by one or both (at various times during a growing season) of the water stresses: water scarcity (Molden et al., 2011) and waterlogging (Mustac et al., 2011a; Singh, 2013). Water scarcity causes a stress by limiting readily available rhizosphere moisture and its uptake and release to the atmosphere in the evapotranspiration (ET) process, whereas waterlogging disturbs root access to air, causing root hypoxia and (in a long term) numerous associated soil constraints— salinity/alkalinity (Dang et al., 2006), ionic toxicity (Ondrasek et al., 2011), and soil compaction/ erosion (Petosic and Tomic, 2011). Both stress situations jeopardize crop production around the world and must be managed appropriately, often with relatively costly agrohydrotehnical strategies (Mustac et al., 2011b; Gjetvaj et al., 2012) depending on numerous environmental factors (e.g., hydropedology, geomorphology, geochemistry) (MacEwan et al., 2012). During the last decade managing the optimal water relationships in the root zone became increasingly challenging due to global climate change and variability, as evidenced by more frequent natural disasters such as droughts, heat waves, floods, and so on; this further threatens the suitability and stability of the principal environmental resources for food production. Another problem that has escalated in the world’s agroecosystems in the last few decades is a markedly reduced quality of natural resources due to different anthropogenic pressures (e.g., human population growth, pollution of land and water resources) (Schneider et al., 2011; Topcu and Kirda, 2013). Both natural and anthropogenic pressures require long-term and costly approaches for remediation and may not even be effective (e.g., in the case of highly contaminated resources). At present, the investments in the management of water and land resources to underpin increasing food demands are substantially below the level necessary to address the persistent food insecurity and to deal with natural resources’ vulnerability and scarcity (FAO, 2011). The same source P. Ahmad (Ed): Emerging Technologies and Management of Crop Stress Tolerance, Volume 2. DOI: http://dx.doi.org/10.1016/B978-0-12-800875-1.00013-2 © 2014 Elsevier Inc. All rights reserved.

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estimated that global investments in food production related to water strategies (i.e., irrigation development and management) will reach BUS$1 trillion in the period 2007 to 2050, whereas land strategies (i.e., land conservation and protection, flood control) may require an additional BUS$160 billion. Most of the investments will have a high probability of failure, notably in croplands of undeveloped countries, where cropping either in rain-fed (see Section 13.2.1) or irrigated conditions (see Section 13.2.2) may require implementation of sustainable and efficient strategies for water and/or land management.

13.2 Strategies for improving crop production in water-deficient agroecosystems A water deficiency, that is, negative water balance (2ΔW), can be defined in the case when total water output (Wout) exceeds total water input (Win) as follows: ΔW 5 Win (e.g., precipitation, irrigation, capillary rise, subsurface inflows) 2 Wout (e.g., evapotranspiration, runoff, deep percolation) (Ondrasek, 2014). However, even under positive ΔW, crops may be stressed by water deficiency due to exacerbation caused by various natural or anthropogenic (a)biotic factors (e.g., soil and water salinity, weeds, pests) (Vasileiadis et al., 2011; Zovko et al., 2013), thus demanding appropriate landwater strategies (see Section 13.3). The majority of modern long-term sustainable agricultural strategies focus on using water and land resources effectively (i.e., avoiding or reducing losses and quality deterioration) and efficiently (i.e., maximally increasing crop production), encompassed by the concept of water-use efficiency (WUE). The WUE concept is valid in both irrigated (Tanaskovik et al., 2011; Knox et al., 2012) and rain-fed conditions (Pereira et al., 2012). It describes the relationship between Win and agricultural production (e.g., crop yield, biomass), quantifying the relationship between delivered and used water volume in an agroecosystem (efficiency). Depending on the scale of an (sub)ecosystem, it is possible to define WUE, by the appropriate approach (e.g. Figure 13.1).

13.2.1 Improvement of crop production in rain-fed agriculture Of the global land area (13.2 billion ha) only B1.6 billion ha (12%) supports agricultural crops, whereas 3.7 billion ha (28%) are forests, 4.6 billion ha (35%) are grassland/woodland ecosystems, B2.8 billion ha (21%) are sparsely vegetated and barren, and the rest are urban zones and inland water bodies (Fischer et al., 2010). Rain-fed agriculture is the predominant crop production system globally, with B1.3 billion ha (80%) of cultivated areas contributing B60% (B2.4 billion tons) of global food production which uses B4000 km3 of water (IME, 2013; Ondrasek, 2014). Depending on climate and pedological conditions, rain-fed cropping is possible if annual precipitation reaches around 300 mm (FAO, 2011). Given that soilwater relationships can explain a predominant portion of yield variation in the field, temporal and spatial management of soil water may significantly improve crop production (i.e., WUE) by increasing crop yield (Figure 13.2) or enhancing its quality. For instance, in the case that available water in the rhizosphere is below the optimum (e.g., less than the full crop ET demand), first there will be a relatively low (curve section Aa) followed by a more progressive

FIGURE 13.1 A schematic presentation of the water use efficiency (WUE) in an irrigated corn field (furrow irrigation system) where a water supply is ensured from an unlined surface accumulation source and transferred to the field by an unlined open channel, assuming there is no any other water input (Win). Source: Adapted from Fairweather et al. (2002), Pereira et al. (2012), and Ondrasek (2014).

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FIGURE 13.2 Crop yield response curve in relation to water input (Win). Source: Adapted from Stirzaker (1999) and Grassini et al. (2011b).

(curve section Ab) response in crop yield with Win increasing until point B (see Figure 13.2). After so-called optimum point B, there should be no further significant changes in the yield with increased Win (curve section Bc); in contrast, at point C, further increases in Win are likely to induce the yield (curve section Cc) and water losses, and trigger other negative ecological/ economic implications (e.g., nutrient leaching, soil erosion, decreased yield quality). Particularly in rain-fed agroecosystems, it is possible to implement or integrate numerous land and water management strategies to improve crop production (i.e., WUE). A cropping system adaptation (opportunity cropping) is one such strategy that is widely used for mitigation of many (sub) soil constraints linked with rhizosphere water relations (i.e., salinity/alkalinity, organic matter depletion, desertification). This strategy encompasses a wide range of agricultural measures such as: (1) double cropping (consociation of cereals and forages or cereals and tree species— agroforestry; see later); (2) cultivation of more appropriate (e.g., deep-rooted perennials), and/or genetically improved (e.g., more salt-/drought-tolerant) crop genotypes; (3) changing crop establishment techniques—for example, from transplanted to direct seeded systems (dry seeding), from anaerobic to aerobic cultivation to avoid flooding of cultivated fields; (4) application of (in)organic mulching; (5) using conservation tillage systems (Figure 13.3); and so on. Conservation agriculture is practiced on B120 Mha worldwide (FAO, 2011) because of its numerous environmental benefits (Flower et al., 2012; Kassam et al., 2012). By leaving the crop residues or by applying additional organic mulch material on the soil surface (see Figure 13.3), some of Wout parameters (e.g., surface runoff, evaporation) can be efficiently reduced, conserving readily available water (and organic matter) in the root zone. Increasing or at least conserving soil organic matter has numerous benefits: for example, improved soil biodiversity/health, mitigation of land erosion and soil compaction, enhanced (rain)water infiltration, retained soil nutrients (decreased fertilizer requirement), and minimizing the impact of some potentially toxic elements. By focusing on the C and N cycles, soil conservation practices may enhance C sequestration and mitigate the release of greenhouse gases (GHG), which is important because the contribution of the agrisector to global

13.2 Strategies for improving crop production

295

FIGURE 13.3 Land conservation strategies for barley. Shown are (a) barley, (b) canola, (c) wheat (zero tillage in Western Australia), and (d) vegetable production (organic mulching) in Croatia. Source: Adapted from Ondrasek et al. (2011) and Ondrasek et al. (2013).

anthropogenic GHG emission amounts to 5 to 6 billion t CO2eq per year (1012%) (FAO, 2008). In intensive crop and livestock production area, N2O emissions from fertilized fields and animal waste may contribute .50% of the total GHG emissions from farms (FAO, 2011). In rain-fed agriculture where application of mineral fertilizers can be environmentally risky (see Figure 13.3a,b,c), application of organic fertilizers/amendments (Figure 13.3d) in combination with rainwater harvesting can be an effective alternative. Rainwater harvesting covers a wide spectrum of different systems, from the simplest O- or V-shaped topsoil structures with a planting pit (on plain terrains), over permanent terraces and/or runoff diversion systems (on slope terrains) to hydrotechnically the most complex large-scale structures (e.g., dams, accumulations, and/or retentions; see Section 13.3.3). Some of the most effective rainwater harvesting systems can boost yield by 2- to 3-fold compared to conventional rain-fed agriculture, especially when combined with improved crop varieties and minimum-tillage methods that conserve water (FAO, 2011). Agroforestry is an integrated land-use system in which woody perennials are consociated with agricultural crops and/or livestock to enhance beneficial interactions and balance ecological needs, combined with the sustainable harvesting of tree and forest resources (Thorlakson and Neufeldt, 2012; Vermeulen et al., 2012; Mbow et al., 2014). An example of a promising agroforestry

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cropping system is a consociation of the legume tree species Faidherbia (Acacia) albida and cereals, where grain yield can be several times higher under the tree canopy (4.1 t/ha) than in the open field (1.3 t/ha) (FAO, 2011). The multiple beneficial effects are brought about by a higher content of soil organic matter (minimum or no tillage), fertilizing effects (N fixation, leaf litter enriched with N compounds), and using crop residues as mulch. Also, unlike most other robust trees, Acacia albida drops the leaves during the rainy vegetation period, thus minimizing competition (i.e., for light, soil moisture, nutrients) with consociate crops.

13.2.2 Improving crop production in irrigated agriculture During the last several decades irrigation was one of the widely accepted and fast-growing strategies for combating water deficit (stress) in agroecosystems worldwide. From 1961 to 2009 the global area of cultivated land has grown by only 12% (from 13681527 Mha), whereas irrigated areas grew by almost 120% (from 139301 Mha) and areas under rain-fed systems slightly decreased (by 0.2%, from 12291226 Mha) (FAO, 2011, 2012), confirming a trend of agricultural intensification and transition from rain-fed to irrigated systems. However, the most recent data of the International Commission on Irrigation and Drainage (ICID, 2010) show that global irrigated areas have been relatively steady (between 290 and 300 Mha) since 1990s, with long-term projections indicating only a small expansion to 318 Mha by 2050, or 6% compared with the current area (FAO, 2011, 2012). Even such a relatively negligible increase in the irrigated area globally will be hard to achieve given strong demands for quality water resources in competitive industrial and municipal sectors. For instance, irrigated area (ha) per capita sharply decreased during the last decades from B0.05 in 1975 to B0.04 presently, and in accordance to some population projections could reach only B0.03 in 2050. So, the crucial challenges in the near future will be to retain sustainable and safe crop production in the world’s irrigated agroecosystems whose current contribution to global food supply is estimated at 40% (B1.6 billion tons). By 2050, it is estimated that food production in irrigated areas will increase by 40% (Tubiello and van der Velde, 2010), mostly due to increases in productivity (e.g., integrated pest and nutrient management, integrated plastic mulch cropping and lowpressurized fertigation, double/triple cropping). However, by 2050 demands for food could increase by 70%. Some of the crucial preconditions for achieving more intensive (productive) irrigated cropping assume successful institutional changes at (inter)national and regional levels (e.g., defined longterm land and water management strategies accompanied with effective policies) and infrastructural modernization (Gosling et al., 2011; Ondrasek, 2014). Modernization of (irrigated) agriculture includes technical, managerial and institutional upgrading of the system to improve resource utilization (labor, equipment, land, water) (e.g., FAO, 2011; Gosling et al., 2011), and thus enhance water productivity (i.e., WUE). For instance, taking into consideration the overall maximum biopotential of the most productive crops globally, a large gap still remains in water productivity (between the actual and attainable yield per unit of potentially usable water) in irrigated/rain-fed production of rice and wheat (Figure 13.4), clearly showing a need for modern alternatives for the improvement of WUE (explained later). Namely, rice cropping in certain low-efficient irrigation systems (unlined channel network for water supply, surface gravity irrigation systems) may demand up to 5 million liters of water per kilogram of product, whereas the losses of rice grain can reach up to 80% of the total production due to poor efficiency of the (post)harvest


297

FIGURE 13.4 Water productivity of cereals in a broad range of agroecosystems. (a) Rice in the lower Mekong River Basin in southwestern Asia and (b) maize in the Western Corn Belt of the United States. Source: Adapted from Sadras et al. (2010) and Grassini et al. (2011a,b).

practices and a lack of facilities for food storage/transport (see Ondrasek, 2014 and references therein). Contrary to rice, in irrigated maize cropping, water productivity (efficiency) is close to the full potential, i.e., only 14% below (see Figure 13.4), at least in part due to modern irrigation systems. Before the implementation of modernized (more efficient) irrigation systems, there are numerous possibilities to improve the overall system WUE, including (1) the optimal planning, design, and construction (e.g., avoiding the over- or under-capacity of the system, integration of irrigation and drainage systems to re-use drainage water), (2) management (e.g., irrigation rates/frequencies based on real-time crop requirements), and (3) maintenance (e.g., soil and water quality monitoring) (e.g., Romic et al., 2005; Tanaskovik et al., 2011). Better management of irrigation water appears to be the most feasible way of achieving large increases in water productivity (Sadras et al., 2010) in preference to irrigation system adaptation and/or modernization. Traditional surface irrigation methods predominate (.90% of the global irrigated land area), and have relatively low WUE (e.g., index of field application efficiency in gravity surface and drip irrigation system reaches 0.5 and 0.95, respectively). Thus, there is a significant potential for water saving via shifting from traditional to modern irrigation systems, or by modifying/upgrading particular elements of traditional systems (Ondrasek, 2014). Improved WUE and beneficial environmental impacts (reduced nutrients use/leaching, improved food quality) can also be achieved by optimizing irrigation management strategy to use (1) irrigation on plant demand (maintaining the rhizosphere moisture close to the water potential required to meet the full crop ET demands) or (2) deficit (supplemental) irrigation (substantially below the full crop ET demand) (Bos et al., 2009; Medici et al., 2014). In horticultural crop production (fruit trees, vineyards, and some vegetable crops), it is possible to implement a regulated deficit irrigation (RDI) and partial root-zone drying (PRD) irrigation strategy (Figure 13.5), aiming to control the generative/vegetative growth and development and/or the improvement in WUE. In RDI a plant water status is maintained within prescribed limits of deficit with respect to maximum water potential for a prescribed part or parts of the seasonal cycle of crop

298


FIGURE 13.5 Regulated deficit irrigation (1) and partial root-zone drying (2) irrigation strategy in a Zagreb County vineyard in Croatia, 2013. Source: Adapted from Ondrasek et al. (2013).

development, whereas in PRD a water deficit in the (partial) root zone (i.e., in B50% of its volume) is manipulated temporally and spatially (Bevery 12 weeks in different 50% of the root zone volume) to maintain a plant water status at optimal water potential and control vegetative growth for prescribed parts of the seasonal cycle of crop development (Kriedemann and Goodwin, 2002). For instance, in pome and stonefruits, some of the most responsive to RDI, optimal application for (regulated) deficit irrigation would be during the early summer when shoots grow rapidly and canopy expansion is maximal. In that stage, reduction in crop canopy due to RDI can improve orchard WUE (by 2530% compared to traditional irrigation methods), but also ensure better sunlight penetration and enhance initiation/differentiation of fruit buds for the next vegetation (Kriedemann and Goodwin, 2002). The PRD is a physiologically based concept, where roots exposed to dry conditions synthesize a hormonal signal (abscisic acid, ABA) and transport it to the shoots (leaves) inducing reduction in stomatal conductance (Leib et al., 2006)—that is, ET losses (Wout). Given that in PRD about 50% of the root zone is exposed to drying (responsible for the ABA supply) and the other 50% is kept well watered (responsible for the water supply), disturbances in plantwater relationships are minimal but water savings (WUE) may reach up to 50% (Leib et al., 2006). Recycling and reusing of marginal waters and wastewaters is another alternative for irrigated cropping (Sharpley, 2013; Sou/Dakouré et al., 2013), but only with effective regulation and application of the most advanced (albeit potentially expensive) technologies, water can be safely used, for example from surface/underground drainage systems (see Section 13.3.3.2), saline


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hydroresources and/or municipal or industrial effluents. For example, wastewaters are used in irrigating B20 million ha (7% of total irrigated area) (UNDP, 2006), and the use of treated wastewater is on the increase in urban areas, known as periurban cropping. Countries with the highest annual use (m3 per capita) of treated wastewater for irrigation are: Kuwait (82.3), United Arab Emirates (71.1), Qatar (51.7), Israel (46.4), and Cyprus (31.9) (Mateo-Sagasta and Burke, 2010). Given that different chemicals—trace elements, polyaromatic hydrocarbons (PAHs), radionucleotides—in wastewater may pose serious threats to humans and the ecosystems (Savic et al., 2013c and references therein), it is crucial to appropriately design and successfully implement policies and institutional regulations related to wastewater treatment and usage (Sato et al., 2013). Doing this is lacking in many developing and (un)developed countries. For instance, about 75% of all industrial and up to 95% of sewage effluents in the developing countries are discharged without any treatment into surface waters—the main hydrosources for irrigation in many countries (Ondrasek, 2014). Desalination, representing ,1% of the global water withdrawals, is mostly used for meeting water demands of the public sector in areas affected by water scarcity, and very rarely is used for irrigation of high-value crops. However, desalinized water (including drainage water), is becoming a more competitive option because the costs of expensive treatment technologies are declining while the costs of surface water and groundwater are increasing (FAO, 2011); nevertheless, it is unlikely that desalination could be one of the long-term strategies for mitigation of the increasing water demands in irrigated agriculture.

13.3 Strategies for improving crop production in (transiently) waterlogged agroecosystems 13.3.1 Types of waterlogging and the impact on crop production In contrast to water deficit, waterlogging occurs when total water input (Win) exceeds total water output (Wout) (i.e., a positive water balance; 1ΔW, see Section 13.2). Many interrelated factors are responsible for waterlogging (flooding as well) in agroecosystems. The most important ones are climatic, geomorphological, and hydropedological factors of the specific area. In the next section, we emphasize hydropedology; that is, interdisciplinary approaches to elucidate pedologic and hydrologic processes/interactions within a solum. From the hydropedological perspective, excessive soil water can be divided into two basic categories: surface and subsurface (ground). Surface water is often identified with the concept of excessive water because it stagnates on the surface of the agricultural land (Figure 13.6). According to the origin of the excessive water, it can be classified as internal (rain, storm) or external (runoff from higher ground) waters. In a broader sense, the appearance of rainwater is related primarily to the specific climatic conditions of the area, and then to soil geomorphology (i.e., pedology). External excess water flows into drainage areas from surrounding higher ground, or from flooding of natural or artificial watercourse areas (see Figure 13.6). Depending on the specific hydropedological microlocations, excessive subsurface water may occur at depth, saturating a part of the soil profile temporarily or permanently (Filipovic et al., 2013).

300


FIGURE 13.6 Flooding of wheat paddocks. This was done on hydromorphic soil of the amphigley type without a drainage system. Surface waters originated from extreme rainwater and by discharges from the surrounding channel network in Slavonia, Croatia, 2012.

The excess can be a consequence of a rising water table, or alternatively, in poorly permeable areas where incoming rainfall or runoff is retained in the top soil profile, because of a shallow clay layer with poor permeability (e.g., sand-over-clay soils in Western Australia), plough pan, or other types of compacted zones (Ondrasek et al., 2011). In amelioration drainage practice, one should distinguish: (1) slow-draining subsurface water, (2) stagnant subsurface water, and (3) groundwater (water table) (Petosic and Tomic, 2011; Petosic et al., 2012). Slow-draining and stagnant subsurface waters are the same type of water; the difference is only in the velocity of percolation through the soil profile (i.e., stagnant water having very low percolation velocity or even no percolation into deeper soil layers). Both types of waterlogging conditions usually occur in the upper part of the soil profile (0100 cm) as a result of the presence of poorly permeable soil horizons. The origin of this water is usually from rainfall. The term “groundwater” in the narrow sense means the water in the underground that completely saturates the soil that is below the water’s surface (water table) (Figure 13.7). Specifically, groundwater permanently fills soil pores of the aquifer, which have the lighter texture (gravel, sand) and lie above the impermeable (clay, rock) deeper layer. The soil profile can be divided into two zones from a hydrological point of view (see Figure 13.7). The first represents the unsaturated zone (vadoze zone), apart from the soil surface to the groundwater table in which the water is at a pressure head of less than atmospheric pressure; the second is the saturated zone in which groundwater is filling all the pore spaces in the soil and fractures of rock formations. In between there is a layer called the capillary fringe—that is, the pore space is partially filled with water (pressure less than that of the atmosphere) due to the influence of capillary forces. The effects of waterlogging in agricultural crop production can be manifested as: (1) short term (e.g., reduced fruit quantity/quality due to lack of O2, accumulation of CO2, ethylene and other organic products of the anaerobic metabolism, reduced performance of agrotechnical measures, and so on) and/or (2) long term (e.g., groundwater-induced soil salinity and associated subsoil constraints) (Ondrasek et al., 2011). For instance, groundwater-induced or seepage/dryland salinity


301

FIGURE 13.7 Water redistribution in the soil profile with three different ways of filling pore spaces. Source: Adapted from Filipovic et al. (2012).

is specific for the lowest positions when water flows relatively easily through the light-textured soils in upslope locations; however, it cannot move through the heavy soils at the footslope, causing waterlogging. It is induced by upward intrusion and/or capillary rising of the saline water table even up to topsoil, inducing soil salinization and associated constraints (e.g., alkalinity, Na/ Cl/B/Al toxicity, low permeability), thus restricting cropping in such an area (Dang et al., 2006; Ondrasek et al., 2011). For the majority of the most productive agricultural crops, depending on the current stage of growth/development (and duration), waterlogging causes a reduction in quality and quantity of crop yield, mostly due to oxygen deficiency—the major cause of waterlogging damage to crops. For instance, in the area of moderate continental climate (Croatia), the largest decrease in corn yield can be expected if waterlogging affects crops at the beginning of the growing season (AprilJune), whereas winter cereals do not tolerate long moisture periods at the end of their growing season (MayJune) and spring cereals in the middle of the growing season (AprilMay) (Petosic and Tomic, 2011). In humid Asian regions where soybean is growing, waterlogging before, at, or after germination causes severe seed and seedling damage (i.e., substantial reduction of grain yield at maturity), whereas after emergence it impairs root function (due to hypoxia) and thereby the capacity for nutrient uptake and growth (Kokubun, 2013). Depending on the soil’s characteristics in general, agricultural soils with a heavier texture should have relatively deep groundwater, whereas light-textured soils can tolerate relatively shallow groundwater (Petosic and Tomic, 2011) for achieving optimal crop yields. In the long term, permanent or periodic waterlogging of the

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rhizosphere is likely to result in some (sub)soil degradation, such as formation of halomorphic soils (explained before) or some specific limitations associated with hydromorphic soils (see next section).

13.3.2 Agriculture under waterlogging conditions of hydromorphic soils: a Croatian case study The Croatian agropedosphere is heterogeneous. Out of the total land area there (B5.7 Mha) agricultural land occupies B3 Mha, with 5 soil class orders and almost 40 soil types: 1. 2. 3. 4. 5.

the the the the the

order order order order order

of terrestrial or automorphic soils (7 classes and 23 soil types), of semiterrestrial soils (2 classes and 3 soil types), of hydromorphic soils (6 classes and 10 soil types), of halomorphic soils (2 classes and 2 soil types), and of subaquatic soils (2 classes and 2 soil types) (Basic, 2013; Bogunovic et al., 1998).

Hydromorphic soils have constraints regarding permanent or periodic waterlogging due to excessive (sub)surface waters; they are not necessarily salinized as in halomorphic soils. Croatia has one of the highest proportions of hydromorphic soils in Europe (Basic et al., 2007). They cover an area of B1.6 Mha (B30% of the national territory) (Basic, 2013); on around 50% of that area (0.8 Mha), sustainable crop production is almost impossible without implementation of appropriate land ameliorating strategies. Among hydromorphic soils dominant ones are pseudogley (B0.58 Mha) and eugley (B0.50 Mha), as well as hydromeliorated soils (B0.16 Mha) (Table 13.1). Hydromeliorated soils are those with installed subsurface (plastic pipe) drainage systems (see Section 13.3.3.2); currently at the national level, there are B0.73 Mha of soils completely ameliorated by surface (open-channel) drainage systems (see Section 13.3.3.1), and B0.33 Mha of soils partially ameliorated by surface drainage systems (Petosic et al., 2012). From the hydropedological perspective, Croatian hydromorphic soils are further classified into nine units according to excessively wet due to a slowly percolating and perched water table as well as groundwater within 2 m depth (Figure 13.8). The hydromorphic alluvial clay loamy and sandy clay loamy unit is wet due to surface water and groundwater linked to the stream water table, with moderately rapid average hydraulic conductivity (2.06.0 cm/h) (Figure 13.8), whereas the hydromorphic hypogleic silty clay loamy-to-loamy unit is characterized by a groundwater table up to the surface within horizons of moderately slow hydraulic conductivity (0.62.0 cm/h) (see Figure 13.8). Based on those differences, appropriate land amelioration measures (e.g., drainage systems) should be implemented in areas with some hydromorphic soil units (see next section) (Mustac et al., 2011a,b). For hydropedological soils in Croatia, the implementation of low-intensity basic drainage was estimated to be a priority on B0.13 Mha, and about 0.74 Mha would require both basic and detailed drainage (of higher intensity) (Vidacek et al., 2008).

13.3.3 Crop production improvement in waterlogged agroecosystems Depending on the specific characteristics of the agroecosystems (e.g., intensive agriculture on alluvial floodplains and foothills of hilly areas) there are certain requirements for the effective protection of the ameliorated area from the external waters (Romic et al., 2005, 2012; Zovko et al., 2013).


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Table 13.1 Classification and Distribution of Croatian Hydromorphic Soil Order Area Soil Class/Soil Profile Stratigraphy 1. Surface water gley soils A-Eg-Bg-C 2. Undeveloped soils (A)-C 3. Semigleys A-C-G 4. Gleys A-G 5. Histosols T-G 6. Anthropogenic hydromorfic soils P-G Total

Soil Type

ha

% of Total Land

% of Total Order

Pseudogley

577,025

10.3

35.7

Fluvisol

136,343

2.5

8.4

Humofluvisol

89,901

1.6

5.6

Pseudogley-gley Eugley Humogley Low peat

84,713 49,9526 64,555 2577

1.5 8.9 1.2 2.9

5.2 30.9 4.0

Hydroameliorated soil

163,000

0.05

10.1

1,617,640

29

100

Source: Adapted from Bogunovic et al. (1998).

FIGURE 13.8 Principal hydropedological units of Croatian hydromorphic soils. Source: Adapted from Vidacek et al. (2008) and Petosic and Tomic (2011).

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13.3.3.1 General, large-scale strategies The protection of agricultural fields from external waters is usually achieved by relatively simple hydrotechnical structures such as dikes, side channels, bypass channels, mountain, and/or lowland detentions/retentions (see next section), or by more technically-demanding constructions (e.g. pump stations). Some are more technically demanding constructions (e.g., pump stations) than others (Mustac et al., 2011a; Petosic and Tomic, 2011; Gjetvaj et al., 2012). A dike (i.e., embankment, levee) is an elongated ridge, naturally occurring or artificially constructed from fill material (e.g., soil from watercourse construction), protecting agricultural (urban) areas from flooding (Petosic and Tomic, 2011). There are different types of dikes including the most common, a major control dike (levee) built along the river banks. The control dike is almost always effective in preserving specific (vast) areas from large flooding events. The dikes can be constructed further from the river banks and a “berm” (a widening at a higher level than the riverbed) also can be constructed allowing low flows to continue in their natural-size channel and higher flows to occupy a greater area as levels rise, thus carrying large amounts of water. The side (lateral) channels are hydraulic structures with the basic purpose of protecting agricultural areas in the valley from excess water from higher terrains. Most often, redundant higherterrain waters threaten the lowland areas through flash floods and streams. The basic feature of these flash floods and streams is a torrential water regime characterized by sudden flood arrival. The fundamental purpose of the side channel is to collect all the flash flood water and streams from the higher ground and to take it to the main water recipient (river) in order to protect the lowland agricultural areas (Petosic et al., 2012). A bypass channel, also known as a flood-relief channel, is an artificially made waterway constructed in order to protect urban and rural agricultural areas from flooding. It is built to carry excess water from a main stream or river so that it is translocated into the lower parts of the same stream or into another stream with the ability to accept large amounts of excess water. There are two types of bypass channels regarding placement: parallel and transverse (vertical). The most common case of a parallel bypass/flood-relief channel is the one starting from the main river before the flood-prone part and reunites with the river after that part. In lowland areas, the construction of bypass channels is often combined with the construction of retention areas (Petosic and Tomic, 2011). The highland (mountain) and lowland detention/retention basins are also important natural or artificial structures for collecting the excess water from the ecosystems during rainy periods (Petosic and Tomic, 2011; Vorogushyn et al., 2012). The highland retention basins are built on rivers and/or streams in the hilly part of the basin. They can be single-purpose (detention) or multipurpose (detention/retention) hydrotechnical facilities. A detention basin, sometimes called a “dry pond,” is constructed in order to temporarily store water after a storm, but eventually it empties out at a controlled rate into a downstream water body. Its main purpose is to protect lowland amelioration areas from water flow from higher ground (mountain streams and flash floods) (Petosic et al., 2012). Unlike detention basins, the retention basins are built as multipurpose facilities—for example, for flood control in lowland areas and thereafter for the use of stored water for crop irrigation, domestic and recreational purposes, and so on. A retention basin is used to manage stormwater runoff to prevent flooding and downstream erosion and improve water quality in an adjacent river, stream, lake, or bay. Sometimes called a wet


305

pond or a wet detention basin, it is an artificial lake with vegetation around the perimeter; it includes a permanent pool of water in its design. The lowland detention/retention basins are usually located near the main water bodies or rivers and occupy the areas of natural depression in the landscape that are not used for agriculture because of year-round high groundwater. This area is mostly occupied by the native vegetation (forest, pastures) used in extensive agriculture. The difference from the higher-ground detention/retention basins is that they cover a much bigger area than the lowland ones, whereby excess water can be stored for long periods. The construction of lowland basins and their functioning is generally associated with other hydraulic structures and facilities (e.g., bypass canals, dams, dikes, pumping stations, syphons, traps).

13.3.3.2 Specific, small-scale strategies The main purpose of specific measures against flooding applied in the agroameliorative system is to drain excess water from productive agricultural fields (i.e., from the root zone on acceptable time scales). To achieve this effectively, the hydroamelioration drainage systems must satisfy several conditions. For instance, excess water needs to be removed from the ameliorative area and/or productive agricultural land quickly enough to avoid a negative impact on crop production (yield and quality). This removal time is dependent on the differences between crops with regard to tolerance to waterlogging and/or inundation, as well as the vegetation period in which excess water occurs. A drainage coefficient represents the amount of water to be removed from the specific area in time and is dependent on physical and hydraulic soil properties, the sensitivity of crops to waterlogging/inundation, the amount and/or intensity of rainfall, slope/shape and the catchment size, the water table position, and so forth. In addition, the agricultural drainage criteria may require a deep system, which can be hydrotechnically and/or economically difficult to achieve (Petosic and Tomic, 2011). In other words, specifying the highest permissible levels of the water table in the soil profile is dependent on the rooting zone depth.

13.3.3.2.1 Surface drainage systems using an open drainage-channel network This drainage system evacuates excess water from the crop fields by using the open natural watercourse and/or an artificial channel network to deliver water to the main recipient (river, accumulation, or retention basin). This system consists of different categories (classes) of drainage channels and is accompanied by hydraulic structures, usually pumping stations and floodgates, that enable efficient removal of water collected from the whole ameliorative area to the main water recipient (Figure 13.9). There is a possibility of using this system for the water supply in crop irrigation (e.g., a system upgrade by reverse pump stations). For instance, in southeastern European agroecosystems (Slovenia, Croatia, Serbia, Bosnia, and Herzegovina), one of the most common types of open drainage-channel system is a network with 3 to 4 channel classes (Romic et al., 2005; Petosic and Tomic, 2011; Savic et al., 2013c). Accordingly, the main (first class) channel’s hydraulic dimensions (e.g., drainage coefficient, flow velocities, depth, length) are the largest, depending on the size of the catchment; it receives water from the second and third (fourth) channel classes

306


FIGURE 13.9 A surface drainage system with an open drainage channel network in Posavina, Croatia. Source: Petosic et al. (unpublished).

(see Figure 13.9). In Croatia, the average basic hydraulic system measures of the first channel class (i.e., trapezoid shape in the cross-section) are: • • •

Base width from 3.0 to 10.0 m Depth of the channel from 3.0 to 3.5 m but can be up to 5.0 m Length of the slope (side) from 1.5 to 2.0 m but can be up to 2.5 to 3.0 m

In general, the surface drainage system has been shown to be effective for the removal of large amounts of excess water in a short period of time from the crop fields; it is also capable of retaining a large volume of excess water at relatively low slopes (0.150.50m) (Petosic and Tomic, 2011). However, the loss of the cropping area (up to 15%), the obstacles in carrying out farming operations (sowing, harvesting, spraying) and favorable conditions for growth of hydrophilic (herbaceous and woody) vegetation, and the requirement for periodic desilting (every 46 years) are the main disadvantages of this type of system (Petosic et al., 2011). Also, many recent studies have confirmed that drainage-channel sediments can be loaded with potentially toxic chemicals (e.g. trace metal elements, PAHs) and thus may represent a threat to adjacent crop production (Savic et al., 2013a,b).

13.3.3.2.2 Subsurface pipeline drainage systems Intensive development of this drainage system in Europe began in the late 1800s with the production of the first modern clay pipe; however, a significant shift in draining excess water through the pipe from agricultural land occurred after polyvinyl chloride (PVC) pipes began to be used during


307

FIGURE 13.10 Schematic representation of the combined drainage system of an amphigley soil type. Source: Filipovic and Petosic (unpublished).

the mid-20th century (Petosic and Tomic, 2011). The efficient functioning of this system depends on properly designed parameters. For instance, the depth of tile drainage is a function of several important factors, most notably the crop being grown, soil stratigraphy and layering, the possibility of a good runoff of collected excess water, tile drainage spacing, and a potential need for special land practices for deep interventions in the soil profile (see next section). For drainage amelioration practices in Croatia, the average depth at which the tile drainage is installed varies from 0.7 to 0.8 m for most vegetable crops, 0.8 to 1.1 m for cereal crops, and 1.2 to 1.6 m for perennialorchard crops (Petosic and Tomic, 2011). Tile spacing is one of the most important elements in the subsurface drainage system. The success of regulating an excessive groundwater level in hydromorphic soils in large part depends on the density of tile drains. Most of the approaches for determining the spacing of drainage and drainage nomograms are based on the Hooghoudt and Ernst approaches for steady flow conditions, or an equilibrium between the intensity of the arrival of water (rainfall intensity) and the intensity of the water drainage (flow intensity) in the system (Petosic and Tomic, 2011). Frequently employed in drainage practices worldwide is a combined system comprised of the surface (see previous section) and the subsurface pipeline (mole or chisel-tillage) drainage (see next section). Thus, the combined system is suitable for regulating excess surface and subsurface water simultaneously. The combined system is used especially for drainage of heavy-textured soils with low to very low hydraulic permeability (,6.0 cm/day) (Petosic and Tomic, 2011). In Croatia, the combined drainage system is used mostly for drainage of amphigley and pseudogley soils (Section 13.3.2); it consists of open channels of the third and fourth classes, tile drains (diameters of 50, 65, and 80 mm) with hydraulic filter material (gravel fraction 525 mm) with an average pipe spacing of 25 to 40 m and a depth of 0.8 to 1.1 m, as well as some additional amelioration measures (see next section) (Figure 13.10).

308


“Baula” Unplowed soil

“Baula” Shallow channel

FIGURE 13.11 A so-called “baula” drainage system with temporary shallow channels in Posavina, Croatia.

13.3.3.2.3 Possible other strategies to mitigate waterlogging A so-called “baula” drainage system (specific for central and southeastern Europe) was applied in Croatian agro conditions in the past on soils with a heavy texture (clay with low porosity) when the natural slope of the surface was insufficient to remove excess storm runoff (surface) water (Petosic and Tomic, 2011). This system reshapes the soil surface by a specific plowing technique that stacks furrows on top of each other (Figure 13.11). It creates ridges that have several variants such as a two-way baula system with permanent or temporary (shallow) channels (Figure 13.11). The main disadvantages of this drainage system are quite high maintenance costs with a relatively large loss of arable land, as well as unevenly developed crops and variable yields. Mole drainage (moling) is a special way of deep soil loosening and profiling. The drains can be described as unlined channels formed in a clay subsoil by a ripper blade with a cylindrical foot, often with an expander that compacts the channel wall. Depending on the specific soil-amelioration problem being dealt with, this system can be used separately and/or in combination with tile drainage (the most common in Croatia). In the combined system, a mole plough cuts the ground to a certain depth vertically, with a low incline rate that forms tentative moles or horizontal corridors; these are used for the collection and removal of mostly stagnating surface water toward the drainage ditch or tile drains. The successful implementation of mole drainage depends on stratigraphy/ texture of the soil profile, soil moisture during performance of moling, stability of structural aggregates, and so on (Petosic and Tomic, 2011). Multiannual observations under Croatian pedological conditions have confirmed that the best performance of this drainage system can be expected if clay content is .30%, the ratio of clay to silt is .0.5, the slope of moling is .0.5%, the depth is 50 to 60 cm, and the spacing is B5 m (Petosic and Tomic, 2011).


309

Deep vertical soil aeration is the amelioration practice that can be used with or without tile drainage. For instance, a long-term (19942011) combined drainage (with tile drainage and no drainage) and deep soil tillage (no till and chisel-tillage) experiment with a corn cropping system confirmed that subsurface tile drainage treatment significantly influenced the relative gas exchange in soils and improved corn yield (Nakajima and Lal, 2014). In general, deep soil tillage (in combination or without tile drainage) is applied mostly in pseudogley-gley soils or soils that have a problem of excess surface and subsoil water with a period of stagnation in a poorly permeable or nonporous, relatively shallow (3555 cm) Bt horizon (Section 13.3.2). Such soils are characterized by an unstable structure as a result of high silt content. The clay content in these soils is generally ,30%. In typical vertic soil types with clay content .40%, this measure should be avoided. It is performed in the direction of the terrain, or vertically, or diagonally to tile drainage with an incline of 5m. The depth of vertical soil aeration is usually 60 to 80 cm with 75 to 100 cm spacing (Petosic and Tomic, 2011). A laser land-leveling technique can be successfully implemented on parts of the crop field with excess surface water due to depressions in the topography. It also is widely used in land contouring for various irrigation practices (e.g., in surface irrigation systems), conserving water by reducing runoff, and allowing uniform distribution of water (e.g., Ondrasek, 2014).

13.4 Conclusion and future prospects Agroecosystems (especially rain-fed) are usually under periodic water stress: water scarcity or excess. To successfully manage agricultural crop production and minimize or avoid water stresses and related negative ecological consequences (e.g., crop yield and quality reduction, water and topsoil losses, nutrient leaching, contamination of hydroresources), appropriate long-term sustainable water and/or land strategies need to be implemented. Most of modern sustainable agricultural strategies (especially those against water scarcity) are encompassed by the concept of using principal natural resources (i.e., notably arable lands, fresh surface, and groundwater) more efficiently—that is, avoiding/reducing losses and quality deterioration with maximal increases of crop yield. For instance, in waterlogging agoecosystems crop production has been successfully improved by the implementation of an adequate (sub)surface drainage system(s) on B200 Mha, principally hydromorphic and/or halomorphic soil types. Some of the most employed strategies against water deficit in agroecosystems, such as irrigation and conservation agriculture, are currently implemented on B300 Mha and B120 Mha, respectively. However, some of the modern approaches for combating waterlogging/flooding (e.g., combined drainage systems) and water scarcity (e.g., irrigation) conservation (e.g., agricultural strategies) in croplands are challenged by the additional unfavorable impact of the modern era (i.e., global warming, climate change and variability, contamination, human population growth). Under such conditions, most existing strategies will need to be upgraded and modernized to be sustainable, including (sub)surface drainage systems combined with regular (every 35 years) additional land operations (moling, deep vertical soil aeration) in transiently waterlogged croplands, and/or an increased proportion (at the expense of traditional systems) of water-use efficiency systems/strategies (e.g., low-pressurize sprinklers/drip systems, deficit irrigation) for irrigated

310


cropping. Therefore, it is expected that in the future, successful long-term sustainable agricultural practices will be predominantly focused on the so-called WUE concept—that is, using water and land resources more effectively (avoiding or reducing losses and quality deterioration) and more efficiently (maximally increasing crop yield per unit of water).

Acknowledgments This work was partially supported by the Croatian Ministry of Agriculture, Council for Investigation in Agriculture (VIP), Contract 2012-11-02, and by Zagreb County. Additionally, it was supported by the People Programme (MC-IOF Action) of the European Union’s Seventh Framework Programme (FP7/2007-2013) under REA grant agreement number PIOF-GA-2012-330669.

References Basic, F., 2013. The Soils of Croatia. Springer, Dordrecht, The Netherlands. Basic, F., Bogunovic, M., Bozic, M., Husnjak, S., Juric, I., Kisic, I., et al., 2007. Regionalisation of Croatian agriculture. ACS 72 (1), 2738. Bogunovic, M., Vidacek, Z., Husnjak, S., Sraka, M., 1998. Inventory of soils in Croatia. ACS 63 (3), 105112. Bos, M.G., Kselik, R.A.L., Allen, R.G., Molden, D.J., 2009. Water Requirements for Irrigation and the Environment. Springer, New York. Dang, Y.P., Dalal, R.C., Routley, R., Schwenke, G.D., Daniells, I., 2006. Subsoil constraints to grain production in the cropping soils of the north-eastern region of Australia. Aust. J. Exp. Agr. 46, 1935. FAO, 2008 Financial mechanisms for adaptation to and mitigation of climate change in the food and agriculture sectors. High-Level Conference on World Food Security. Available at: ,ftp://ftp.fao.org/docrep/fao/ meeting/013/k2516e.pdf. (accessed 01.10.10). FAO, 2011. The State of the World’s Land and Water Resources for Food and Agriculture (SOLAW)— Managing Systems at Risk. Food and Agriculture Organization of the United Nations, Rome and Earthscan, London, p. 308. FAO, 2012. FAO water reports 38. Coping with water scarcity. An action framework for agriculture and food security. FAO, Rome, p. 100. Fairweather, H., Austin, N., Hope, M., 2002. Water use Efficiency, an Information Package. Irrigation Insights Number 5. Land & Water Australia, Canberra, ACT. Filipovic, V., Petosic, D., Nakic, Z., Mustac, I., Ruzicic, S., Zovko, M., et al., 2012. Identifying spatial and temporal variation of nitrate concentration in shallow groundwater aquifer. J. Food Agri. Environ. 10 (3/4), 10011004. Filipovic, V., Kodesova, R., Petosic, D., 2013. Experimental and mathematical modeling of water regime and nitrate dynamics on zero tension plate lysimeters in soil influenced by high groundwater table. Nutrient Cycling in Agroecosystems 95 (1), 2342. Flower, K.C., Cordingley, N., Ward, P.R., Weeks, C., 2012. Nitrogen, weed management and economics with cover crops in conservation agriculture in a Mediterranean climate. Field Crops Res. 132, 6375. Gjetvaj, G., Petosic, D., Mustac, I., 2012. Contribution of the melioration canal to the water regime of forest areas. Sci. Res. Essays 7 (17), 17161726.

References

311

Gosling, S.N., Arnell, N.W., Lowe, J.A., 2011. The implications of climate policy for avoided impacts on water scarcity. Proc. Environ. Sci. 6, 112121. Grassini, P., Thorburn, J., Burr, C., Cassman, K.G., 2011a. High-yield irrigated maize in the Western U.S. Corn Belt: I. On-farm yield, yield potential, and impact of agronomic practices. Field Crops Res. 120, 142150, doi: 10.1016. Grassini, P., Yang, H., Irmak, S., Thorburn, J., Burr, C., Cassman, K.G., 2011b. High-yield irrigated maize in the Western U.S. Corn Belt: II Irrigation management and crop water productivity. Field Crops Res. 120 (1), 133141. IME Institute of Mechanical Engineers, 2013. Global food: Waste not, Want not. Report. p. 35. Available from: ,www.imeche.org.. International Commission on Irrigation and Drainage in Agriculture (ICID), 2010. Available from: ,www. icid.org/imp_data.pdf.. Kassam, A., Friedrich, T., Derpsch, R., Lahmar, R., Mrabet, R., Basch, G., et al., 2012. Conservation agriculture in the dry Mediterranean climate. Field Crops Res. 132, 717. Knox, J.W., Kay, M.G., Weatherhead, E.K., 2012. Water regulation, crop production, and agricultural water management—understanding farmer perspectives on irrigation efficiency. Agri. Wat. Manag. 108, 38. Kokubun, M., 2013. Genetic and cultural improvement of soybean for waterlogged conditions in Asia. Field Crops Res. 152, 37. Kriedemann, P.E., Goodwin, I., 2002. Regulated deficit irrigation and partial rootzone drying. An overview of principles and applications. Irrigation Insights 3, Land & Water Australia, Canberra, 107 p. Leib, B.G., Caspari, H.W., Redulla, C.A., Andrews, P.K., Jabro, J.J., 2006. Partial root zone drying and deficit irrigation of “Fuji” apples in a semi-arid climate. Irrig. Sci. 24, 8599. MacEwan, R., Dahlhaus, P., Fawcett, J., 2012. Hydropedology, geomorphology, and groundwater processes in land degradation: case studies in south west Victoria, Australia. Hydropedology 449481. Mateo-Sagasta, J., Burke, J., 2010. Agriculture and water quality interactions. SOLAW Background Thematic Report TR08. Rome, FAO. Mbow, C., Van Noordwijk, M., Luedeling, E., Neufeldt, H., Minang, P.A., Kowero, G., 2014. Agroforestry solutions to address food security and climate change challenges in Africa. Cur. Op. Environ. Sustain. 6, 6167. Medici, L.O., Reinert, F., Carvalho, D.F., Kozak, M., Azevedo, R.A., 2014. What about keeping plants well watered? Environ. Experiment. Bot. 99, 3842. Molden, D., Vithanage, M., de Fraiture, C., Faures, J.M., Gordon, L., Molle, F., et al., 2011. Water availability and its use in agriculture. In: Peter Wilderer (Ed.), Treatise on Water Science. Elsevier, Oxford, pp. 707732. Mustac, I., Petosic, D., Gjetvaj, G., Filipovic, V., 2011a. Goundwater dynamics in drained soils of the Bidfield District. ACS 76 (1), 4147. Mustac, I., Gjetvaj, G., Petosic, D., Tomic, F., 2011b. Impact of the future multipurpose Danube-Sava Canal on groundwater dynamics. Tech. Gazzete 18, 211218. Nakajima, N., Lal, R., 2014. Tillage and drainage management effect on soil gas diffusivity. Soil. Till Res. 135, 7178. Ondrasek, G., 2014. Water scarcity and water stress in agriculture. In: Ahmad, P., Wani, M.R. (Eds.), Physiological Mechanisms and Adaptation Strategies in Plants under Changing Environment, Vol. 1. Springer, New York, pp. 7596. Ondrasek, G., Rengel, Z., Veres, S., 2011. Soil salinisation and salt stress in crop production. In: Shanker AK, Venkateswarlu B (eds) Abiotic stress in plants: mechanisms and adaptations, pp. 171190. Available from: ,www.intechopen.com/articles/show/title/soil-salinisationand-salt-stress-in-crop-production. (accessed 12.06.13).

312


Ondrasek, G., Bubalo, M., Knezevic, D., Romic, D., Zupanac, G., Vujec, L., et al., 2013. Perspectives for avoiding water stress in agriculture: Croatian example. CASEE Conference Food and Biomass Production—Basis for a Sustainable Rural Development, July 1-3, 2013, Zagreb, Croatia. Pereira, L.S., Cordery, I., Iacovides, I., 2012. Improved indicators of water use performance and productivity for sustainable water conservation and saving. Agri. Wat. Manag. 108, 3951. Petosic, D., Tomic, F., 2011. Management of Excessive Waters. University of Zagreb, Zagreb, Croatia, p. 106. Petosic, D., Marusic, J., Tomic, F., Mustac, I., Stricevic, I., 2012. The role and importance of melioration drainage in flood protection of R. Croatia. In: Biondic, D., Holjevic, D. (Eds.), Flood Protection in Croatia, Conference Proceedings, pp. 207221. Romic, D., Marusic, J., Petosic, D., Husnjak, S., Ondrasek, G., et al., National Project for Irrigation and Management by Agricultural Land and Water in Croatia (in Croatian only). University of Zagreb, Zagreb. Romic, D., Romic, M., Rengel, Z., Zovko, M., Bakic, H., Ondrasek, G., 2012. Trace metals in the coastal soils developed from estuarine floodplain sediments in the Croatian Mediterranean region. Environ. Geochem. Health 34 (4), 399416. Sadras, V.O., Grassini, P., Steduto, P., 2010. Status of water use efficiency of main crops. SOLAW Background Thematic Report TR07. FAO, Rome. Sato, T., Qadir, M., Yamamoto, S., Endo, T., Zahoor, A., 2013. Global, regional, and country level need for data on wastewater generation, treatment and use. Agri. Wat. Manag. 130, 113. Savic, R., Radovic, J.R., Ondrasek, G., Pantelic, S., 2013a. Occurrence and sources of polycyclic aromatic hydrocarbons (PAHs) in drainage channel sediments in Vojvodina (Serbia). Environ. Eng. Manag. J. Available from: http://dx.doi.org/10.1002/jsfa.6515. Savic, R., Maksimovic, L., Cimpeanu, S., Bucur, D., Ondrasek, G., Vasin, J., et al., 2013b. Hazardous and harmful substances in sediments of the Jegricka stream. J. Food Agric. Environ. 11 (1), 11521156. Savic, R., Ondrasek, G., Josimov-Dundjerski, J., 2013c. Heavy metals in agricultural landscapes as hazards to human and ecosystem health—a case study on zinc and cadmium in drainage channel sediments. J. Sci. Food Agric. submitted. Schneider, U.A., Havlı´k, P., Schmid, E., Valin, H., Mosnier, A., Obersteiner, M., et al., 2011. Impacts of population growth, economic development, and technical change on global food production and consumption. Agri. Syst. 104 (2), 204215. Sharpley, A.N., 2013. Agriculture, nutrient management, and water quality. Encyclopedia Biodiver. 95110. Singh, A., 2013. Groundwater modelling for the assessment of water management alternatives. J. Hydro. 481, 220229. Sou/Dakouré, M.Y., Mermoud, A., Yacouba, H., Boivin, P., 2013. Impacts of irrigation with industrial treated wastewater on soil properties. Geoderma 200201, 3139. Stirzaker, R., 1999. The problem of irrigated horticulture: matching the biophysical efficiency with the economic efficiency. Agroforest. Syst. 45, 187202. Tanaskovik, V., Cukaliev, O., Romic, D., Ondrasek, G., 2011. The influence of drip fertigation on water use efficiency in tomato crop production. ACS 76 (1), 5763. Thorlakson, T., Neufeldt, H., 2012. Reducing subsistence farmers’ vulnerability to climate change: evaluating the potential contributions of agroforestry in western Kenya. Agric. Food Secur. 1 (15), 113. Topcu, S., Kirda, C., 2013. Irrigation: Environmental Effects, In Reference Module in Earth Systems and Environmental Sciences. Elsevier. Tubiello, F., van der Velde, M., 2010. Land and water use options for climate change adaptation and mitigation in agriculture. SOLAW Background Thematic Report TR04A. Rome, FAO. Available at: ,www.fao. org/nr/solaw/. (accessed 07.08.12). UNDP, 2006. Human Development Report—Beyond Scarcity: Power, Poverty and the Global Water Crisis. United Nations Development Programme, New York.

References

313

Vasileiadis, V.P., Sattin, M., Otto, S., Veres, A., Pálinkás, Z., Ban, R., et al., 2011. Crop protection in European maize-based cropping systems: current practices and recommendations for innovative Integrated Pest Management. Agric. Sys. 104 (7), 533540. Vermeulen, S.J., Campbell, B.M., Ingram, J.S.I., 2012. Climate change and food systems. Annu. Rev. Environ. Resour. 37, 195222. Vidacek, Z., Bogunovic, M., Husnjak, S., Sraka, M., Bensa, A., 2008. Hydropedological map of the Republic of Croatia. ACS 73 (2), 6774. Vorogushyn, S., Lindenschmidt, K.-E., Kreibich, H., Apel, H., Merz, B., 2012. Analysis of a detention basin impact on dike failure probabilities and flood risk for a channel-dike-floodplain system along the river Elbe, Germany. J. Hydro. 436437, 120131. Zovko, M., Romic, D., Romic, M., Bakic, H., Ondrasek, G., 2013. Soil and water management for sustained agriculture in alluvial plains and floodplains exposed to salinity: a case of Neretva River Valley. In: Ahmad, P., Azooz, M.M., Prasad, M.N.V. (Eds.), Ecophysiology and Responses of Plants under Salt Stress. Springer, New York, pp. 473494.


CHAPTER

Integrating Physiological and Genetic Approaches for Improving Drought Tolerance in Crops

14

Ahmad Ali, Zeshan Ali, Umar M. Quraishi, Alvina Gul Kazi, Riffat N. Malik, Hassan Sher and Abdul Mujeeb-Kazi

14.1 Introduction Water is an essential ecological element in all ecosystems. Its availability, distribution, and quality affect the human population in all regions on Earth. Water scarcity is one of the greatest challenges faced by humankind in the 21st century (Ahmad and Yasin, 2006; Kahlown et al., 2007). Increasing water demand in urban/industrial sectors and conventional irrigation practices have created water shortages for the agricultural sector (Fedoroff et al., 2010). Globally water resources are unevenly distributed; some countries are blessed with plenty of this renewable resource whereas others are facing chronic water shortages (Pereira et al., 2002). Wise management of available water resources, recycling by suitable means, and efficient utilization in different water-consumption sectors can conserve water in voluminous amounts to serve future generations. Water scarcity is broadly divided into two types: economic and physical. Physical water scarcity prevails in those regions where surface and groundwater resources are inadequate to supply the region’s water demands. In economic water scarcity regions, water resources are abundant but scarcity is observed due to mismanagement of optimally available supplies. In most countries, economic water scarcity is more prevalent than physical, which is attributable to poor management of available supplies and overexploitation of water in industrial, urban, recreational, agricultural, and other sectors. In Pakistan, economic water scarcity prevails and available resources are continuously on the decline. Agriculture is the largest consumer of freshwater and losses are very high as a result of mismanagement, provincial disputes, and conventional irrigation practices (Saeed et al., 2002; Pakistan Economic Survey, 2010). Pakistan has one of the largest canal systems in the world, which supplies water to nearly 86% of the irrigated areas (18 million ha) producing around 90% of the food/fiber requirements of the country. The remaining 13% of the total cultivated area (B23.38 million ha) is entirely rain-fed (GoP, 2008) (Figure 14.1). The approximate percentages of rain-fed areas in different provinces are Punjab (15%), Khyber-Pakhtunkhwa (57%), Baluchistan (90%), Sindh (55%), Federally Administered Tribal Areas (50%), and Azad Kashmir (95%). P. Ahmad (Ed): Emerging Technologies and Management of Crop Stress Tolerance, Volume 2. DOI: http://dx.doi.org/10.1016/B978-0-12-800875-1.00014-4 © 2014 Elsevier Inc. All rights reserved.

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CHAPTER 14 Integrating Physiological and Genetic Approaches

CHINA

AFGHANISTAN

INDIA Legend

IRAN

ARABIAN SEA 0

Irrigated areas Rain-fed areas River flow direction Provinces Cities Province boundary River 150 300 450

600

Kilometers

FIGURE 14.1 Irrigated and rain-fed areas of Pakistan.

Declining water availability is adversely affecting food security because most of the food/fiber requirements are met from the irrigated areas. Climate change and global warming are also affecting rainfall patterns, which in turn may further decrease agricultural productivity in the rain-fed areas of Pakistan. According to some statistics, per capita water availability in 2010 had declined to ,1000 m3; it was 5600 m3 on Pakistan’s independence in 1947 (Martin et al., 2006). Under current circumstances, the country will soon be in a condition of outright water scarcity due to mismanagement in the major water utilization sectors. Pakistan fulfills its water demands from surface and underground water resources. Surface water supplies are mainly driven by the Indus river system, including all major and small rivers that drain B944,569 km2 of the catchment area (Pakistan Water Sector Strategy, 2002). Riverine water supplies are not uniform in the two main agricultural seasons (i.e., Kharif and Rabi). In Kharif (summer season), water supplies are at a peak due to snow/glacier melt and abundant rainfalls; however, low flow periods have been recorded for the Rabi season (Agricultural Statistics of Pakistan, 2011; Shaheen and Baig, 2011). Nearly 40 million acre feet (MAF) per annum of freshwater input is delivered to the riverine system through rainfall (monsoons). Rainfall patterns are becoming erratic due to the changing climate in the region. Groundwater contributes 40% of the total available freshwater supplies per annum. Across all provinces, this underground resource is exploited to the maximum (Kahlown et al., 2004). The stress is greater in the heavily populated areas where water is used not only for urban needs but also in industrial and agricultural activities (Pakistan Water Partnership, 1999). The delicate

14.1 Introduction

317

FIGURE 14.2 Dams on the western and eastern rivers’ headwater regions in Indian territories.

equilibrium between water withdrawal and water recharge is disturbed resulting in the decline of water levels at an alarming rate of 30 to 40 cm/year (Pakistan Country WRAS, 2005; Shakir et al., 2011). Fewer water storage bodies, conveyance losses through conventional irrigation systems, inadequate maintenance/sedimentation of water channels/reservoirs, and nonadoption of highefficiency irrigation systems (HEIS) are adding to rising water scarcity issues in Pakistan (Hsiao et al., 2007; Shakir and Qureshi, 2007). Construction of dams, reservoirs, and hydroelectric power projects on the eastern and western rivers near India at several headwater sources also significantly contribute to Pakistan’s increasing water scarcity problems (Figure 14.2). The twin menace of water scarcity and water quality is compromising agricultural productivity in Pakistan. Declining water availability (i.e., water scarcity) has led farmers to use wastewater for irrigation, which is a serious health concern (Ensink et al., 2002). Irrigating with raw domestic and industrial effluents has raised issues regarding food safety (Nan et al., 2002). Contaminants accumulate in the plants and on consumption affect human and livestock health. In addition, higher levels of inorganic/ organic contaminants in the wastewater affect plant growth and metabolism (Gupta and Sinha, 2007). It is known that the available surface water and groundwater supplies for agriculture are significantly contaminated due to unchecked disposal of domestic and industrial effluents (Ali et al., 2013b). Expanding population and industrial activities are responsible for the generation of a large amount of wastewater leading to environmental degradation (Qadir et al., 2003, 2010). The population is expected to grow .260 million by the year 2025, followed by increased water demands and wastewater discharge from urban centers. Similarly, more industrial areas will be established to

318


meet increasing human needs, reciprocally increasing water consumption and more discharge from industries. Agriculture is the major sector that will need more water to meet the food/fiber requirements of an increasing population. All water utilization sectors across Pakistan generate 4369 million m3 of wastewater/annum out of 180,000185,000 million m3 of available freshwater/annum. Wastewater treatment globally is not prioritized and nearly 90% of the total generated ends up in freshwater channels and open lands that leach into underground aquifers and the ocean. In Pakistan there is no effective treatment system for municipal and industrial wastewaters. To cope with the scarcity of freshwater and to minimize health risks associated with the wastewater and deteriorating water and environmental quality, a cost-effective, sustainable, and viable wastewater treatment system may be the solution to all the related problems (Ali et al., 2013a,c). Sufficient food production is one of the main challenges worldwide and this is directly related to water availability. However, water is expected to be one of the most critical natural resources during the next century. The International Water Management Institute (IWMI) estimates that, by 2025, cereal production will have to increase by 38% to meet food demands (Seckler et al., 1999). One of the most important issues in the world’s food policy debate is whether more demand will require large investments in additional irrigation systems or whether increased area and yields from rain-fed agriculture can satisfy at least a substantial part of the demand. This issue has gained in importance because water in developing countries is becoming increasingly scarce, water development increasingly expensive, and in some cases environmentally destructive. Rain-fed agriculture is of increasing importance across the globe in view of its inherent problem of low or sparse rainfall that is attenuated by climate change. Rain-fed areas, although they vary from region to region, are important in terms of agriculture because more of the poor live in these areas. About 60% of the world’s population that faces food insecurity resides in South Asia and sub-Saharan Africa. Most of these areas are rain-fed and there are several challenges in terms of area, extent, and future perspectives to improve livelihood. It has been reported that there is an increased frequency of extreme events (e.g., drought, floods, and hurricanes) due to climate change. Many scenarios indicate that losses of rain-fed production areas (1020%) are expected to affect nearly 1.2 billion people by 2080 (IIASA, 2002). Climate change has been reported to adversely affect water availability and food production, and as a result, land degradation, poverty, and food insecurity are expected to grow to menacing proportions (Wani et al., 2009, 2011). Pakistan is a country of more than 19 million people with wheat being its staple crop. About one-third of the wheat is grown under rain-fed (barani) conditions every year but the yield is extremely low. In spite of the fact that wheat acreage covers the maximum of all the crops in rainfed areas, production is not enough to meet the area’s total requirements. In short, the scarcity of water has seriously restricted the social and economic improvement of the nation in general and the populous of barani areas specifically. The problem may be clearly understood by comparing the wheat production level of irrigated versus rain-fed areas in the country (Table 14.1). Drought is one of the serious constraints for global agriculture; it has been projected to worsen with the likely climate change. Interdisciplinary sciencists are trying to identify and dissect plant drought-tolerance mechanisms through various approaches with limited success so far. Precise breeding methodologies and advanced phenotyping techniques, along with modern genetics and genomics approaches, may be able to unravel metabolic processes and the genes to produce crops with tolerance to drought.

14.2 Drought stress in changing environments

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Table 14.1 Wheat Statistics for Rain-fed and Irrigated Areas of Pakistan Years

Location

Area (000s of ha)

Production (Million tons)

kg/ha

200809

Irrigated Rain-fed Irrigated Rain-fed Irrigated Rain-fed Irrigated Rain-fed

7821.0 1225.0 8075.5 1056.2 7712.5 1188.2 8055.4 1156.4

22.41 1.62 22.37 0.94 23.72 1.49 24.00 1.48

2865.0 1324.0 2770.0 893.0 3076.0 1254.0 2894.0 1222.0

200910 201011 201112

Source: Pakistan Bureau of Statistics (2012).

The following sections discuss drought stress, plants’ drought stress responses, and precision phenotyping approaches with regard to advances in plant physiology for implementation of the genetic and molecular strategies needed to explore the complex drought-tolerance mechanisms. Crop improvement based on molecular breeding approaches, including the discovery of genes through association and linkage mapping, are also addressed. Molecular dissections of drought tolerance by quantitative trait loci (QTL), candidate gene identification, QTL cloning, functional genomics, and transcriptomics are also discussed.

14.2 Drought stress in changing environments Drought has been understood and accordingly defined differently under a variety of perspectives. It has been classified into four categories by the US National Drought Mitigation Center (NDMC) at Nebraska University in Lincoln: socioeconomic, hydrological, agricultural, and meteorological. In this chapter, drought is being discussed as an agricultural drought, which occurs when soil water in a sufficient quantity is not available for normal growth and development of a crop at a particular time (NDMC, 2006). The seriousness of drought stress depends on its timing, duration, and intensity (Serraj et al., 2005; Vadez et al., 2011). It is predicted that the occurrence of drought in many foodproducing regions will rise significantly as a result of climate change (Reynolds and Ortiz, 2010). On the other hand, drought tolerance is plants’ capability to live, grow, and reproduce adequately with a limited supply of water or under intermittent water shortage conditions. Drought tolerance is a complex quantitative trait controlled by several small-effect genes or QTLs. This often may be confounded by differences in plants’ phenology (Fleury et al., 2010; Atkinson and Urwin, 2012). It has been projected that developing countries will be severely affected due to climate change by 2030 because: (1) population growth will occur mostly in these countries, (2) the impact will be more severe in the tropics and subtropics, and (3) the proportion of the workforce associated with agriculture is the highest in developing countries (Reynolds and Ortiz, 2010). However, converging

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population growth with variable climate is expected to be a menace to food security on a global scale. It is also a fact that occurrences of drought have become endemic, which is a serious concern, due to climate change. There is a huge responsibility on scientists’ shoulders to develop drought-tolerant plant varieties with optimized yield and stability through modern breeding and modified genetic approaches (Reynolds and Ortiz, 2010).

14.3 Water deficit as a major abiotic factor limiting crop yields Abiotic stress is any single or combination of environmental conditions that impose negative effects on plant growth, genetic potential, development, and reproduction (Acevedo et al., 2002; Feng et al., 2011; Krasensky and Jonak, 2012; Ma et al., 2012). Drought, heat, low temperatures, and soil salinity are some of the most important abiotic stresses that have deleterious effects on wheat yield in large areas worldwide. The key limitations to plant productivity is water availability, verified by the fact that almost 45% of the world’s agricultural lands are subject to continuous or frequent water deficiency (Ashraf and Fooland, 2007). This can result in up to 50% yield loss, or complete crop failure, under severe conditions. Thus, developing drought-tolerant crops in the near future is undoubtedly a critical requirement for the enhancement of agricultural productivity.

14.4 Crop growth and response to water deficits The term “economic yield,” or biological yield, generally is used to explain crop production. The dry matter that is useful economically is the known as economic yield while total plant dry matter at the time of harvest is the biological yield. For wheat, economic yield is grain yield and biological yield equals aboveground dry matter because roots are not harvested. Economic yield and biological yield can be related by using the harvest index (HI), which represents the proportion of aboveground biomass allocated to harvested grain (Loss and Siddique, 1994). Cereals are grown mainly for grain yield that, for example, in wheat is the function of the number of plants per unit area, the number of grains per spike, and grain weight. Factors that affect one of these components directly or indirectly will affect grain yield. Drought adversely affects these components, resulting in a marked decline in grain yield. Fischer and Maurer (1978) reported a decrease in average grain yield by 37 to 86% when durum wheats, triticales, barley, and bread wheats were subjected to drought by withholding irrigation at various stages before anthesis. In Pakistan, drought at postanthesis is a frequent phenomenon that results in wheat yield loss. Water deficit reduces leaf area in most crop species, for example, by 35% in wheat (Siopongco et al., 2006). Because leaf area is influenced by phenology, stem morphology, rates of emergence, and potential size, any effect of water deficit on these factors can also modify it. Blum (1996) reported reduced leaf area in wheat caused by total cessation of the appearance of new tillers. Another important characteristic during drought stress is deep rooting (Pugnaire et al., 1999; Aroca et al., 2012) enabling crops (e.g., wheat and rice) to take water from deeper layers of the soil profile, thus accessing more water. At the same time, deep roots may not be advantageous in the case of availability of small amounts of soil water because there is inadequate water to extract

14.4 Crop growth and response to water deficits

321

(Siopongco et al., 2006). The benefit of a deep root system in terms of its adaptation to drought stress depends on stress duration, water-holding capacity of soil, and amount of water present in the deeper soil layers (Kamoshita et al., 2001). Chlorophyll molecules harvest light energy used to produce chemical energy such as adenosine50 -triphosphate (ATP) and nicotinamide adenine dinucleotide phosphate-oxidase (NADPH) (Taiz and Zeiger, 2006; Chutia and Borah, 2012). Significant reductions of chlorophyll and carotenoid content in hexaploid and diploid wheat subjected to drought for 10 d at 50, 60, and 70 d after sowing have been reported by Chandrasekar et al. (2000). Drought enhances senescence by increasing chlorophyll degradation, lipid peroxidation, and nitrogen loss (Yang et al., 2001). Similarly, Liu et al. (2006) observed marked increases in electrolyte leakage and decreases in Chl a and Chl b in wheat cultivars subjected to water stress conditions. The combination of the continued impact of drought and high temperatures impairs photosynthesis during the daytime and increases surface temperatures at night, which in turn increases the photorespiratory losses and thus productivity. Leaf growth is reduced more than root growth during water deficit conditions, resulting in an increase in the rootshoot ratio because of the greater photosynthate supply to the roots, thus leading to a greater proportion of roots. This increase helps improve the ability of the root system to take in more water per unit of shoot area by exploring the maximum volume of soil that otherwise may not be possible (Pugnaire et al., 1999). Abiotic stresses, including drought, often lead to the overproduction of highly toxic and reactive oxygen species (ROS) in plants because of high electron leakage toward oxygen during the respiratory and photosynthetic processes. This causes harm to carbohydrates, proteins, lipids, and DNA resulting, ultimately, in oxidative stress, which has been well documented in crop plants (Asada, 1999; Gill and Tuteja, 2010). It contains free radicals (i.e., OH2, hydroxyl radicals; O22, superoxide radicals; RO0 , alkoxy radicals; and HO22, perhydroxy radicals) as well as molecular (nonradical) forms (i.e., 1O2, singlet oxygen; H2O2, hydrogen peroxide). Photosystems I and II in the chloroplast are the main sites for the production of O22 and 1O2, while in the mitochondria, complex I and complex III of the electron transport chain are the sites for O22 (Gill and Tuteja, 2010). Plants have antioxidant enzymatic systems to protect them against the adverse effects of ROS. These include superoxide dismutase (SOD), ascorbate peroxidase (APX), glutathione peroxidase (GPX), glutathione-S-transferase (GST), and catalase (CAT); they are present in almost all cellular compartments (Mittler et al., 2004; Gill et al., 2011). Further, proline as a nonenzymatic antioxidant has been reported and can work against the inhibitory effects of ROS (Chen and Dickman, 2005). Mishra et al. (1993) studied changes in the activities of antioxidant enzymes in wheat leaves during exposure to strong visible light at different temperatures in the presence of protein synthesis inhibitors; they observed significantly increased activities of SOD and APX, indicating an increase in the rate of generation of ROS. The activities of CAT, on the other hand, decreased under stress conditions which may be due to its photolability, particularly at a lower temperature. The increased enzyme activities, except for CAT, in response to stress conditions revealed that they play an important role in the protection of higher plants from the damaging effects of toxic ROS. Similarly, the role of plant antioxidant systems in stress tolerance was studied by Sairam et al. (1998) in leaves of three contrasting wheat genotypes. Antioxidant enzymes (e.g., SOD, APX, and CAT) significantly increased under water stress. The authors also concluded that H2O2 scavenging systems, as represented by APX and CAT, were more important in imparting tolerance against droughtinduced oxidative stress than SOD alone.

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14.5 Osmotic adjustment during drought stress Osmoregulation is a specific form of solute accumulation that regulates turgor pressure and hydration during drought periods, with positive effects on growth (DaCosta and Huang, 2006). Solute accumulation in wheat is reported to be an adaptive strategy to mitigate drought conditions (Morgan, 1977). Other crop species, such as barley and sorghum, have also been shown to osmoregulate under drought conditions (Blum, 2005). In wheat, genotypic differences in osmoregulation tend to be discrete, with responses being either high or low. Morgan (1983) selected wheat lines for higher osmoregulation in segregating populations in the greenhouse. The selected lines had greater growth and seed yields under water-limited conditions in the field and single-gene control of osmoregulation was suggested in wheat. Wheat genotypes with high osmoregulation capacity started to accumulate solutes immediately at the onset of drought, whereas the genotypes with low osmoregulation capacity failed to accumulate solutes right away. Despite this successful research, the difficulties associated with osmoregulation studies and analyses have so far prevented the application of this trait in plant breeding. One of the most common plant responses under water deficit is an increase in the different types of compatible organic solutes (Serraj and Sinclair, 2002). Compatible solutes include proline, sucrose, polyols, trehalose, and quaternary ammonium compounds (e.g., glycinebetaine, alaninebetaine, prolinebetaine, and hydroxyprolinebetaine) (Rhodes and Hanson, 1993). Proline in plants is largely observed when subjected to drought stress where it accumulates largely in the cytosol and contributes substantially to the cytoplasmic OA (Ashraf and Fooland, 2007). The normal amount of free proline in plants is usually low, ranging between 0.2 and 0.7 mg g21 dry matter. This rapidly rises to between 40 and 50 mg g21 dry matter during slow dehydration of tissues. In wheat, an increase of proline and asparagines in the leaves has been associated with adaptation to severe conditions such as winter stress or drought. Increases in sugar content, especially in the youngest growing leaves where contributions to OA can be substantial, are an important adaptive response to water deficit; it accumulates when utilization (i.e., growth, translocation, and polysaccharide synthesis) is reduced relative to photosynthesis (Lei et al., 2006; Xue et al., 2008). Similarly, during drought stress, linear increases in soluble sugar concentrations, with a decrease in osmotic potential playing a role in OA, have been observed in field-grown sorghum. Accumulation of sugars, such as trehalose, sucrose, and raffinose, can help protect membrane integrity under cellular water deficits by replacing water molecules (Bohnert et al., 1995).

14.6 Methodologies for screening genotypes under drought stress Field evaluation of genotypes (e.g., for OA) is difficult to control because of the influence from the relevant environmental conditions as well as other field confounding factors (Chandra Babu et al., 1999); still, such evaluations provide useful information about adaptation of genotypes to drought stress. The field environment permits steady acclimation to water shortage (Fereres et al., 1978). For instance, OA could be useful when a high level of soil water can be exploited through continued development of plant roots at depth (Wright et al., 1983). Similar evaluation under controlled conditions (e.g., controlled-environment chambers or glasshouses), where photoperiod, water

14.7 Key physiological attributes for targeted breeding programs

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management, temperature, and nutrition can be imposed more accurately, is also recommended. Some of these have been used successfully in pots in the glasshouses for wheat breeding (Morgan et al., 1986). However, because of the limited volume of soil water accessible to roots in small pots, the rate of drought imposition under controlled experimental conditions can be more rapid than in the field (Fereres et al., 1978); thus, such experiments under controlled conditions should be integrated with field measurements. Polyethylene glycols (PEGs) are osmotically active molecules that are highly water soluble, not permeable to biological membranes, and available in a range of molecular weights ranging from 200 to 20,000. PEGs with molecular weights from 4000 to 8000 are more commonly being used in physiological experiments to induce stress under controlled nutrient culture solutions through water potential decrease of the medium; this, thus, decreases the availability of water to plants (Steuter et al., 1981) and ultimately the water potential to the plant. Further, PEGs of 1000, 4000, and 20,000 were observed to block the water movement pathway, reduce absorption of water, and cause plant desiccation (Lawlor, 1970). The study of plant responses to PEG-induced drought stress is mostly associated with the water relationship of plants, chlorophyll content, antioxidant enzymes, and other osmoprotectants. Drought stress evaluation under both laboratory and field conditions may provide information on plant water deficit tolerance at the levels of the tissues and crop community. To understand the complexity of crop responses to drought stress, it is necessary to explore their physiological and genetic roots (Sinclair, 2011). The latest advances in phenotyping approaches, physiological insights, and genomics have added to agriculturists’ understanding of droughttolerance mechanisms, and crop breeders now have access to ample knowledge about the gene networks for plant improvement to increase crop yield (Tuberosa and Salvi, 2006). Plant physiology facilitates comprehension of drought tolerance-related attributes and the complex mechanisms involved, while genomics and molecular biology approaches can lead to the QTLs and candidate genes linked with these attributes (Varshney et al., 2011). Several reviews pertaining to drought stress and plant responses are available in the literature for different crop plants including wheat (Fleury et al., 2010), maize (Tsonev et al., 2009), rice (Bernier et al., 2008; Chen et al., 2013), and pearl millet (Yadav et al., 2011). Also, the descriptions of the molecularphysiological mechanisms of drought tolerance have been outlined by several reviews (Bartels and Sunkar, 2005; Maggio et al., 2006; Bressan et al., 2009; Charron and Quatrano, 2009). Molecular dissections of drought tolerance by QTL, candidate gene identification, QTL cloning, functional genomics, and transcriptomics have also been studied.

14.7 Key physiological attributes for targeted breeding programs Using physiological attributes (PAs) in a breeding program depends on their relative genetic correlation with yield, level of genetic variation, heritability, and genotype 3 environment interactions. Under water-limited conditions, superior photosynthesis, accumulation and remobilization of stem reserves, different stress-tolerant enzymes, osmotic adjustment, and so on are important PAs. Detection of such drought-adaptive PAs and the mechanisms involved is laborious, costly, and time consuming; however, the benefits are likely to be significant if successful. The information on potential PAs can be collected on parental lines that involve screening either a whole crossing

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block, or a set of frequently used parents. This thus increases the probability of transgressive segregation, ultimately bringing desirable attributes together. Further, if resources are not the limitation, tests for PAs may be extended to segregate generations in yield trials, depending on when genetic gains from selection are optimal (Reynolds et al., 2000; Qin et al., 2011; Wasson et al., 2012). Breeding approaches based on specific PAs are useful only if defined appropriately in terms of the developmental stage of the plant, the specific attributes of the target environment for which they are adaptive, and their potential role in yield (Reynolds and Trethowan, 2007; Mujeeb-Kazi et al., 2013; Ogbonnaya et al., 2013). Drought escape, for example, under water-limited conditions via manipulation of plant phenology is a commonly used genetic approach for relative yield stability (Richards, 1991). Finally, if considerable genetic diversity is established for a particular physiological trait in a genotype collection of a given species, it is then necessary that the importance of the attribute as a selection criterion be determined. The three important drivers suggested by Passioura (1977) for drought yield adaptation are: (1) water-use efficiency (WUE), (2) water uptake (WU), and (3) harvest index (HI). In the case of WU, measurements related to stomatal conductance, such as canopy temperature (CT), offer indirect indicators of uptake by roots (Reynolds and Tuberosa, 2008). For WUE, carbon isotope discrimination, which is based on the higher affinity of the carbon-fixing enzyme (Rubisco) for the more common 12C isotope over the less common 13C, seems to be the best approximation (e.g., a lower discrimination value indicates higher WUE). Signaling molecules, such as abscisic acid (ABA), photoprotective mechanisms including antioxidant systems, regulation of water flow via aquaporins, and spike photosynthesis in cereals, are the other attributes associated with WUE. In the same context, the extreme sensitivity of reproductive processes to drought may result in reproductive failure, which is associated with low HI. In a nutshell, steady HI is linked with higher yield potential (Blum, 2009, 2011), while WU is important for increasing yield potential in drought environments. Translocation of soluble stem carbohydrates to the grain is one of the droughtadaptive attributes related, particularly, to increased partitioning. The focus of improving all three components needs to be accomplished through complex physiological attribute-based breeding. Important attributes that could be considered for drought adaptation include: (1) preanthesis growth; (2) WUE (relatively higher biomass/mm of water extracted from the soil) transpiration efficiency of growth (biomass/mm water transpired) indicated by C-isotope discrimination; (3) access to water due to deep rooting or intensity that may be expressed by a relatively cool canopy (Reynolds et al., 2005); and (4) photoprotection through energy dissipation, antioxidant systems, and anatomical attributes (e.g., leaf wax). Similarly, root architecture that helps to give better access to soil moisture under drought enables heat-stressed crop canopies to meet the high evaporative demand associated with hot, low-relative humidity environments, thus resulting in cooler canopies (Reynolds et al., 2000). Deeper/prolific roots have been found to increase plants’ access to water from deeper soil layers and support greater crop growth under drought conditions (Sinclair, 2011). Therefore in crops, such as wheat (Reynolds et al., 2007a) and rice (Price et al., 2002a), root systems are targeted to improve grain yield under rain-fed conditions. At the same time, other critical attributes that contribute to soil moisture conservation during late-season water deficits must be addressed. Generally, photosynthesis is reduced under drought stress, and many species depend on the assimilates produced from current photosynthesis under drought. Thus, exploring genotypes possessing efficient mechanisms for staying green may be beneficial (Tian et al., 2013).

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14.8 Precise phenotyping for drought-tolerance attributes After identifying suitable target traits for selecting grain yield under drought stress, the next step is to establish a precision phenotyping platform for pinning down the source trait most tightly connected to yield (Tuberosa, 2010). Platforms for high-throughput phenotyping (HTP), particularly in field environments, are needed to complement the wealth of genomic information in plant genetics. The precise phenotyping for drought-related PAs often requires the utilization of sophisticated and expensive techniques.

14.8.1 Near-infrared spectroscopy This method provides spectral information corresponding to the field plot in a single near-infrared (NIR) spectrum, where the physical and chemical characteristics of the harvested seed material are captured. By using calibration models, attributes (e.g., protein, nitrogen and oil content, grain texture, and grain weight) can be determined based on a single spectrum (Hacisalihoglu et al., 2010). In comparison to conventional methods, NIR spectroscopy on agricultural harvesters secures a good distribution of measurements within plots and covers substantially larger amounts of material (Welle et al., 2003); as a result, sampling error is reduced to provide more representative measurements in terms of homogeneity.

14.8.2 Canopy spectral reflectance Canopy spectral reflectance (CSR) is a noninvasive, remote-sensing phenotyping technique for complex attributes (e.g., biomass accumulation) with high temporal resolution (Montes et al., 2007; Li et al., 2011). The basic theme is that the pattern of light reflection on leaves at different wavelengths through NIR (7001200 nm) and photosynthetically active radiation (PAR) of 400 to 700 nm is very different from other materials including soil. Leaf pigments significanly absorb light in the PAR region but not in the NIR, thus reducing the reflection of PAR but not of NIR. Such a pattern of pigment absorption determines the distinctive leaf reflectance. Its measurement is quick and easy; integration at the canopy level and additional parameters can also be measured simultaneously via a series of diverse spectral indices (e.g., chlorophyll content, leaf area index, canopy green biomass, water content, and amount of PAR absorbed by the canopy) and its photosynthetic potential. Therefore, canopy reflectance is considered to be one of the valuable tools for HTP (Gutierrez et al., 2010). Further, crop water status as determined by plant water content or water potential (Jones et al., 2009) integrates the effects of several drought-adaptive attributes. Methods used to measure plant water content include stomatal conductance, leaf water potential, and CT (Reynolds et al., 2007a,b).

14.8.3 Magnetic resonance imaging and nuclear magnetic resonance These techniques are used to explore rootshoot systems in a soil or sand medium that permit examination of transport routes, structure, and the translocation dynamics of newly fixed photoassimilates labeled with radioactive carbon isotope. Thus, these two techniques help discriminate between species and improve the information about water relationships, the growth pattern, and the translocation properties of assimilates, providing new insights into the structurefunction relationship of intact plants (Jahnke et al., 2009).

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The utility of magnetic resonance imaging (MRI) in studying sourcesink relationships in structures, such as small developing seeds, is limited by the short half-life of 11C (Jahnke et al., 2009). Therefore, an alternative detection platform (in vivo) is provided by using 1H NMR; thus, water movement and sucrose may be imaged and quantified. A 13C/1H double-resonant high-resolution coil is employed in the nuclear magnetic resonance (NMR) technique for obtaining optimum resolution and monitoring tissues (e.g., seeds) through noninvasive visualization and mapping water movement through 13C-labeled sucrose (Melkus et al., 2011).

14.8.4 Digital imaging platforms Digital platfoms include imaging, image processing automatization, and data-handling modules. They can easily measure almost unlimited sets of parameters, thus allowing comprehensive screening, and various plant attributes can be statistically validated in a dynamic way. The procedure is simple; first, plants are manually placed in the Scanalyzer 3D or transported directly to the imaging chambers from greenhouses. These chambers have top- and side-imaging systems of both shoots and roots for nondestructive quantification of plant height/width, architecture, and biomass. Further, application of different cameras and acquisition modes (i.e., fluorescence imaging) from visual light to NIR are opening new ways for visualization and quantification of these attributes. Ultimately, this may enhance scientists’ understanding of plant growth kinetics and help improve plant models for breeding programs and systems biology. Summing up, the techniques and platforms discussed here may help improve precise phenotyping and contribute to better elucidation of the genetic control of crops’ complex drought-tolerance attributes. Nevertheless, many of the mentioned techniques are applicable to crops grown under controlled conditions on a limited number of genotypes due to high costs and/or practicality; they also may not be heritable in field conditions. Therefore, multitier selection screens, where a simple but less accurate screen allows a large number of genotypes to be evaluated, followed by tiers of more sophisticated screens of decreasing numbers of genotypes, have been proposed by Sinclair (2011). Further, bringing digital imaging platforms from controlled to field conditions may help improve the assessment of plant responses to drought while enabling high-throughput screening and generation of accurate and comprehensive phenotypic data.

14.9 Identification and characterization of drought-related genes and QTLs Due to the complex nature of drought response, large-scale identification of candidate dehydration stress-related genes or QTLs is necessary. Potential markers for stress tolerance can be identified either through loci mapping of yield-related attributes or “omics” studies under drought-prone environments. These markers can assist in screening genotypes for drought tolerance and/or improvement of drought tolerance in wheat (Ravi et al., 2011). Recent advances in genome mapping technologies and functional genomics have provided new tools for molecular dissection of drought tolerance (Worch et al., 2011). The molecular markers and/or candidate genes identified can then be used in molecular breeding.

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14.9.1 QTL and association mapping for drought tolerance Drought-tolerance dissection requires the identification of related QTLs. QTL cloning is a challenging task in terms of resources, technology, and time required, but its determination is preceded by great advantages in marker-assisted selection (MAS) and the development of better yield cultivars. A large number of linkage mapping studies have been conducted during the past decade with several crops to identify QTLs linked to drought tolerance (see Cattivelli et al., 2008; Fleury et al., 2010, for a review). The biggest concern about linkage mapping, however, is insufficient time for recombination to occur and shuffle the genome into small fragments; as a result, the QTLs identified are generally localized to large genomic regions/chromosomal segments. Association mapping (AM), or linkage disequilibrium mapping, is an alternative approach. The idea behind AM is that attributes of interest first arise as a mutation in one individual gene, resulting in the creation of a new allele for a trait. The new allele then passes along with the surrounding loci in a nonrandom coinheritance pattern into succeeding generations provided that it improves the individual’s fitness. Recombination will slowly break down the block of coinherited loci proportional to the distance from the beneficial allele. The genes closest to the mutation will continue to be coinherited throughout generations. Association mapping seeks to exploit this phenomenon by allowing plant breeders to tag the genetic material surrounding attributes of interest with molecular markers. The markers themselves can then be used as genetic flags for cultivar improvement. Association mapping is similar to linkage mapping in its goal but different from the latter in the methodology to achieve this goal. Conventional MA requires biparental segregating populations such as recombinant inbred lines (RILs), doubled haploid (DH) lines, and backcrossed lines; many QTLs for yield and its components have been identified using various types of mapping populations (Borner et al., 2002; Huang et al., 2003, 2004). On the other hand, AM uses natural populations to detect variations associated with quantitative attributes based on linkage disequilibrium (LD). Therefore, association mapping can detect many alleles and display a much higher resolution than conventional QTL mapping. The main idea with AM is to carry out genome-wide searches through panels of accessions having medium- to highLD levels for chromosomal regions harboring loci regulating the expression of particular phenotypic attributes (Breseghello and Sorrells, 2006; Ravel et al., 2006; Ersoz et al., 2008; Sorrells and Yu, 2009). From a biological perspective, combining phenotypic and molecular data of the natural variations from core collections of germplasm is important, in general, to dissect those considered to be complex (Alonso-Blanco et al., 2009) and, in particular, for the adaptive attributes including yield under different water regimens (Araus et al., 2008; Annicchiarico et al., 2009; Reynolds et al., 2009; Tardieu and Tuberosa, 2010). Assuming samples from structured populations, the general approach in AM in plants includes the following: 1. Selection of a group of genetically diverse individuals from a germplasm collection or from a natural population. 2. Evaluation of the selected group of individuals under varying environmental conditions and multiple trials/designs for phenotypic attributes (tolerance or resistance, quality or yield). 3. Genotyping of the same group by using molecular markers. 4. Estimation of the extent of the LD of the studied group genome using molecular marker data.

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5. Assessment of the level of genetic differentiation among groups within a sampled individual (e.g., population structure). 6. Measuring the coefficient of relatedness between pairs of each individual within a sample (e.g., kinship). 7. Based on the information gained, correlation of phenotypic and genotypic/haplotypic data by using a suitable statistical approach that reveals “marker tags” positioned within close proximity of the targeted trait of interest. Accordingly, these marker tags can then be used to clone a specific gene(s) controlling a QTL of interest and annotated for an exact biological function. It is important, for designing and conducting an unbiased association mapping, to obtain knowledge of LD patterns for genomic regions of the “target” organisms and its specificity among different populations or groups (Nordborg et al., 2002). Some of the reported markers linked to drought-tolerance attributes in wheat (Sanguineti et al., 2007; Maccaferri et al., 2011), maize (Lua et al., 2010), barley (Varshney et al., 2012), and rice are given in Table 14.2. Nevertheless, obtaining a clean set of reproducible phenotypic data for drought tolerance from a larger germplasm collection for AM studies remains an open challenge even in the era of phenomics technology.

14.9.2 Candidate genes associated with drought tolerance Advances made in the model plant systems of major crops provides an opportunity to identify candidate genes (CGs) with some relevance to drought tolerance. Molecular physiological, genome annotation, and functional genomics studies of major species have shown indications of the CGs involved in conferring drought tolerance. These may be (1) genes involved in protection of the cell under drought stress such as proteins having a role in osmotic adjustment, repairs, degradation, and detoxification (Khoshro et al., 2013); and (2) genes that regulate other genes involved in drought responsetranscription factors (e.g., DREB, MYB, and bZIP). Knowledge of the CGs responsible for tolerance is valuable for understanding the functional basis of drought tolerance and is applicable in molecular breeding through MAS once they have been validated. Validation of the CGs can be achieved by utilizing approaches such as expression analysis using qRT-PCR, allele mining, and Targeting Induced Local Lesions in Genomes (TILLING). As an example, a set of nearly 30 drought tolerance-related CGs have been compiled by Sehgal and Yadav (2010). In another instance, mapping of OsEXP2 and EGase involved in cell expansion within the expected intervals of QTL for root attributes in rice was done by Zheng et al. (2003). Functional genomics and transcriptomics have been used in recent years to better understand the stress-responsive mechanisms in crop plants. The generation of expressed sequence tags (ESTs) from either normalized or nonnormalized cDNA libraries from tissues of drought-responsive genotypes is one of the most common approaches for isolation of candidate genes (Hadiarto and Tran, 2011). Similarly, a survey of all the publicly available ESTs in various cereal crops, including barley, maize, rice, and wheat, has led to the identification of drought stress-responsive genes in these species (Sreenivasulu et al., 2007; Deihimi et al., 2013; Negrao et al., 2013). Such studies provide important sources for marker development and identification and selection of CGs (both up- and down-regulated) associated with drought tolerance.

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Table 14.2 QTLs Reported in Some Major Crops for Drought Tolerance-Related Attributes Crops

Attributes

Wheat

Water-soluble carbohydrates and related attributes Grain yield and yield components under drought Growth and yield

Morphophysiological

Phenological, agronomic, and physiological Growth and grain yield Maize

Barley

Rice

Root characteristics, drought-tolerance index and yield Yield components Leaf ABA Osmotic adjustment Relative water content Morphological and physiological attributes related to drought Chlorophyll content and chlorophyll fluorescence Morphological and physiological attributes related to drought Drought avoidance Water stress indicators, phenology and production attributes

Linkage Group/ Chromosome

Number of QTLs

PVE (%)

Reference

1A, 2A, 3A, 4A, 5A, 6A, 7A, 1B, 3B, 4B, 5B, 6B, 7B, 1D, 2D, 7D 4AL

48

1.17.6

Yang et al. (2007)

1

12.041.0

Kirigwi et al. (2007)

16

Mathews et al. (2008)

110

0.842.4

Peleg et al. (2009)

104

11.233.5

Pinto et al. (2010)

3A, 4A, 5A, 6A, 7A, 1B, 2B, 4B, 5B, 6B, 7B, 1D, 4D, 6D 1A, 2A, 3A, 4A, 5A, 6A, 7A, 1B, 2B, 3B, 4B, 5B, 6B, 7B 1A, 3A, 4A, 5A, 6A, 7A, 1B, 2B, 3B, 4B, 5B, 6B, 7B, 1D, 4D 1A, 2A, 3A, 4A, 5A, 7A, 1B, 2B, 3B, 4B, 6B, 7B All chromosomes

42

3.453.9

Maccaferri et al. (2008, 2011)

56

6.747.2

Tuberosa et al. (2002)

1, 2, 3, 5, 7, 8, 9 2 1H, 2H, 4H, 5H, 7H 2H, 5H, 6H, 7H

20 1 22 6

4.131.3 32.0 5.020.0 6.811.5

Xiao et al. (2005) Landi et al. (2005) Teulat et al. (2001) Teulat et al. (2003)

IH, 2H, 3H, 4H, 5H, 6H, 7H

68

4.016.0

Diab et al. (2004)

1H, 2H, 4H, 6H, 7H

5

6.213.6

Guo et al. (2008)

1H, 2H, 3H, 4H, 5H, 6H, 7H

18

14.357.5

Chen et al. (2010)

1, 2, 3, 4, 5, 6, 7, 8, 10, 11, 12 1, 2, 3, 4, 6, 7, 8, 9, 10, 11, 12

17

4.425.6

Price et al. (2002b)

47

5.059.0

Babu et al. (2003)

(Continued)

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Table 14.2 (Continued) Crops

Attributes Root attributes Basal root thickness and thousand grain weight Drought-tolerance index and coleoptile length Specific water use and relative growth rate Grain yield

Linkage Group/ Chromosome

Number of QTLs

PVE (%)

Reference

1, 2, 3, 4, 5, 6, 7, 8, 9, 10, 11, 12 4, 6

18

1.218.5

Ping et al. (2003)

2

20.633.4

Li-Feng et al. (2007)

1, 2, 4, 5, 6, 7, 9, 10, 12

15

4.922.7

Song-ping et al. (2007)

2, 4, 5, 6, 7, 8

7

10.022.0

Kato et al. (2008)

2, 3

2

13.031.0

Venuprasad et al. (2009)

PVE, phenotypic variation explained.

Transcript profiling is another way of identifying CGs that involves analysis of differential gene expression between drought-tolerant and susceptible genotypes after exposure to drought stress (Micheletto et al., 2007; Hampton et al., 2010). Targeting the right tissue at the right stress-treatment time imposed to mimic drought conditions for isolation of the RNA to be used in transcriptomic studies is a prerequisite. Further, near-isogenic lines (NILs) are preferable for such studies as they ensure that differential expression of genes is connected to the trait and not to the genetic background (Talame et al., 2007). Transcript profiling can be accomplished through the following platforms: (1) cDNAamplified fragment length polymorphism (cDNAAFLP) analysis, (2) digital expression analysis based on counts of ESTs, (3) cDNA and oligonucleotide microarrays, and (4) differential display RTPCR (DDRTPCR) (Liang and Pardee, 1992; Bachem et al., 1996; Raju et al., 2010; Sreenivasulu et al., 2010). To proceed further, sequence-based transcriptome analysis is preferred for crops where genome sequence information is lacking because it is a real-time, digital, and highly accurate analytical method. Therefore, it is likely that microarrays may soon be replaced by digital gene expression analysis (Varshney et al., 2009). Similarly, genetic genomic techniques for quantitative analysis of transcript profiling of the CGs may lead to QTLs for drought tolerance-related attributes.

14.10 Proteomic studies Despite the impressive technological advances in the genomics of drought-tolerant cultivars, new dimensions need to be explored to reveal the exact wheat drought-response processes. Accordingly, studies that focus wheat tolerance at the proteomic level in order to understand the role of different proteins in drought stress need to be emphasized (Zandalinas et al., 2012; Verelst et al., 2013). One example of such a study can be seen from the experiments conducted by Jiang et al. (2012) on

14.11 Breeding approaches for developing drought-tolerant germplasm

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drought-tolerant and sensitive wheat varieties. They applied linear and nonlinear two-dimensional gel electrophoresis (2-DE) and matrix-assisted laser desorption/ionizationtime-of-flight (MALDITOF) mass spectrometry and noted that nonlinear 2-DE showed a high resolution. They identified 152 differentially expressed protein spots, 122 of which were detected by MALDI-TOF. The characterized proteins were primarily those involved in defense and detoxification (22.8%), metabolism proteins (25.7%), and storage proteins (17%). The study successfully showed the differential expression of various proteins in drought-tolerant and sensitive varieties. Thus, differential expression proved that biochemical and protein-level expression may be a simpler approach to understanding and manipulating drought stress in plants (Jiang et al., 2012).

14.11 Breeding approaches for developing drought-tolerant superior germplasm Once the candidate genes or markers associated with QTLs for drought tolerance are identified, the next step is their deployment in breeding practices. Some of these approaches are discussed next.

14.11.1 Marker-assisted selection Marker-assisted selection (MAS) is the utilization of molecular markers through various molecular breeding approaches based on specific attributes for cultivar drought tolerance. Targeted loci in MAS are most often derived from QTL mapping studies, usually involving physiomorphological characteristics related to yield under drought conditions (Witcombe et al., 2008). Examples of markers utilized include Xgwm136 (SSR marker) and NW3106, linked to genes affecting tillering capacity and coleoptile length, respectively (Gulnaz et al., 2011). The reduced height (Rht) gene is another selection marker associated with HI. The genotype-by-sequencing (GBS) approach using three enzyme library sequencing (Saintenac et al., 2013) is reported to yield approximately 415,000 SNPs covering the whole genome with a genetic density of 0.005 cM per marker in wheat. GBS not only yields more markers but also provides information about the sequence and SNP of alien introgressions in wheat. Cost effectiveness is also an added plus to all the advantages of GBS. The integration of GBS and SNP mapping data may increase the ability of wheat breeders and researchers to conduct high-resolution mapping of WUE and other drought-tolerance traits. More authentic markers are likely to promote current MAS efforts for developing new cultivars that can ameliorate the negative impacts of climate change (Brenchley et al., 2012; Jia et al., 2013; Ling et al., 2013). Moreover, transcription factor-derived markers, such as DREB proteins (PCR-based), can be useful in MAS (Wei et al., 2009). However, the isolation of transcription factors is a challenge because they belong to large gene families containing members with high sequence similarities. In addition, identification and successful isolation of single drought-related loci is compelling in general due to the complex genomic structure of wheat.

14.11.2 Genome-wide selection Genomic selection (GS) or genome-wide selection (GWS) is a relatively recent approach for developing superior genotypes that exhibit tremendous performance in the target environment.

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Genome-wide marker genotyping is carried out for GS instead of selecting markers showing significant associations with the attributes of interest. Briefly, genotypes in a training population (phenotyped population) are genotyped using GWS markers and breeding values of alternative alleles of all the markers are fitted as random effects in a linear model. Individuals in subsequent recurrent selection generations are then selected based on genomic estimated breeding value (GEBV). Therefore, GWS reduces the frequency of phenotyping and similarly increases annual gains from selection by reducing cycle time (Meuwissen et al., 2001; Rutkoski et al., 2010). Several groups have recently started exploring the GWS approach in both self- and cross-pollinated crops with some modifications for both types of crops (Bernardo, 2010). This approach has been used to improve durable stem rust resistance in wheat (Rutkoski et al., 2010) and eventually may be systematically explored to determine the different components of multigenic drought tolerance using the GS approach.

14.12 Conclusion and future prospects The way forward modus operandii without crop specificity basically revolves around two parameters that comprise the population status linked with yield potential targeted to a futuristic time frame. Narrowing this down to wheat as the cereal food, agriculturalists are looking at a population of about 9.2 billion people by 2050 for which yield maximization is crucial. Yield maximization can occur by enhancing the overall production obtained from irrigated and rain-fed growing conditions. It is the latter that has the capacity to augment or penalize yield outputs. The focus is to manipulate the rain-fed growing condition in hopes that yield enhancement may take place. Simultaneously with manipulation is the all-important performance of the crops’ genetic components plus a management technology that together can embrace all the factors pivotal for a holistic effort around the categories presented in this chapter. We end here by emphasizing the fact that water per se, as it influences drought tolerance, is a complex phenomenon requiring in-depth handling across all basic, strategic, and applied scenarios structured around multiple disciplines. The salient points to the overall theme of this chapter focused on water usage; therefore we are inclined to take the reader from theoretical reality to a functional mode of operation and to propose guidelines for future research and development of drought tolerance. Inroads as to water usage associated with drought stress form a befitting closure to what has been discussed. Vital digression to address very briefly the current cutting-edge scientific scenarios, which give future directives to amend water constraints, is an essential and justifiable conclusion for this important topic. Drought is the major stress that varies yield outputs annually and is affected all the more by the harsh influence of climate change. Drought stress is one of the major limitations to crop production. The physiological analysis of complex drought-related attributes is a key step to better understanding genetic control of tolerance to ultimately enhance the efficiency of molecular breeding strategies (Reynolds and Trethowan, 2007). Developing improved cultivars with sufficient tolerance to drought stress and identification of osmotic stress-related molecules and their roles in biochemical, physiological, and gene regulatory networks is necessary. It is obvious that precise phenotyping is vital for screening larger core collection/mapping populations to explore the QTLs and CGs to be used in plant breeding. Several phenotyping approaches are available now under the umbrella of “phenomics”; however, crop modeling, which is a relatively recent approach, needs to be integrated with phenomics to ensure rapid assessment of the value of certain attributes on plant performance (Tardieu and Tuberosa, 2010).


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The new molecular “omics” tools, which include genomics, proteomics, transcriptomics, and metabolomics, have opened up new ways for characterization of stress-related morphophysiological and molecular mechanisms (Arbona et al., 2013). This information is used to develop models for QTL analysis and positional cloning by providing functional data to select CGs for loci. Elucidation of the complex networks interacting during stress responses can now be achieved through analysis of transcript-level, microarray analysis, RT-qPCR, massive parallel signature sequencing (MPSS), and serial analysis of gene expression (SAGE). Further, several bioinformatics tools (e.g., ESTs and subtractive cDNA libraries) have added new dimensions for diciphering the genetic basis of stress tolerance (Roychoudhury et al., 2010). The current initiative in functional genomics or proteomic research for stress tolerance is based on 2-DE and identification of differentially displayed spots by MALDI-TOF, quadrupole time-of-flight (QTOF), and liquid chromatography coupled with tandem mass spectrometry (LC-MS/MS). In addition, the use of sequenced cereal genomes in defining target regions and CGs for drought tolerance in wheat is another promising option. The significant conservation of gene order between grasses means that the rice and Brachypodium genomes provide a valuable resource for developing fine-mapping markers in a target region and for identifying candidate genes for the QTLs. Production of drought-tolerant cultivars no doubt has its own place in water-scarce regions. Utilization of properly treated municipal and industrial wastewater for agriculture may also help overcome drought issues, reduce pressure on freshwater resources, and decrease diseases in plants and humans associated with these environmental hazardous waters. Wastewater treatment systems need to adopt chemical, biological, or physical processes. Biological processes are usually costeffective and environmentally friendly; these may include phytoremediation (through plants), biodegradation (through microbes), and mycoremediation (through fungi). Plants, microbes, and fungi can be used to clean wastewaters, contaminated soils/sediments/sludge, and so on. Application of organisms can be at a contaminated site (in situ) or away from the site (ex situ). Constructed wetlands (CWs) and detention ponds containing different aquatic macrophytes/ microbial strains are now used extensively for the treatment of municipal and industrial wastewaters (Ali et al., 2013a,b; Farid et al., 2014) and use plants and microbial strains for treatment. This process can be applied to a wide range of municipally and industrially contaminated effluents containing inorganic/organic and pathogenic elements. Constructed wetlands are generally of three types: surface flow, subsurface flow, and vertical flow; they are commonly used for municipal, industrial, and agricultural wastewater treatment. Aquatic macrophytes introduced in CWs and detention ponds may include Eichhornia crassipes, Pistia stratiotes, Lemna minor, Lemna gibba, Typha latifolia, Vetiver zizanoides, Phragmites australis, Pteris vittata, Hydrilla verticillata, Salvinia molesta, Azolla filiculoides, and others (Ali et al., 2013a). Such macrophytes are involved in a number of phytoremediation processes that they perform in constructed wetlands and detention ponds (e.g., phytotransformation, phytostabilization, phytoextraction, phytovolatilization, and rhizofiltration) (Salt et al., 1998; Pilon-Smits and Freeman, 2006). All these processes have their own unique benefits and disadvantages. Phytoextraction is the uptake of contaminants by roots followed by accumulation in the aboveground plant parts (Peer et al., 2005). After harvest, the plants are disposed of in an environmentally safe manner. Other names given to this technique are phytosequestration, phytomining/biomining, phytoabsorption, and phytoaccumulation (Chaney et al., 2000). Phytostabilization is the in situ (in place) inactivation of pollutants in the contaminated matrices through physical, biological, or chemical

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modifications; further dispersal of contaminants after phytostabilization is not possible. Rhizofiltration (phytofiltration) is the process of precipitation or adsorption of pollutants onto root surfaces. Phytotransformation (phytodegradation) is the metabolic breakdown of contaminants within plants. Plants use enzyme systems to catalyze all contaminant breakdown reactions in and around their vicinities. After metabolic processing, some of the contaminant’s metabolic products are released into the air through the leaves; this process is termed phytovolatilization (Meagher et al., 2000). Aquatic macrophytes and microbes used for wastewater treatment can be genetically engineered to enhance their pollutant-accumulation potential from the contaminated wastewaters (Meagher and Heaton, 2005). Genetically engineered plants and microbes are known as transgenic organisms having nuclear fragments to enhance remediation potential. Current research focuses on the uptake of inorganic/organic pollutants by plants/microbes and their fate in selected living organisms. Higher uptake and accumulation of pollutants is the ultimate goal of genetically engineered plants/ microbes in the bioremediation processes. Decontaminated waters then can be effectively used in various ways. Treated wastewater through the previously mentioned biological methods is mostly fit for agriculture. Risks for environmental contamination are minimized because a significant number of the contaminants are degraded into nontoxic simpler substances after the bioremediation process. Treated wastewater is of extreme significance for agriculture due to its continuous supply, high nutrient value, and ready availability (Ali et al., 2013a). Treated water can be efficiently used in crop production. In this connection, WUE is defined as the ratio between plant biomass produced to the holistic water input (through irrigation and/or rain from germination to harvest) (Zhang and Oweis, 1999; Xu-rong et al., 2013). Water-use efficiency of Pakistan’s conventional canal system is around 45%; this can be increased to 90% by use of a high-efficiency irrigation system (MINFAL, 2008). Wastewater treatment through CWs and/or detention ponds and its application through HEIS may be of momentous help in overcoming water scarcity in Pakistan. Compared to conventional irrigation systems, a HEIS involves high capital investment followed by sound management (Zhang and Oweis, 1999). Higher cost is the only hindrance currently faced by the farming communities for adoption of this innovative technique (Romero et al., 2006; Muhammad et al., 2007). Some recent studies have shown that water-saving irrigation is instrumental in conserving precious freshwater and also to help reduce greenhouse gas (GHG) emissions into the environment (Karimi et al., 2012). In this way, water-saving irrigation is linked with reversing the ill effects of climate change that hamper agricultural production. A HEIS includes drip and sprinkler systems used for water savings. The drip irrigation method is also known as microirrigation, or trickle irrigation; it supplies localized water slowly to plant roots through a series of valves, tubes, emitters/applicators, pipes, and so on. Drip irrigation methods are popular in the arid regions across the globe, saving precious water and fertilizer inputs to a variety of crops. This irrigation system is more suited to plants grown in rows where water is provided either at the soil surface or subsurface. A drip irrigation system is set up at the ground level, which differs from the sprinkler irrigation system, in which water is collected in overhead pipes from where it is sprayed via a high-pressure spray gun to different parts of the field. Sprinklers also save water (B3540%) when compared to flood irrigation methods that prevail in Pakistan. Wind can affect the direction of the sprinkler’s shower; however, its affect is negligible on drip irrigation


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Light

Photosynthesis

CO2 Vegetable biomass

O2

H2O

Animal manure Fertiliser

Biogas Organic wastes

Anaerobic digestion

Electricity and heat

FIGURE 14.3 Sustainable production of biogas by anaerobic digestion. Source: Adapted from Al-Seadi (2001).

water that is released very close to the soil surface. HEISs have competitive advantage over conventional irrigation systems, although .80% of Pakistani farmers (having land holdings of ,5 ha) cannot afford the high installation and maintenance costs involved. Besides a HEIS, bed-planting techniques (bed and furrow irrigation) can help save precious irrigation water. Traditionally, basin irrigation is popular among the majority of Pakistani farmers, but it has the lowest efficiency. In bed planting methods, plants are grown over the beds and irrigation water is provided in the furrows; this saves plenty of water in comparison to basin irrigation. Spared irrigation water can easily be used to increase cropping intensity. Additional benefits of bed planting include ease of weeding, crop maintenance, intercropping, and the least water-borne plant health risks. Bed planting is a lot less expensive method compared to HEIS; however, it may take a few hours using agricultural machines to develop beds and furrows in fields. Due to the high cost involved in HEISs, farmers may be able to be educated for bed planting to save natural resources (i.e., water). By 2025, the agricultural sector may require an additional 35 MAF of irrigation water. With construction of new reservoirs and adequate canal maintenance, additional irrigation water can hardly be supplied unless alternate options are explored on a marginal basis. Biological treatment of municipal and industrial wastewater, and its subsequent utilization in irrigation, can ensure even higher water availability than required for irrigation in years to come. Biological wastewater treatment technology can be replicated across all provinces of Pakistan in different agroecologies so

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that water is available to every farmer without compromising environmental and food safety. Sufficient irrigation water in Pakistan may very ably increase the irrigated area under cultivation from 18 to 26 million ha. In case energy scenarios are totally incorrect, we may need to evaluate whether entrepreneurship should to be entertained because energy-driven alternate water access may salvage the situation. Thus, efficiently exploiting biogas production as detailed in Figure 14.3 may be an option worth exploring (Al-Seadi, 2001).

References Acevedo, E., Silva, P., Silva, H., 2002. Wheat growth and physiology. In: Curtis, B.C., Rajaram, S., Macpherson, H.G. (Eds.), Bread Wheat. Improvement and Production, FAO, Rome, pp. 5389. Available at: ,www.fao.org///DOCREP/006/Y4011E/y4011e04.htm. Agricultural Statistics of Pakistan, 2011. Ministry of Food and Agriculture (Economic Wing). Government of Pakistan, Islamabad. Ahmad, M., Yasin, M., 2006. Low quality water management for sustainable irrigation and crop production. Pak. J. Water Res. 10, 2331. Al-Seadi, T., 2001. Report Made for the International Energy Agency, Task 24Energy from Biological Conversion of Organic Waste. IEA Bioenergy and AEA Technology Environment, Oxfordshire, UK, Good practice in quality management of AD residues from biogas production. Ali, Z., Ali, B., Mohammad, A., Ahmad, M., Ahmad, I., Napar, A.A., et al., 2013a. Combating water scarcity for global food security. In: Amir, Raza (Ed.), Agricultural Systems in the 21st Century. Nova Science Publishers, Hauppauge, NY. Ali, Z., Malik, R.N., Qadir, A., 2013b. Heavy metals distribution and risk assessment in soils affected by tannery effluents. Chem. Ecol. 29, 676692. Ali, Z., Malik, R.N., Shinwari, Z.K., Qadir, A., 2013c. Enrichment, risk assessment and statistical apportionment of heavy metals in tannery-affected areas. Int. J. Environ. Sci. Technol. Available from: http://dx.doi. org/10.1007/s13762-013-0428-4. Alonso-Blanco, C., Aarts, M.G., Bentsink, L., Keurentjes, J.J., Reymond, M., Vreugdenhil, D., et al., 2009. What has natural variation taught us about plant development, physiology, and adaptation? Plant Cell 21, 18771896. Annicchiarico, P., Royo, C., Bellah, F., Moragues, M., 2009. Relationships among adaptation patterns, morphophysiological traits and molecular markers in durum wheat. Plant Breed. 128, 164171. Araus, J.L., Slafer, G.A., Royo, C., Seerret, M.D., 2008. Breeding for yield potential and stress adaptation in cereals. Crit. Rev. Plant Sci. 27, 377412. Arbona, V., Manzi, M., de Ollas, C., Go´mez-Cadenas, A., 2013. Metabolomics as a tool to investigate abiotic stress tolerance in plants. Int. J. Mol. Sci. 14, 48854911. Aroca, R., Porcel, R., Ruiz-Lozano, J.M., 2012. Regulation of root water uptake under abiotic stress conditions. J. Exp. Bot. 63, 4357. Asada, K., 1999. The water cycle in chloroplast: scavenging of active oxygen and dissipation of excess photons. Annu. Rev. Plant. Physiol. Plant. Mol. Biol. 50, 601639. Ashraf, M., Fooland, M.R., 2007. Roles of glycine betaine and proline in improving plant abiotic stress resistance. Environ. Exp. Bot. 59, 206216. Atkinson, N.J., Urwin, P.E., 2012. The interaction of plant biotic and abiotic stresses: from genes to the field. J. Exp. Bot. 63, 35233543.

References

337

Babu, C.R., Nguyen, B.D., Chamarerk, V., 2003. Genetic analysis of drought resistance in rice by molecular markers: association between secondary traits and field performance. Crop Sci. 43, 14571469. Bachem, C.W.B., van der Hoeven, R.S., De Bruijn, S.M., Vreugdenhil, D., Zabeau, M., Visser, R.G.F., 1996. Visualization of differential gene expression using a novel method of RNA fingerprinting based on AFLP: analysis of gene expression during potato tuber development. Plant J. 9, 745753. Bartels, D., Sunkar, R., 2005. Drought and salt tolerance in plants. Crit. Rev. Plant Sci. 24, 2358. Bernardo, R., 2010. Genome-wide selection with minimal crossing in self-pollinated crops. Crop Sci. 50, 624627. Bernier, J., Atlin, G.N., Serraj, R., Kumar, A., Spaner, D., 2008. Breeding upland rice for drought resistance. J. Sci. Food Agric. 88, 927939. Blum, A., 1996. Crop responses to drought and the interpretation of adaptation. Plant Growth Reg. 20, 135148. Blum, A., 2005. Drought resistance, water-use efficiency, and yield potential: are they compatible, dissonant, or mutually exclusive? Aust. J. Agric. Res. 56, 11591168. Blum, A., 2009. Effective use of water (EUW) and not water use efficiency (WUE) is the target of crop yield improvement under drought stress. Field Crops Res. 112, 119123. Blum, A., 2011. Drought resistance—is it really a complex trait? Funct. Plant Biol. 38, 753757. Bohnert, H.J., Nelson, D.E., Jensen, R.G., 1995. Adaptations to environmental stresses. Plant Cell 7, 10991111. Borner, A., Schumann, E., Furste, A., Coster, H., Leithold, B., Roder, M.S., et al., 2002. Mapping of quantitative trait loci determining agronomic important characters in hexaploid wheat (Triticum aestivum L.). Theor. Appl. Genet. 105, 921936. Brenchley, R., Spannagl, M., Pfeifer, M., Barker, G.L., D’Amore, R., Allen, A.M., et al., 2012. Analysis of the bread wheat genome using whole-genome shotgun sequencing. Nature 491, 705710. Breseghello, F., Sorrells, M.E., 2006. Association mapping of kernel size and milling quality in wheat (Triticum aestivum L.) cultivars. Genetics 172, 11651177. Bressan, R., Bohnert, H., Zhu, J.K., 2009. Abiotic stress tolerance: from gene discovery in model organisms to crop improvement. Mol. Plant 2, 12. Cattivelli, L., Rizza, F., Badeck, F.W., Mazzucotelli, E., Mastrangelo, A.M., Francia, E., et al., 2008. Drought tolerance improvement in crop plants: an integrated view from breeding to genomics. Field Crops Res. 105, 114. Chandra Babu, R., Blum, A., Zhang, J., Sarkarung, S., Nguyen, N.T., 1999. Screening for osmotic adjustment in rice. In: Ito, O., O’Toole, J., Hardy, B. (Eds.), Genetic Improvement of Rice for Water-Limited Environments. International Rice Research Institute, Los Banos, Phillipines, pp. 292305. Chandrasekar, V., Sairam, R.K., Srivastava, G.C., 2000. Physiological and biochemical responses of hexaploid and tetraploid wheat to drought stress. J. Agron. Crop Sci. 185, 219227. Chaney, R.L., Li, Y.M., Brown, S.L., 2000. Improving metal hyperaccumulator wild plants to develop commercial phytoextraction systems: approaches and progress. In: Terry, N., Ban˜uelos, G. (Eds.), Phytoremediation of Contaminated Soil and Water. Lewis, Boca Raton, FL, pp. 129158. Charron, A.J., Quatrano, R.S., 2009. Between a rock and a dry place: the water-stressed moss. Mol. Plant 2, 478486. Chen, C., Dickman, M.B., 2005. Proline suppresses apoptosis in the fungal pathogen Colletotrichum trifolii. PNAS 102, 34593464. Chen, G., Krugman, T., Fahima, T., Chen, K., Hu, Y., Roder, M., et al., 2010. Chromosomal regions controlling seedling drought resistance in Israeli wild barley, Hordeum spontaneum C. Koch. Genet. Resour. Crop Evol. 57, 8599. Chen, Q., Tao, S., Bi, X., Xu, X., Wang, L., Li, X., 2013. Research progress in physiological and molecular biology mechanism of drought resistance in rice. Amer. J. Mol. Biol. 3, 102107.

338


Chutia, J., Borah, S.P., 2012. Water stress effects on leaf growth and chlorophyll content but not the grain yield in traditional rice (Oryza sativa L.) genotypes of Assam, India. II. Protein and proline status in seedlings under PEG induced water stress. Amer. J. Plant Sci. 3, 971980. DaCosta, M., Huang, B., 2006. Osmotic adjustment associated with variation in bentgrass tolerance to drought stress. J. Am. Soc. Hortic. Sci. 131, 338344. Deihimi, T., Niazi, A., Ebrahimie, E., 2013. Identification and expression analysis of TLPs as candidate genes promoting the responses to both biotic and abiotic stresses in wheat. Plant Omics J. 6, 107115. Diab, A.A., Teulat-Merah, B., This, D., Ozturk, N.Z., Benscher, D., Sorrells, M.E., 2004. Identification of drought-inducible genes and differentially expressed sequence tags in barley. Theor. Appl. Genet. 109, 14171425. Ensink, J.H.J., van der Hoek, W., Matsuno, Y., Munir, S., Aslam, M.R., 2002. Use of Untreated Wastewater in Peri-Urban Agriculture in Pakistan: Risks and Opportunities IWMI Research Report No 64. International Water Management Institute (IWMI), Colombo, Sri Lanka. Ersoz, E.S., Yu, J., Buckler, E.S., 2008. Applications of linkage disequilibrium and association mapping. In: Varshney, R.K., Tuberosa, R. (Eds.), Genomics-Assisted Crop Improvement, vol. 1. Genomics Approaches and Platforms. Springer, Dordrecht, pp. 97120. Farid, M., Irshad, M., Fawad, M., Ali, Z., Eneji, A.E., Aurangzeb, N., et al., 2014. Effect of cyclic phytoremediation with different wetland plants on municipal wastewater. Int. J. Phytorem. 16, 572581. Fedoroff, N.V., Battisti, D.S., Beachy, R.N., 2010. Radically rethinking agriculture for the 21st century. Science 327, 833834. Fereres, E., Acevedo, E., Henderson, D.W., Hsiao, T.C., 1978. Seasonal changes in water potential and turgor maintenance in sorghum and maize under water stress. Plant Physiol. 44, 261267. Fischer, R.A., Maurer, R., 1978. Drought resistance in spring wheat cultivars. I. Grain yield responses. Aust. J. Agric. Res. 29, 897912. Fleury, D., Jefferies, S., Kuchel, H., Langridge, P., 2010. Genetic and genomic tools to improve drought tolerance in wheat. J. Exp. Bot. 61, 32113222. Gill, S.S., Tuteja, N., 2010. Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol. Biochem. 48, 909930. Gill, S.S., Khan, N.A., Anjum, N.A., Tuteja, N., 2011. Amelioration of cadmium stress in crop plants by nutrients management: morphological, physiological and biochemical aspects. Plant Stress 5, 123. GoP, 2008. Economic Survey of Pakistan (200708). Ministry of Finance, Pak Secretariat, Q Block, Islamabad, Pakistan. Gulnaz, S., Sajjad, M., Khaliq, I., Khan, A.S., Khan, S.H., 2011. Relationship among coleoptile length, plant height and tillering capacity for developing improved wheat varieties. Inter. J. Agri. Biol. 13, 130133. Guo, P., Baum, M., Varshney, R., Graner, A., Grando, S., Ceccarelli, S., 2008. QTLs for chlorophyll and chlorophyll fluorescence parameters in barley under post-flowering drought. Euphytica 163, 203214. Gupta, A.K., Sinha, S., 2007. Phytoextraction capacity of the plants growing on tannery sludge dumping sites. Bioresour. Technol. 98, 17881794. Gutierrez, M., Reynolds, M.P., Klatt, A.R., 2010. Association of water spectral indices with plant and soil water relations in contrasting wheat genotypes. J. Exp. Bot. 61, 32913303. Hacisalihoglu, G., Larbi, B., Settles, A.M., 2010. Near-infrared reflectance spectroscopy predicts protein, starch, and seed weight in intact seeds of common bean (Phaseolus vulgaris L.). J. Agric. Food Chem. 58, 702706. Hadiarto, T., Tran, S.P., 2011. Progress studies of drought-responsive genes in rice. Plant Cell Rep. 30, 297310. Hampton, M., Xu, W.W., Kram, B.W., Chambers, E.M., Ehrnriter, J.S., Gralewski, J.H., et al., 2010. Identification of differential gene expression in Brassica rapa nectaries through expressed sequence tag analysis. PLoS One 5, e8782.

References

339

Hsiao, T.C., Steduto, P., Fereres, E., 2007. A systematic and quantitative approach to improve water use efficiency in agriculture. Irrig. Sci. 25, 209231. Huang, X.Q., Coster, H., Ganal, M.W., Roder, M.S., 2003. Advanced backcross QTL analysis for the identification of quantitative trait loci alleles from wild relatives of wheat (Triticum aestivum L.). Theor. Appl. Genet. 106, 13791389. Huang, X.Q., Kempf, H., Ganal, M.W., Roder, M.S., 2004. Advanced backcross QTL analysis in progenies derived from a cross between a German elite winter wheat variety and a synthetic wheat (Triticum aestivum L.). Theor. Appl. Genet. 109, 933943. IIASA, 2002. Climate change and agricultural vulnerability. Special report for the UN World Summit on Sustainable Development. Johannesburg. Available at: ,www.iiasa.ac.at/ResearchILUC/JB-Report.pdf.. Jahnke, S., Menzel, M.I., van Dusschoten, D., Roeb, G.W., Buhler, J., Minwuyelet, S., et al., 2009. Combined MRIPET dissects dynamic changes in plant structures and function. Plant J. 59, 634644. Jia, J., Zhao, S., Kong, X., Li, Y., Zhao, G., He, W., et al., 2013. Aegilops tauschii draft genome sequence reveals a gene repertoire for wheat adaptation. Nature 496, 9195. Jiang, S.S., Liang, X.N., Li, X., et al., 2012. Wheat drought-responsive grain proteome analysis by linear and nonlinear 2-DE and MALDI-TOF mass spectrometry. Inter. J. Mol. Sci. 13, 1606516083. Jones, H.G., Serraj, R., Loveys, B.R., Xiong, L., Wheaton, A., Price, A.H., 2009. Thermal infrared imaging of crop canopies for the remote diagnosis and quantification of plant responses to water stress in the field. Func. Plant Biol. 36, 978989. Kahlown, M.A., Tahir, M.A., Sheikh, A.A., 2004. Water quality status in Pakistan Second Report 20012003, Pakistan Council of Research in Water Resources. Ministry of Science & Technology, Shaheed-e-Millat Secretariat, Islamabad, Pakistan. Kahlown, M.A., Raoof, A., Zubair, M., Kemper, W.D., 2007. Water use efficiency and economic feasibility of growing rice and wheat with sprinkler irrigation in the Indus basin of Pakistan. Agric. Water Manage. 87, 292298. Kamoshita, A., Rodriguez, R., Yamauchi, A., Wade, L.J., 2001. Response of rainfed-lowland rice genotypes to prolonged drought and rewatering during the vegetative stage. In: Fukai, S., Basnayake, J. (Eds.), Increased Lowland Rice Production in the Mekong Region. ACIAR Proceedings No 101, Canberra, Australia, pp. 7885. Karimi, P., Qureshi, A.S., Bahramloo, R., 2012. Reducing carbon emissions through improved irrigation and groundwater management: a case study from Iran. Agric. Water Manage. 108, 5260. Kato, Y., Hirotsu, S., Nemoto, K., Yamagishi, J., 2008. Identification of QTLs controlling rice drought tolerance at seedling stage in hydroponic culture. Euphytica 160, 423430. Khoshro, H.H., Taleei, A., Bihamta, M.R., Shahbazi, M., Abbasi, A., 2013. Expression analysis of the genes involved in osmotic adjustment in bread wheat (Triticum aesItivum L.) cultivars under terminal drought stress conditions. J. Crop Sci. Biotech. 16, 173181. Kirigwi, F.M., Ginkel, W.V., Brown-Guedira, G., Gill, B.S., Paulsen, G.M., Fritz, A.K., 2007. Markers associated with a QTL for grain yield in wheat under drought. Mol. Breed. 20, 401413. Krasensky, J., Jonak, C., 2012. Drought, salt, and temperature stress-induced metabolic rearrangements and regulatory networks. J. Exp. Bot. 63, 15931608. Landi, P., Sanguineti, M.C., Salvi, S., 2005. Validation and characterization of a major QTL affecting leaf ABA concentration in maize. Mol. Breed. 15, 291303. Lawlor, D.W., 1970. Absorption of polyethylene glycols by plants and their effects on plant growth. New Phytol. 69, 501513. Lei, Y., Yin, C., Li, C., 2006. Differences in some morphological, physiological, and biochemical responses to drought stress in two contrasting populations of Populus przewalskii. Physiol. Plant 127, 182191. Li, H., Luo, Y., Ma, J.H., 2011. Radiation-use efficiency and the harvest index of winter wheat at different nitrogen levels and their relationships to canopy spectral reflectance. Crop Pasture Sci. 62, 208217.

340


Li-Feng, L., Hong-Liang, Z., Ping, M., 2007. Construction and evaluation of near-isogenic lines for major QTLs of basal root thickness and 1000-grain weight in lowland and upland rice. Chin. J. Agric. Biotechnol. 4, 199205. Liang, P., Pardee, A.B., 1992. Differential display of eukaryotic messenger RNA by means of the polymerase chain reaction. Science 257, 967971. Ling, H.Q., Zhao, S., Liu, D., Wang, J., Sun, H., Zhang, C., et al., 2013. Draft genome of the wheat A-genome progenitor Triticum urartu. Nature 496, 8790. Liu, S.B., Zhou, R.G., Dong, Y.C., Li, P., Jia, J.Z., 2006. Development, utilization of introgression lines using a synthetic wheat as donor. Theor. Appl. Genet. 112, 13601373. Loss, S.P., Siddique, K.H.M., 1994. Morphological and physiological traits associated with wheat yield increases in mediterranean environments. Adv. Agron. 52, 229276. Lua, Y., Zhangc, S., Shah, T., Xiec, C., Haoc, Z., Lic, X., et al., 2010. Joint linkagelinkage disequilibrium mapping is a powerful approach to detecting quantitative trait loci underlying drought tolerance in maize. Proc. Natl. Acad. Sci. USA 107, 1958519590. Ma, Y., Qin, F., Tran, L.S.P., 2012. Contribution of genomics to gene discovery in plant abiotic stress. Mol. Plant 5, 11761178. Maccaferri, M., Sanguineti, M.C., Corneti, S., Ortega, J.L., Salem, M.B., Bort, J., et al., 2008. Quantitative trait loci for grain yield and adaptation of durum wheat (Triticum durum Desf) across a wide range of water availability. Genetics 178, 489511. Maccaferri, M., Sanguineti, M.C., Demontis, A., El-Ahmed, A., del Moral, L.G., Maalouf, F., et al., 2011. Association mapping in durum wheat grown across a broad range of water regimes. J. Exp. Bot. 62, 409438. Maggio, A., Zhu, J.K., Hasegawa, P.M., Bressan, R.A., 2006. Osmogenetics: aristotle to arabidopsis. Plant Cell 18, 15421557. Martin, P., Nishida, J., Afzal, J., Akbar, S., Damania, R., Hanrahan, D., 2006. Pakistan Strategic Country Environmental Assessment, South Asia Region, vol. I. World Bank, 36946-PK. Mathews, K.L., Malosetti, M., Chapman, S., McIntyre, L., Reynolds, M., Shorter, R., et al., 2008. Multienvironment QTL mixed models for drought stress adaptation in wheat. Theor. Appl. Genet. 117, 10771109. Meagher, R.B., Heaton, A.C.P., 2005. Strategies for the engineered phytoremediation of toxic element pollution: mercury and arsenic. J. Ind. Microbiol. Biotechnol. 32, 502513. Meagher, R.B., Rugh, C.L., Kandasamy, M.K., 2000. Engineered phytoremediation of mercury pollution in soil and water using bacterial genes. In: Terry, N., Ban˜uelos, G. (Eds.), Phytoremediation of Contaminated Soil and Water. CRC Press/Lewis, Boca Raton, FL. Melkus, G., Rolletschek, H., Fuchs, J., Radchuk, V., Grafahrend-Belau, E., Sreenivasulu, N., et al., 2011. Dynamic 13C/1H NMR imaging uncovers sugar allocation in the living seed. Plant Biotechnol. J. 9, 10221037. Meuwissen, T., Hayes, B.J., Goddard, M.E., 2001. Prediction of total genetic value using genome-wide dense marker maps. Genetics 157, 18191829. Micheletto, S., Rodriguez-Uribe, L., Hernandeza, R., Richinsa, R.D., Currya, J., O’Connell, M.A., 2007. Comparative transcript profiling in roots of Phaseolus acutifolius and P. vulgaris under water deficit stress. Plant Sci. 173, 510520. Ministry of Food, Agriculture and Livestock (MINFAL), 2008. Water Conservation and Productivity Enhancement Through High Efficiency (Pressurized) Irrigation Systems. Islamabad, Pakistan. Mishra, N.P., Mishra, R.K., Singh, G.S., 1993. Changes in the activities of antioxidant enzymes during exposure of intact wheat leaves to strong visible light at different temperatures in the presence of protein synthesis inhibitors. Plant Physiol. 102, 903910. Mittler, R., Vanderauwera, S., Gollery, M., Van Breusegem, F., 2004. Reactive oxygen gene network of plants. Trends Plant Sci. 9, 490498.

References

341

Montes, J.M., Melchinger, A.E., Reif, J.C., 2007. Novel throughput phenotyping platforms in plant genetic studies. Trends Plant Sci. 12, 433436. Morgan, J.M., 1977. Differences in osmoregulation between wheat genotypes. Nature 270, 234235. Morgan, J.M., 1983. Osmoregulation as a selection criterion for drought tolerance in wheat. Aust. J. Agric. Res. 34 (607-6), 14. Morgan, J.M., Hare, R.A., Fletcher, R.J., 1986. Genetic variation in osmoregulation in bread and durum wheats and its relationship to grain yield in a range of field environments. Aust. J. Agric. Res. 37, 449457. Muhammad, A.K., Abdur, R., Muhammad, Z., 2007. Water use efficiency and economic feasibility of growing rice and wheat with sprinkler irrigation in the indus basin of pakistan. Agric. Water Manage. 87, 292298. Mujeeb-Kazi, A., Kazi, A.G., Dundas, I., Rasheed, A., Ogbonnaya, F., Kishi, M., et al., 2013. Genetic diversity for wheat improvement as conduit to food security. Adv. Agron. 122, 179258. Nan, Z., Zhao, C., Li, J., Chen, F., Sun, W., 2002. Relations between soil properties and selected heavy metal concentrations in spring wheat (Triticum aestivum L) grown in contaminated soils. Water Air Soil Pollut. 133, 205213. National Drought Mitigation Center (NDMC), 2006. What is drought? University of Nebraska, Lincoln. Available at: ,www.drought.unl.edu/whatis/concept.htm.. Negrao, S., Almadanim, M.C., Pires, I.S., Abreu, I.A., Maroco, J., Courtois, B., et al., 2013. New allelic variants found in key rice salt-tolerance genes: an association study. Plant Biotechnol. J. 11, 87100. Nordborg, M., Borevitz, J.O., Bergelson, J., Berry, C.C., Chory, J., Hagenblad, J., et al., 2002. The extent of linkage disequilibrium in Arabidopsis thaliana. Nat. Genet. 30, 190193. Ogbonnaya, F.C., Abdalla, O., Mujeeb-Kazi, A., Kazi, A.G., Xu, S.X., Gosman, N., et al., 2013. Synthetic hexaploid in wheat improvement. In: Janick, J. (Ed.), Plant Breed. Rev. pp. 35122. Pakistan Bureau of Statistics, 2012. Wheat: area, production and yield. Agricultural Statistics of Pakistan, 201112. Federal Bureau of Statistics, Statistics Division, Islamabad, Pakistan. Pakistan Country Water Resources Assistance Strategy (WRAS), 2005. Water economy: running dry. South Asia Region Agriculture and Rural Development Unit. South Asia Region, Report No. 34081PK, Washington DC. Pakistan Economic Survey, 2010. 200910 Survey, Finance Division, Islamabad, Pakistan. Printing Corporation, Pakistan Press. Pakistan Water Partnership, 1999. Pakistan Country Report: Vision for the 21st Century. First Draft (Global Water Partnership South Asia Technical Advisory Committee), Islamabad. Pakistan Water Sector Strategy, 2002. In: National Water Sector Profile, vol. 5. Ministry of Water and Power National Water Sector Profile, Pakistan, pp. 142. Passioura, J.B., 1977. Grain yield, harvest index, and water use of wheat. J. Aust. Inst. Agric. Sci. 43, 117120. Peer, W.A., Baxter, I.R., Richards, E.L., 2005. Phytoremediation and hyperaccumulator plants. In: Klomp, L. W.J., Martinoia, E., Tamás, M.J. (Eds.), Molecular Biology of Metal Homeostasis and Detoxification: From Microbes to Man. Topics in Current Genetics. Springer-Verlag, New York, pp. 299340. Peleg, Z., Fahima, T., Krugman, T., Abbo, S., Yakir, D., Korol, A.B., et al., 2009. Genomic dissection of drought resistance in durum wheat 9 wild emmer wheat recombinant inbreed line population. Plant Cell Environ. 32, 758779. Pereira, L.S., Oweis, T., Zairi, A., 2002. Irrigation management under water scarcity. Agric. Water Manage. 57, 175206. Pilon-Smits, E.A.H., Freeman, J.L., 2006. Environmental cleanup using plants: biotechnological advances and ecological considerations. Front. Ecol. Environ. 4, 203210. Ping, M., Zichao, L., Chunping, L., Hongliang, Z., Changming, W., Chen, L., et al., 2003. QTL mapping of the root traits and their correlation analysis with drought resistance using DH lines from paddy and upland rice cross. Chin. Sci. Bull. 48, 27182724.

342


Pinto, R.S., Reynolds, M.P., Mathews, K.L., McIntyre, C.L., Olivares-Villegas, J.J., Chapman, S.C., 2010. Heat and drought adaptive QTL in a wheat population designed to minimize confounding agronomic effects. Theor. Appl. Genet. 121, 10011021. Price, A.H., Cairns, J.E., Horton, P., Jones, H.G., Griffiths, H., 2002a. Linking drought-resistant mechanisms to drought avoidance in upland rice using a QTL approach: progress and new opportunities to integrate stomatal and mesophyll responses. J. Exp. Bot. 53, 9891004. Price, A.H., Townend, J., Jones, M.P., Audebert, A., Courtois, B., 2002b. Mapping QTLs associated with drought avoidance in upland rice grown in the Philippines and West Africa. Plant Mol. Biol. 48, 683695. Pugnaire, F.I., Serrano, L., Pardos, J., 1999. Constraints by water stress on plant growth. In: Passarakli, M. (Ed.), Handbook of Plant and Crop Stress, 2nd ed. Marcel Dekker, New York/Basel, pp. 271283. Qadir, M., Boers, Th.M., Schubert, S., Ghafoor, A., Murtaza, G., 2003. Agricultural water management in water-starved countries: challenges and opportunities. Agric. Water Manage. 62, 165185. Qadir, M., Wichelns, D., Raschid-Sally, L., McCornick, P.G., Drechsel, P., Bahri, A., et al., 2010. The challenges of wastewater irrigation in developing countries. Agric. Water Manage. 97, 561568. Qin, F., Shinozaki, K., Yamaguchi-Shinozaki, K., 2011. Achievements and challenges in understanding plant abiotic stress responses and tolerance. Plant Cell Physiol. 52 (9), 15691582. Raju, N.L., Gnanesh, B.N., Lekha, P., Jayashree, B., Pande, S., Hiremath, P.J., et al., 2010. The first set of EST resource for gene discovery and marker development in pigeonpea (Cajanus cajan L.). BMC Plant Biol. 10, 45. Ravel, C., Praud, S., Murigneux, A., Linossier, L., Dardevet, M., Balfourier, F., et al., 2006. Identification of Glu-B1-1 as a candidate gene for the quantity of high-molecular-weight glutenin in bread wheat (Triticum aestivum L.) by means of an association study. Theor. Appl. Genet. 112, 738743. Ravi, K., Vadez, V., Isobe, S., Mir, R.R., Guo, Y., Nigam, S.N., et al., 2011. Identification of several small main-effect QTLs and a large number of epistatic QTLs for drought tolerance in groundnut (Arachis hypogaea L.). Theor. Appl. Genet. 122, 11191132. Reynolds, M.P., Ortiz, R., 2010. Adapting crops to climate change: a summary. In: Reynolds, M.P. (Ed.), Climate Change and Crop Production. CAB International, Wallingford, UK, pp. 18. Reynolds, M.P., Trethowan, R.M., 2007. Physiological interventions in breeding for adaptation to abiotic stress. In: Spiertz, J.H.J., Struik, P.C., van Laar, H.H. (Eds.), Scale and Complexity in Plant Systems Research, GenePlantCrop Relations, 21. Wageningen UR Frontis Series, pp. 129146. Reynolds, M.P., Tuberosa, R., 2008. Translational research impacting on crop productivity in drought-prone environments. Curr. Opin. Plant Biol. 11, 171179. Reynolds, M.P., Skovmand, B., Trethowan, R., Pfeiffer, W., 2000. Evaluating a conceptual model for drought tolerance. In: Ribaut, J-M., Poland, D. (Eds.), Molecular Approaches for the Genetic Improvement of Cereals for Stable Production in Water-Limited Environments: A Strategic Planning Workshop Held at CIMMYT, El Batan, Mexico, pp. 4953. Reynolds, M.P., Mujeeb-Kazi, A., Sawkins, M., 2005. Prospects for utilising plant-adaptive mechanisms to improve wheat and other crops in drought- and salinity-prone environments. Ann. Appl. Biol. 146, 239259. Reynolds, M.P., Dreccer, S., Trethowan, R., 2007a. Drought-adaptive traits derived from wheat wild relatives and landraces. J. Exp. Bot. 58, 177186. Reynolds, M.P., Pierre, C.S., Saad, A.S.I., Vargas, M., Condon, A.G., 2007b. Evaluating potential genetic gains in wheat associated with stress-adaptive trait expression in elite genetic resources under drought and heat stress. Crop Sci. 47, 172189. Reynolds, M.P., Manes, Y., Izanloo, A., Langridge, P., 2009. Phenotyping approaches for physiological breeding and gene discovery in wheat. Ann. Appl. Biol. 155, 309320.

References

343

Rhodes, D., Hanson, A.D., 1993. Quaternary ammonium and tertiary sulfonium compounds in higher plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 44, 357384. Richards, R.A., 1991. Crop improvement for temperate Australia: Future opportunities. field Crops Res. 26, 141169. Romero, P., Garcıá, J., Botıá, P., 2006. Costbenefit analysis of a regulated deficit-irrigated almond orchard under subsurface drip irrigation conditions in southeastern Spain. Irrig. Sci. 24, 175184. Roychoudhury, A., Datta, K., Datta, S.K., 2010. Abiotic stress in plants: from genomics to metabolomics. In: Tuteja, et al. (Eds.), Omics and Plant Abiotic Stress Tolerances. Bentham Science Publishers, India, pp. 91120. Rutkoski, J.E., Heffner, E.L., Sorrells, M.E., 2010. Genomic selection for durable stem rust resistance in wheat. Euphytica 179, 161173. Saeed, M., Ashrif, M., Bruen, M., 2002. Diagnostic analysis of framers skimming well technologies in the Indus Basin of Pakistan. Irrig. Drain Sys. 16, 139160. Saintenac, C., Zhang, D., Wang, S., Akhunov, E., 2013. Sequence-based mapping of the polyploid wheat genome. Genes Genomes Genet. 3, 11051114. Sairam, R.K., Deshmukh, P.S., Saxena, D.C., 1998. Role of antioxidant systems in wheat genotypes tolerance to water stress. Biol. Plant 41, 387394. Salt, D.E., Smith, R.D., Raskin, I., 1998. Phytoremediation. Annu. Rev. Plant Physiol. Plant Mol. Biol. 49, 643668. Sanguineti, M.C., Li, S., Maccaferri, M., Corneti, S., Rotondo, F., Chiari, T., et al., 2007. Genetic dissection of seminal root architecture in elite durum wheat germplasm. Ann. Appl. Biol. 151, 291305. Seckler, D., Barker, R., Amarasinghe, U., 1999. Water scarcity in the twenty-first century. Water Resour. Dev. 15, 2942. Sehgal, D., Yadav, R., 2010. Molecular markers based approaches for drought tolerance. In: Jain, S.M., Brar, D.S. (Eds.), Molecular Techniques in Crop Improvement. Springer, New York, pp. 207230. Serraj, R., Sinclair, T.R., 2002. Osmolyte accumulation: can it really help increase crop yield under drought conditions? Plant Cell Environ. 25, 333341. Serraj, R., Hash, C.T., Rivzi, S.M.H., 2005. Recent advances in marker-assisted selection for drought tolerance in pearl millet. Plant Prod. Sci. 8, 334337. Shaheen, A., Baig, M.A., 2011. Drought severity assessment in arid area of Thal Doab using remote sensing and GIS. Int. J. Water Res. Arid. Env. 1, 92101. Shakir, A.S., Qureshi, M., 2007. Irrigation water management on canal command level: a case study of lower Bari Doab canal system. Proceedings of International Conference on Water and Flood Management, Dhaka, Bangladesh. Institute of Water and Flood Management, pp. 215222. Shakir, A.S., Rehman, H., Khan, N.M., Qazi, A.U., 2011. Impact of canal water shortages on groundwater in the lower Bari Doab canal system in Pakistan. Pak. J. Eng. Appl. Sci. 9, 8797. Sinclair, T.R., 2011. Challenges in breeding for yield increase for drought. Trends Plant Sci. 16, 289293. Siopongco, J.D.L.C., Yamauchi, A., Salekdeh, H., Bennett, J., Wade, L.J., 2006. Growth and water use response of doubled-haploid rice lines to drought and rewatering during the vegetative stage. Plant Prod. Sci. 2, 141151. Song-ping, H., Hua, Y., Gui-hua, Z., Hong-yan, L., Guo-lan, L., Han-wei, M., et al., 2007. Relationship between coleoptile length and drought resistance and their QTL mapping in rice. Rice Sci. 14, 1320. Sorrells, M.E., Yu, J., 2009. Linkage disequilibrium and association mapping in the Triticeae. In: Feuillet, C., Muehlbauer, G.J. (Eds.), Genetics and Genomics of the Triticeae. Springer, New York, pp. 655683. Sreenivasulu, N., Sopory, S.K., Kishor, P.B.K., 2007. Deciphering the regulatory mechanisms of abiotic stress tolerance in plants by genomic approaches. Gene 388, 113.

344


Sreenivasulu, N., Sunkar, R., Wobus, U., Strickert, M., 2010. Array platforms and bioinformatics tools for the analysis of plant transcriptome in response to abiotic stress. Methods Mol. Biol. 639, 7193. Streuter, A.A., Mozafar, A., Goodin, J.R., 1981. Water potential of aqueous polyethylene glycol. Plant Physiol. 67, 6467. Taiz, L., Zeiger, E., 2006. Stress Physiology, fourth ed. Sinauer Asssociates, Sunderland, MA, pp. 671702. Talame, V., Ozturk, N.Z., Bohnert, H.J., Tuberosa, R., 2007. Barley transcript profiles under dehydration shock and drought stress treatments: a comparative analysis. J. Exp. Bot. 58, 229240. Tardieu, F., Tuberosa, R., 2010. Dissection and modelling of abiotic stress tolerance in plants. Curr. Opin. Plant Biol. 13, 206212. Teulat, B., Borries, C., This, D., 2001. New QTLs identified for plant water-status, water soluble carbohydrate and osmotic adjustment in a barley population grown in a growth-chamber under two water regimes. Theor. Appl. Genet. 103, 161170. Teulat, B., Zoumarou-Wallis, N., Rotter, B., Salem, M.B., Bahri, H., This, D., 2003. QTL for relative water content in field-grown barley and their stability across Mediterranean environments. Theor. Appl. Genet. 108, 181188. Tian, F., Gong, J., Zhang, J., Zhang, M., Wang, G., Li, A., et al., 2013. Enhanced stability of thylakoid membrane proteins and antioxidant competence contribute to drought stress resistance in the tasg1 wheat staygreen mutant. J. Exp. Bot. 64, 15091520. Tsonev, S., Todorovska, F., Avramova, V., Kolev, S., Abu-Mhadi, N., Christov, N.K., 2009. Genomics assisted improvement of drought tolerance in maize: QTL approaches. Biotechnol. Equip. 23, 14101413. Tuberosa, R., 2010. Phenotyping drought-stressed crops: key concepts, issues and approaches. In: Monneveaux, P., Ribaut, J.M. (Eds.), Drought Phenotyping in Crops: From Theory to Practice. Generation Challenge Programme, CIMMYT, Mexico, pp. 335. Tuberosa, R., Salvi, S., 2006. Genomics approaches to improve drought tolerance in crops. Trends Plant Sci. 11, 405412. Tuberosa, R., Sanguineti, M.C., Landi, P., 2002. Identification of QTLs for root characteristics in maize grown in hydroponics and analysis of their overlap with QTLs for grain yield in the field at two water regimes. Plant Mol. Biol. 48, 697712. Vadez, V., Kholova, J., Choudhary, S., Zindy, P., Terrier, M., Krishnamurthy, L., et al., 2011. Responses to increased moisture stress and extremes: whole plant response to drought under climate change. In: Yadav, S.S., et al. (Eds.), Crop Adaptation to Climate Change. Wiley-Blackwell Publishers, Oxford, UK, pp. 186197. Varshney, R.K., Nayak, S.N., May, G.D., 2009. Next generation sequencing technologies and their implications for crop genetics and breeding. Trends Biotechnol. 27, 522530. Varshney, R.K., Bansal, K.C., Aggarwal, P.K., Datta, S.K., Craufurd, P.Q., 2011. Agricultural biotechnology for crop improvement in a variable climate: hope or hype? Trends Plant Sci. 16, 363371. Varshney, R.K., Paulo, M.J., Grando, S., van Eeuwijk, F.A., Keizer, L.C.P., Guo, P., et al., 2012. Genome wide association analyses for drought tolerance related traits in barley (Hordeum vulgare L.). Field Crops Res. 126, 171180. Venuprasad, R., Dalid, C.O., Del Valle, M., Zhao, D., Espiritu, M., Sta Cruz, M.T., et al., 2009. Identification and characterization of large-effect quantitative trait loci for grain yield under lowland drought stress in rice using bulk-segregant analysis. Theor. Appl. Genet. 120, 177190. Verelst, W., Bertolini, E., de Bodt, S., Vandepoele, K., Demeulenaere, M., Pe, M.E., et al., 2013. Molecular and physiological analysis of growth-limiting drought stress in Brachypodium distachyon leaves. Mol. Plant 6, 311322. Wani, S.P., Sreedevi, T.K., Rockstrom, J., 2009. Rain-fed agriculture-past trend and future prospects. In: Warn, S.P., Rockstrom, J., Oweis, T. (Eds.), Rainfed Agriculture: Unlocking the Potential. Comprehensive Assessment of Water Management in Agriculture Series. Wallingford, UK: CAB International, pp. 135.

References

345

Wani, S.P., Ananta, K.H., Sreedevi, T.K., Sudi, R., Singh, S.N., D’Souza, M., 2011. Assessing the environmental benefits of watershed development: evidence from Indian semi-arid tropics. J. Sust. Watershed Sci. Manag. 1 (1), 1020. Wasson, A.P., Richards, R.A., Chatrath, R., Misra, S.C., Prasad, S.V.S., Rebetzke, G.J., et al., 2012. Traits and selection strategies to improve root systems and water uptake in water-limited wheat crops. J. Exp. Bot. 63, 34853498. Wei, B., Jing, R.C., Wang, C., Chen, J., Mao, X., Chang, X., et al., 2009. Dreb1 genes in wheat (Triticum aestivum L.): development of functional markers and gene mapping based on SNPs. Mol. Breed. 23, 1322. Welle, R., Greten, W., Rietmann, B., Alley, S., Sinnaeve, G., Dardenne, P., 2003. Near-infrared spectroscopy on chopper to measure maize forage quality parameters online. Crop Sci. 43, 14071413. Witcombe, J.R., Hollington, P.A., Howarth, C.J., Reader, S., Steele, K.A., 2008. Breeding for abiotic stresses for sustainable agriculture. Philos. Trans. R. Soc. B. 363, 703716. Worch, S., Rajesh, K., Harshavardhan, V.T., Pietsch, C., Korzun, V., Kuntze, L., et al., 2011. Haplotyping, linkage mapping and expression analysis of barley genes regulated by terminal drought stress influencing seed quality. BMC Plant Biol. 11, 114. Wright, G.C., Smith, R.C.G., Morgan, J.M., 1983. Differences between two grain sorghum genotypes in adaptation to drought stress. 3. Physiological responses. Aust. J. Agric. Res. 34, 637651. Xiao, Y.N., Li, X.H., George, M.L., Li, M.S., Zhang, S.H., Zheng, Y.L., 2005. Quantitative trait locus analysis of drought tolerance and yield in maize in China. Plant Mol. Biol. Rep. 23, 155165. Xu-rong, M., Xiu-li, Z., Vincent, V., Xiao-ying, L., 2013. Improving water use efficiency of wheat crop varieties in the north China plain: review and analysis. J. Integrat. Agr. 12, 12431250. Xue, G.P., McIntyre, C.L., Jenkins, C.L., Glassop, D., van Herwaarden, A.F., Shorter, R., 2008. Molecular dissection of variation in carbohydrate metabolism related to water-soluble carbohydrate accumulation in stems of wheat. Plant Physiol. 146, 441454. Yadav, R.S., Sehgal, D., Vadez, V., 2011. Using genetic mapping and genomics approaches in understanding and improving drought tolerance in pearl millet. J. Exp. Bot. 62, 397408. Yang, D.L., Jing, R.L., Chang, X.P., Li, W., 2007. Identification of quantitative trait loci and environmental interactions for accumulation and remobilization of water-soluble carbohydrates in wheat (Triticum aestivum L.) stems. Genetics 176, 571584. Yang, J., Zhang, J., Wang, Z., Zhu, Q., Liu, L., 2001. Water deficit-induced senescence and its relationship to the remobilization of pre-stored carbon in wheat during grain filling. Agron. J. 93, 196206. Zandalinas, S.I., Vives-Peris, V., Go´mez-Cadenas, A., Arbona, V., 2012. A fast and precise method to identify indolic glucosinolates and camalexin in plants by combining mass spectrometric and biological information. J. Agric. Food Chem. 60, 86488658. Zhang, H., Oweis, T., 1999. Water yield relations and optimal irrigation scheduling of wheat in the Mediterranean region. Agric. Water Manage. 38, 195211. Zheng, B.S., Yang, L., Zhang, W.P., 2003. Mapping QTLs and candidate genes for rice root traits under different water-supply conditions and comparative analysis across three populations. Theor. Appl. Genet. 107, 15051515.


CHAPTER

The Use of Chlorophyll Fluorescence Kinetics Analysis to Study the Performance of Photosynthetic Machinery in Plants

15

Hazem M. Kalaji, Anjana Jajoo, Abdallah Oukarroum, Marian Brestic, Marek Zivcak, Izabela A. Samborska, Magdalena D. Cetner, Izabela Łukasik, Vasilij Goltsev, Richard J. Ladle, Piotr Da˛browski and Parvaiz Ahmad

15.1 Introduction The physiological state of several photosystem II (PSII) components, electron transport chain components, and the cooperation of light-dependent and light-independent biochemical reactions can be evaluated by analysis of chlorophyll fluorescence (ChlF) induction curves (Govindjee, 1995; DeEll and Toivonen, 2003; Papageorgiou and Govindjee, 2004; Strasser et al., 2004; Kalaji et al., 2011; Suggett et al., 2011). The close cooperation and fine adjustments in the speed of these reactions is essential for the entire process of photosynthesis to proceed with high effectiveness (Murkowski, 2002; Van der Tol et al., 2009). ChlF measurements allow the recognition of changes in the general bioenergetic state of the photosynthetic apparatus. Moreover, such measurements relate, directly or indirectly, to all stages of light-dependent photosynthetic reactions, including water splitting, electron transport, and pH gradient formation across the thylakoid membrane and ATP synthesis (Kalaji et al., 2012). Nowadays, ChlF measurements are a popular method for evaluating the impact of stress factors on photosynthesis. They represent a simple, nondestructive, inexpensive, and quick tool for analyzing light-dependent photosynthetic reactions and for indirectly estimating chlorophyll content within the same sample tissue. (For basic information on the relationship of ChlF to photosynthesis, see reviews by Papageorgiou and Govindjee, 2011, and Stirbet and Govindjee (2011, 2012). Improved techniques for ChlF measurements allow for the study of the photosynthesis process at various functional levels (e.g., light-harvesting complexes, primary light reactions, electron transport chain, light-independent reactions in thylakoid stroma, and even slow regulatory processes). Scientists from different fields, such as plant physiology, biotechnology, forestry, ecophysiology, and even plant breeders and farmers, value the technical advantages of ChlF and using it study the structure and function of photosynthetic apparatus. P. Ahmad (Ed): Emerging Technologies and Management of Crop Stress Tolerance, Volume 2. DOI: http://dx.doi.org/10.1016/B978-0-12-800875-1.00015-6 © 2014 Elsevier Inc. All rights reserved.

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CHAPTER 15 The Use of Chlorophyll Fluorescence Kinetics Analysis

The value of the parameters derived from the analysis of ChlF kinetics can be used for investigating direct photosynthetic responses to adverse environmental conditions and for indirectly evaluating stress influences on plants (Kuckenberg et al., 2009). Cautiously chosen ChlF techniques allow the determination of reactions to different components of the environment, such as soil (nutrients deficiency, salinity, heavy metal content), atmosphere (the PAR quality and intensity, high and low temperatures, ozone content), and herbicides (Fracheboud and Leipner, 2003; Dai et al., 2009; Buonasera et al., 2011). Research may be carried out on a single plant (including transgenic and cultured in vitro) or on whole ecosystems to estimate potential productivity and tolerance to individual or groups of stress fac¨ quist, 1993; Schreiber et al., 1994; Krupa and Baszynski, 1995; tors (Bolhár-Nordenkampf and O Maxwell and Johnson, 2000; Strasser et al., 2000; Murkowski, 2002). By using ChlF measurements, there is a possibility to detect the impact of stress factors before morphological symptoms (e.g., wilting, necrosis, and chlorosis) become visible or even before changes in chlorophyll content become apparent (Devi and Prasad, 1996; Roshchina and Melnikova, 1996; Kalaji and Pietkiewicz, 2004; Strasser et al., 2007; Kalaji and Guo, 2008; Tsimilli-Michael and Strasser, 2008; Kuckenberg et al., 2009). ChlF potentially has extensive applications because chlorophyll a is present in all organisms capable of oxygenic photosynthesis (Embryophyta, algae, lichens, and cyanobacteria). Research techniques based on ChlF measurements are being effectively used in a range of research areas such as plant physiology and plant protection (Merz et al., 1996), bioenergetics (Wrochna et al., 2007), agriculture (Murkowski, 2002), horticulture (Flexas et al., 2002; Burzyński ˙ and Zurek, 2007), forestry (Mohammed et al., 1995; Percival et al., 2006), plant biology (Prasil et al., 1992), biotechnology (Takahashi et al., 2007), plant breeding (Kalaji and Pietkiewicz, 2004; Rykaczewska et al., 2004; Kalaji and Guo, 2008), ecology (Roger and Weiss, 2003; Chernev et al., 2006), warehousing of vegetables and fruits (Nedbal et al., 2001), and food technology and processing (Kuckenberg et al., 2008; Qiu et al., 2013). ChlF measurements are also valuable for estimating the quality of fruits, vegetables, and flowers and for defining the best time to sell them (Merz et al., 1996; Nedbal et al., 2001). They can also be used for determining seed maturity (Jalink et al., 1998), for evaluating water quality (Romanowska-Duda et al., 2005), and for estimating the allopathic impact of secondary metabolites on plant growth and development (Devi and Prasad, 1996; Roshchina and Melnikova, 1996). Measurement methods based on ChlF are among the most important instruments currently used in plant breeding programs due to their ability to indicate the physiological state of plants, providing insights into plant growth and yield under naturally occurring environmental stress conditions (Kalaji and Guo, 2008). Some ChlF parameters are recommended as trustworthy biomarkers for a variety of selections for tolerance to certain herbicide groups (e.g., urea, triazine, and diazine herbicides) (Devine et al., 1992; Dewez et al., 2008). One of the most promising techniques for automatic identification of plant species are neural networks, where the ChlF induction curve is one of the main components (Codrea et al., 2004). Thus, as can be seen from the preceding, many ChlF techniques and applications have been developed. All of them contribute to widening knowledge about photosynthesis. In this chapter, we focus mainly on fast fluorescence analysis (up to 1 s) induced by continuous illumination and obtained by JIP-test, a reliable mathematical model suggested by Strasser et al. (2004); it brings detailed information on the status and function of PSII reaction centers, antenna, as well as compounds of donor and acceptor sides of PSII. However, the main focus of this work is to outline the effects of stress factors (stressors) on photochemical processes, reflected in changes in fast ChlF kinetics and related biophysical parameters.

15.2 Chlorophyll a fluorescence and the heterogeneity of PSII

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15.2 Chlorophyll a fluorescence and the heterogeneity of PSII In nature, PSII is heterogeneous in terms of antenna and the reducing side (Guenther and Melis, 1990). Antenna heterogeneity includes antenna size and variation in the connectivity (grouping) of antenna molecules. Based on antenna size, PSII centers have been categorized as alpha (α), beta (β), and gamma (γ) (Melis and Homann, 1976). They differ from each other in life span and number of associated chlorophylls. Reducing-side heterogeneity is linked with the capability to transfer an electron from QA. Centers able to transfer electrons from QA to QB are termed QB reducing, while those that cannot do so are named QB nonreducing centers. Nowadays, research is concentrated on estimating PSII heterogeneity under biotic and abiotic stresses (Jajoo, 2013). Interest in PSII heterogeneity increased when it was observed to change under different environmental conditions. Based on recent studies, it is known that there are changes in PSII heterogeneity under high temperatures (Mathur et al., 2011), high salinity (Mehta et al., 2010a), pH (Tongra et al., 2011), and some pollutants such as polycyclic aromatic hydrocarbons (PAH) (Tomar and Jajoo, 2013). There are changes in the number of active/inactive reaction centers, interconversion of active alpha centers into inactive beta and gamma centers, and increases in the number of QB nonreducing centers under various stress conditions. There are many methods for antenna heterogeneity assessment. One of them is to estimate the heterogeneity of PSII from the fluorescence rise (FR) curve measured with DCMU (Melis and Homann, 1975, 1976). A DCMU poisoning method was used for the calculation of antenna heterogeneity (Strasser, 1978; Hsu et al., 1989): separated leaves were put into small trays filled with 100 ml DCMU solution overnight and in complete darkness—the DCMU concentration was 200 μM (Hsu et al., 1989) and the solution contained 1% ethanol to dissolve the DCMU. The leaves were removed from the DCMU solution (in darkness), wiped, and left in the air for about 1 h to avoid anaerobiosis. Alpha (α), beta (β), and gamma (γ) centers were calculated from the complementary area growth curve (Melis and Homann, 1975, 1976; Melis, 1985). This includes the calculation of growth of a normalized complementary area—determined by the fluorescence induction curve and the line parallel to the maximum level of fluorescence (Fm) with time (Ft/Fm). Kinetics of the complementary area of the dark-adapted sample were fitted with three exponential phases (corresponding to α, β, and γ). The type of centers were then recognized based on the lifetimes (τ) of each of the fractions. For example, in wheat plants grown under controlled conditions, the τ of the fastest α component was B0.37 ms, the β component was about 3.8-fold slower (τ B1.44 ms); the γ component (being slowest) was τ B9.14 ms (Schreiber et al., 2012). Their contribution to the total amplitude (A) of the kinetics of the complementary area is calculated as a percentage of the α, β, and γ centers (Strasser, 1978; Hsu Ð et al., 1989). The kinetics of QA accumulation is the kinetics of the complementary area, B 5 (Fm 2 Ft)dt, where B is the double normalized (between 0 and 1) kinetics of the complementary area (Strasser et al., 2000) and the B kinetics of the first light pulse are fitted with three exponentials that correspond to α-, β-, and γ-type centers. Treating with herbicide avoids the measurement of antenna dynamics in those systems where the rapid reorganization of antenna takes place during inhibition of linear electron flow—as during state transitions or the Zeaxanthin cycle. Nedbal et al. (1999) presented a method by which antenna heterogeneity can be measured without treatment with DCMU by a fast-repetition rate fluorescence (FRRF).

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Here, QA reduction is induced in 60 to 100 microseconds (μsec) by rapidly fired flashes of light. The reaction centers, which supply excitons at a faster rate (within 20 μsec), lead to a reduction of almost 95% in QA acceptors.

15.3 Analysis of chlorophyll fluorescence kinetics Illumination of a dark-adapted photosynthetic sample allows a polyphasic chlorophyll fluorescence induction curve (O-J-I-P-transient) (Figure 15.1). The curve’s characteristic course gives substantial information about the structure and function of the photosynthetic apparatus (Kautsky and Hirsch, ¨ quist, 1993; Schreiber et al., 1931; Lichtenthaler and Rinderle, 1988; Bolha`r-Nordenkampf and O 1994; Krupa and Baszynski, 1995; Maxwell and Johnson, 2000; Murkowski, 2002; Fracheboud and Leipner, 2003; Sayed, 2003; Kalaji and Guo, 2008; Kalaji and Łoboda, 2009). The JIP-test is based on the analysis of the rise in polyphasic fast chlorophyll a and is a method for studying the relationship between light-dependent reactions and ChlF. The JIP-test is based on the theory of “energy flow” across thylakoid membranes (Strasser et al., 2000). This theory is a simple algebraic equation, representing balance between total energy inflows and outflows, for each of the examined light-harvesting complexes. The theory also provides information on the probable distribution of the absorbed energy. By using these equations, it is possible to define the energetic communication, which is also known as the “grouping,” or

FIGURE 15.1 Typical OJIP-transient of chlorophyll fluorescence (Kautsky curve) exhibited on illumination of a dark-adapted leaf sample (4 mm2) by saturating red light (3000 μmol photons m22 s21). The graphic is plotted on a logarithmic time scale. Fluorescence values are expressed as Ft/F0, where Ft represents measured fluorescence intensity in each time interval and F0 represents fluorescence intensity at 20 μs. The figure was created using data measured by the Handy PEA device (Hansatech, England) on barley leaf and plotted according to the scheme of Strasser et al. (2000).

15.4 Examples of successful applications of ChlF measurements

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“connectivity” and “overall grouping probability,” between the PSII complexes (Kalaji and Guo, 2008; Stirbet, 2013). The evaluation of the physiological condition of photosynthetic apparatus is based on several groups of parameters, both recorded and calculated (known as the specific and phenomenological energy flows). It is also based on the analysis of PSII efficiency and the fraction of reaction centers (RCs) that are powerless to reduce the primary quinone electron acceptor of PSII (QA). These RCs are known as the heat absorbers or “silent reaction centers” (RCsi). RCsi neither reduce the QA nor transfer the excitation energy back to light-harvesting complexes. They also do not participate in ChlF. Such centers are reactivated once the stress factor that caused them descends. Other important aspects of physiological condition are functions of slow reopening of RCs fractions, which are powerless to reduce the secondary electron acceptor, plastoquinone QB, and the likelihood of the energy transfer between the numerous components of PSII. The JIP-test (OJIP) name comes from the specific points on the induction curve that is formed by the recorded ChlF signal (see Figure 15.1) and is suitable to the gradual reduction of QA—the primary electron acceptor of PSII. The J-I part of the curve corresponds to the reduction of the secondary electron acceptor QB, plastoquinone (PQ), cytochrome (Cyt b6f), and PC. The increase in ChlF in the I-P part of the induction curve is typically attributed to the reduction of electron transporters of the PSI acceptor-side: ferredoxin (Fd), intermediary acceptors, and the NADP. Stress factors (e.g., high temperature, excessive PAR, nutrient deficiency, or drought) cause the inhibition of the oxygen-evolving complex (OEC) and block the electron transport between OEC and tyrosine (Guissé et al., 1995; Guha et al., 2013). In such situations, within the 200 to 300 μs range of the ChlF induction curve, a peak occurs (K-band) that reveals a disruption in the OEC. OJIP analysis is a tool for determining the correlations between the structure and functions of the photosynthetic apparatus, which is useful in evaluating plant vitality (Strasser et al., 2000, 2004, 2010; Zushi et al., 2012). The idea of the test is to record the ChlF signal at short intervals, from 20 μs to 1 s. The most important measurements are done at 20 μs, 100 μs, 300 μs, 2 ms, 30 ms, and 1 s (see Figure 15.1). The results allow the calculation of JIP-test indicators (e.g., quantum yields, energy fluxes) (Strasser et al., 2004) used for evaluation of PSII function. The speed of electron transport in PSII is connected to high-energy electrons from the light-dependent reactions, the energy of the light-independent reactions, and the products of photosynthesis that in turn depend on plant condition and the impact of various external factors. The JIP-test thus allows the impact of various stress factors on the photosynthesis process to be evaluated in quite a short time (Srivastava et al., 1999; Strasser et al., 2000).

15.4 Examples of successful applications of ChlF measurements 15.4.1 Drought Drought negatively affects the efficiency of photosynthesis, disrupting stomatal functioning, accumulation, and transport of assimilates (Monteiro and Prado, 2006; Rampino et al., 2006; Yin et al., 2006; Hura et al., 2007; Zhou et al., 2007). Plants adapting to drought stress activate mechanisms to avoid the negative effects of water deficiency (Medrano et al., 2002; Chaves and Oliveira, 2004). Water shortage limits the carbon metabolism and utilization of the light-dependent reaction products.

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As a result, a large amount of absorbed light energy cannot be converted into chemical energy, leading to damage in PSII (Matorin et al., 1982; Cornic and Massacci, 1996; Mullet and Whitsitt, 1996; Yin et al., 2006). Moreover, water deficiency adversely affects chlorophyll content (Wright et al., 2009; Zheng et al., 2009). The decrease in photosynthesis efficiency of barley plants during drought stress may be caused by deficiencies of N, P, K, and Fe (Hussein et al., 2009) and by disorders in the structure and functions of the thylakoid membranes. These effects are followed by increased dephosphorylation of PSII proteins and fast phosphorylation of LHCII proteins such as b4 and CP29 (Liu et al., 2009). PSII has a high tolerance to water deficit (compared to PSI) and the negative effects only appear under conditions of extreme drought (Van Rensburg and Kru¨ger, 1993; Souza et al., 2004; Lauriano et al., 2006). Research piloted on several ecotypes of coconut (Cocos nucifera L.) (Gomes et al., 2008) demonstrated that drought stress limits the absorption of light energy and maximum quantum yield of PSII, decreasing electron transport speed and carboxylation efficiency. Likewise, a reduction of PSII activity due to an increase in inactive RCs, a reduction in electron transport, and enhanced energy dissipation were observed in mulberry (Morus indica L.) during progressive drought (Guha et al., 2013). The decrease in maximum quantum yield of PSII due to drought stress was also noticed in wheat (Paknejad et al., 2007; Guo´th et al., 2009a,b), olives (Sofo et al., 2009), grapevines (Wright et al., 2009), as well as in leaves of some desert shrubs (Hamerlynck and Huxman, 2009; Peeva and Cornic, 2009). In shrubs, a decrease in CO2 assimilation and inhibition of electron transport was also observed (Peeva and Cornic, 2009). A decrease in CO2 assimilation may lead to an imbalance between the PSII photochemical activity and the requirement for NADPH. In this situation, reactive oxygen species (ROS) production grows, which may be the reason for the increase in PSII sensitivity to photodestruction (Ohashi et al., 2006). In any case, ChlF measurements indicate enhanced protection of PSII and PSI photochemistry by adjusting the energy distribution between photosystems and by activating alternative electron sinks (Zivcak et al., 2013a,b). In nature, where intense radiation is followed by high temperatures and water deficits, chronic photoinhibition may occur (Souza et al., 2004). Indeed, drought and high temperature are two major abiotic stresses that affect crop growth and yield in agricultural areas and are known to occur simultaneously. The combined effect of drought and heat stress is dissimilar from that observed when they are applied separately, indicating these two stressors affect the metabolism in different ways (Dobra et al., 2010; Silva et al., 2010; Oukarroum et al., 2012). González-Cruz and Pastenes (2012) proved a higher resistance to heat in drought-stressed Orfeo INIA beans (stress-resistant variety) compared to drought-stressed Arroz Tuscola (stress-sensitive variety) chloroplasts. The authors discussed the possible involvement of xanthophyll, lipid, and fatty acid constituents in conferring resistance to high temperature in drought-stressed bean leaves. The effects of the interaction between drought-stressed leaves and high temperature on PSII have been widely studied, generally showing that the thermostability of PSII is intensified in drought-stressed leaves (Havaux, 1992; Lu and Zhang, 1999; Oukarroum et al., 2012). The existence of an antagonistic effect between drought stress and heat stress in plants has also been noted. Indeed, thermotolerance of plants to high temperature is possibly due to the accumulation of some osmolytes (i.e., proline) during exposure to stress (Ashraf and Foolad, 2007). Further, drought stress may enhance the resistance of PSII to heat stress as shown by the disappearance of band K from the OJIP transient, as illustrated in Figure 15.2 (Oukarroum et al., 2012).


3300

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P Control I

Fluorescence intensity (a.u.)

2800

Drought stress + 45°C 2300 45°C J

1800 K 1300 O 800

300 0.01

0.1

1 10 Time (ms)

100

1000

FIGURE 15.2 Fast Chl a fluorescence transient exhibited by barley leaves kept in a dark-adapted condition. After two weeks of growth, the drought treatment was initiated by withholding water for a period of two weeks. The heat stress was applied to detached leaves of drought-stressed plants and a control by exposing leaves to 45 C during 10 min; after 5 min of adaptation to ambient temperature, chlorophyll a fluorescence was measured. The transients are plotted on a logarithmic time scale. Source: The figure was created using the data published in Oukarroum et al. (2012).

ChlF detection is used for monitoring drought stress in plants. A detailed analysis of recorded data gives important information about the course of photosynthesis under conditions of water defi¨ quist, 1993; Schweiger et al., 1996; ciency in plant tissues and organs (Bolha`r-Nordenkampf and O Yordanov et al., 1997; Hura et al., 2007). Currently, there is no universal agreement on the influence of drought on the photosynthetic apparatus, based on the modifications of the values of ChlF parameters (Hura et al., 2007; Guo´th et al., 2009a,b; Munné-Bosch et al., 2009). The ChlF method can be a useful tool for screening genotypes for drought tolerance (Van Rensburg et al., 1996; Oukarroum et al., 2006; Gomes et al., 2012; Guha et al., 2013). Drought stress can, directly or indirectly, influence the photosynthetic activity of plants and as a consequence alter ChlF kinetics. The FR during the first 2 to 3 ms is related to primary photochemistry. It has been suggested that stimulated L and K bands (see Figures 15.1 and 15.2) can be used as a tool for estimating the potential to cope with drought stress (Oukarroum et al., 2007). The L band is affected by the excitation energy transfer between PSII units, commonly denoted as connectivity or grouping (Strasser and Stirbet, 1998). The K band has been related to a dissociation of the oxygen-evolving complex (OEC) (Guissé et al., 1995). The measurement of OLKJIP fluorescence transients and their analysis using the JIP-test might be used as potential indicators for drought stress tolerance and physiological disturbances before the appearance of visible signs of drought stress.

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One of the more well-known parameters from the OJIP transient is the performance index (PI), which provides quantitative information about the general state of plants and their vitality. The PI has been created out of three independent expressions: the concentration of the reaction center per chlorophyll, an expression related to primary photochemistry, and an expression correlated to electron transport (Strasser et al., 2004). Thus, the PI is susceptible to any changes in either antenna properties, trapping efficiency, or electron transport beyond QA. The PI was found to be sensitive to prolonged postanthesis drought stress in winter wheat (Zivcak et al., 2008b). The drought tolerance of wheat genotypes estimated from PI values recorded in drought stress is also related to the drought tolerance assessed by grain yield (Zivcak et al., 2008c). The PI is closely associated with the drought factor index (DFI) and is able to demonstrate large differences in drought responses among plant genotypes. The DFI characterizes the relative drought-induced reduction of PI during a freely defined time of drought stress. This explanation was used by Strauss et al. (2006) for the detection of dark-chilling tolerance in soybean genotypes. DFI has also been used in the characterization of 10 barley varieties (Oukarroum et al., 2007) and 21 mutant germplasm of sesame (Boureima et al., 2012) in terms of drought stress. The most tolerant and the most sensitive landraces of barley and Sorghum bicolour from Egypt were identified using the PI parameter and the ChlF fast-induction curve (Jedmowski et al., 2013). These studies proved that it is possible to differentiate between drought-tolerant and drought-sensitive cultivars at the level of PSII. An increase of ABS/RC ratio under drought stress has been noted (Van Heerden et al., 2007; Gomes et al., 2012), possibly due to inactivation of some PSII RCs or an increase in antenna size. The inactivation of RCs (non-QA reducing or heat sink centers) may be an indication of susceptibility to photoinhibition. This implies downregulation of photochemical activity during drought periods, dissipating the excess of absorbed light as heat. Drought stress has many effects on photosynthetic systems. For example, it can affect the relative amplitude of the I-P phase from the OJIP curve. The I-P phase has been documented as the slowest phase of the fluorescence rise (approximately 30200 ms) and was parallel to another reduction of plastocyanin PC1 and P7001 in PSI (Schreiber et al., 1989; Schansker et al., 2003). The I-P phase seems to be correlated with PSI reaction center content as determined by 820-nm transmission measurements (Ceppi et al., 2012). Moreover, the extent of the I-P loss in the barley varieties as a dependency on their drought tolerance has been proved (Oukarroum et al., 2009; Ceppi et al., 2012). ChlF is emitted following a dark-to-light transition of a photosynthetic sample; during light-to-dark transition, delayed fluorescence (DF) emission is detected (Goltsev et al., 2009; Strasser et al., 2010; Kalaji et al., 2012). The delayed fluorescence was described by Strehler and Arnold (1951) and is emitted mainly from PSII. DF is thought to reflect the recombination, in the dark, between the reduced primary electron acceptor QA2 and the oxidized donor (P6801) of PSII that are formed after light-induced charge separation. The shape of DF induction curve depends on the sample type and its physiological state. Simultaneous measurements of Chl a fluorescence (prompt fluorescence, PF), DF, modulates reflection at 820 nm (MR820), and far-red light (735 nm) reflection (RR) have been developed to obtain rate constants for different photosynthetic reactions (Strasser et al., 2010). Proposed by Goltsev et al. (2013), the Sigma scheme explains the source of the previously mentioned signals in the photosynthetic electron transport chain (Figure 15.3). Using this technique, Goltsev et al. (2012)


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FIGURE 15.3 Σ-Scheme explaining the source of PF, DF, and MR820 signals in the photosynthetic electron transport chain. The boxes represent structural components. Light gray arrows show physical signals that can be measured and dark gray arrows show electron and energy flows recalculated from these signals. Signals: DF, delayed fluorescence; PF, prompt fluorescence; MR, modulated reflection; RR, far-red light (735 nm) reflection. Flows: TR, energy trapping; E21, energy migration from PSII antennas to PSI (spillover); ED, electron donation toward PSII from water or ID, from internal donors; RE, electron flow through PSI to NADP; CE, cycle electron flow. RC1 and RC2 are the reaction center chlorophylls of PSI and PSII, respectively, and the other abbreviations are the standard abbreviations used for the classic Z-scheme of photosynthetic light reactions. Source: Adapted from Goltsev et al. (2010).

observed that reoxidation of QA2 was inhibited during drought stress and that there was a suppression of quantum yields of photoinduced electron transport in PSII reaction centers to QA together with a reduction of the fast phase of photoinduced kinetics of the modulated reflection signal (Figure 15.4). Extra water may also affect photosynthesis causing yield drop. An excess of water in the soil (waterlogging) reduces soil oxygen availability for plant roots. Research on the cockspur coral tree (Erythrina crista-galli L.) revealed a reduction in chlorophyll content, an increase in energy dissipation through chlorophyll a fluorescence, and modifications of ChlF parameters, indicating damage to the structure and function of PSII in plants under flood stress (Larré et al., 2013).

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FIGURE 15.4 JIP-test parameters and the DF parameter I1/I2, calculated from 1184 sets of PF and DF induction curves measured in detached bean leaves with various water content. The spider plot presents the parameters calculated from leaves with different RWC. For each group, 50 measurements from leaves with similar RWC were averaged. The values are normalized to the value at 100% RWC (Goltsev et al., 2012). The parameters of the JIP-test represent quantum yields of photo-induced electron transport in the PSII reaction center to QA (ϕPo), from QA2 to plastoquinone (ϕEo), or from PQ to terminal acceptors of PSI (ϕRo); efficiency/ probability that the electron reaches electron carriers after QA 2 (ψEo), or that the electron is transferred from the intersystem electron carriers to the electron acceptors at the PSI acceptor side (δRo); probability that a PSII chlorophyll molecule functions as a RC (γRC); approximated initial slope (in ms21) of the fluorescence transient normalized to the maximal variable fluorescence Fv (M0); absorption flux from the antenna per RC, which is a measure of PSII apparent antenna size (ABS/RC); trapped energy flux (per RC), which reduces QA (TR0/RC); performance indexes for conservation of energy of the photons absorbed by PSII in the form of reduced intersystem electron acceptors (PIABS) or in the form of reduced acceptors of PSI (PItotal). I1/I2 is the ratio of amplitudes of maxima of delayed fluorescence in the fast phase of the DF induction curve (Goltsev et al., 2005). The spider plot graphically represents the drought-induced modification in the photosynthetic machinery. Each level of drought is represented by a polygon with corners corresponding to the relative (to the values of fully hydrated leaf) JIP parameters, as well as a ratio of two peaks in the induction curve of DF (I1/I2). This ratio was found to be inversely connected to electron flow in PSII (Zaharieva et al., 2001). The functional state of photosynthetic machinery can be visualized as a geometric figure with a shape that is specific for drought stress. It is sensitive to the different levels of desiccation and is why the constellation of the selected parameters can be used for empirical estimation of RWC (Goltsev et al., 2012).

15.4.2 Salinity Plant responses to salinity stress are dependent on many aspects such as the expression of the specific genes, plant development stage, and glycine betaine accumulation, which protects the photosynthetic apparatus by stabilizing the external proteins of the PSII complex (Murata et al., 1992; Belkhodja et al., 1994). Ashraf and Harris (2004) observed that, under high-light intensity, salinity stress increases zeaxanthin synthesis. Zeaxanthin increases dissipation of excessive energy,


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protecting the photosynthetic apparatus against photoinhibition. Salinity stress disturbs the electron transport from the RCs to the plastoquinone pool (Strasser et al., 2000; Roger and Weiss, 2003). Schreiber et al. (1994) and Pereira et al. (2009) identified the OEC as one of the most sensitive components in the photosynthetic electron transport chain. Its reduced performance is usually caused by the electron transport disorder. Likewise, Fricke and Peters (2002) showed that salinity stress reduces osmotic water uptake, decreasing the value of Fv/F0. Modifications can also be observed at the level of ChlF parameters and PSII functioning. Under conditions of high salinity, electron trapping in the PSII reaction center becomes less efficient, which may be due to the dissociation of LHCII and PSII (Havaux, 1993). Such a loss of PSII efficiency has been recorded in barley Hordeum vulgare L. (Belkhodja et al., 1994; Kalaji and Guo, 2008). A decrease in maximum quantum yield of PSII and an increase in nonphotochemical quenching have been proved in a number of plant species, including barley (Kalaji and Rutkowska, 2004), rice (Cha-um et al., 2009), cultivated tobacco (Yang et al., 2008), tomato (Zribi et al., 2009), and even among certain halophytes such as Sarcocornia fruticosa L. Moreover, in tomato (He et al., 2009; Zribi et al., 2009) and cucumber seedlings, the following parameters were limited during salinity stress: PSII efficiency in light, electron transport chain efficiency, and the efficiency of PSII open reaction centers in light (Zhang and Sharkey, 2009). Mehta et al. (2010b) showed that the destruction caused due to salinity stress in wheat was more pronounced at the donor side than the acceptor side of PSII, and that the damage caused by this kind of stress was fully reversible (B100%) at the acceptor side of PSII, while recovery of the donor side was less than 85% (Figure 15.5).

FIGURE 15.5 The OJIP Chl a fluorescence transient curve (logarithmic time scale) in wheat leaves exposed to various concentrations of NaCl for 1 h of dark. Source: Adapted from Mehta et al. (2010b).

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15.4.3 Heavy metals The photosynthetic process may be disrupted by high levels of heavy metals, but the impact of particular heavy metal ions can be specific and depends on plant species (Ku¨pper et al., 1996; Wierzbicka, 1999; Antosiewicz, 2005; Romanowska-Duda et al., 2005; Sharma and Dubey, 2005). PSI is known to be more tolerant to heavy metal stress than PSII (Ku¨pper et al., 1996; Joshi and Mohanty, 2004; Romanowska et al., 2006; Shcolnick and Keren, 2006; Tuba et al., 2010).

15.4.3.1 Lead Lead (Pb) also has harmful effects on plants (Moustakas et al., 1994). Gas emission from coal-fueled power plants, fuel gases, and industrial technology are considered as the main sources of lead in soil (Mishra and Dubey, 2005). Lead causes changes in respiration and increases ATP and the ATPADP ratio, a result of mitochondrial production of this high-energy compound (Romanowska et al., 2002). Another effect of lead stress is the decreasing efficiency of photosynthesis in plants, a disruption of chloroplast ultrastructure and thylakoid membrane lipid composition, and a reduction of synthesis of chlorophyll and carotenoids (Sharma and Dubey, 2005). Lead disturbs the uptake of nutrients (e.g., magnesium and iron) essential for the process of photosynthesis. In addition, it causes the dissociation of the polypeptides OEC and the removal of Ca, Cl, and Mn compounds from this complex (Sharma and Dubey, 2005; Pál et al., 2006; Romanowska et al., 2006). In the O-J-I-P induction curve of the Arabi Aswad variety of barley exposed to lead stress, the intensities of fluorescence at the I and P steps decreased compared to the control, and a peak in point K occurred (Kalaji and Łoboda, 2007), as shown in Figure 15.6. The appearance of this point on the ChlF-induction curve may be related to electron transport inhibition between the OEC and the PSII reaction center (Strasser et al., 2004; Wu et al., 2008). Models of lead stress suggest that energy absorption and dissipation within the PSII are high, while electron trapping and transport are reduced (Lazár and Jablonsky´, 2009).

15.4.3.2 Cadmium Cadmium (Cd) is very harmful and enters living organisms through the food chain. Phosphate fertilizers and industrial waste products are the most common sources of cadmium to the environment (Romanowska et al., 2006; Kalaji and Łoboda, 2007). Cadmium does not appear to affect the amount of photosynthetic pigments; research on oilseed rape Brassica napus L. seedlings, which grew in the presence of this chemical element for two weeks, showed insignificant changes in the content of chlorophyll a, chlorophyll b, and carotenoids (Janeczko et al., 2005). However, cadmium does have a negative influence on the photochemical efficiency of the photosynthetic process (see Figure 15.6). PSII is more sensitive to its impact than the PSI, indicating that cadmium disturbs the PSII functions with greater intensity (Mallick and Mohn, 2003). Cadmium affects both the donor and acceptor sides of PSII. On the donor side, Cd inhibits the OEC, while on the acceptor side it inhibits electron transport between QA2 and QB2 (Sigfridsson et al., 2004). Disruption of the electron transport chain is related to degradation of the LHCII oligomer. The presence of Cd ions also increases the heat dissipation of excitation energy—defined as nonphotochemical quenching (Jalink et al., 1998; Janeczko et al., 2005). A detailed analysis of ChlF records from oilseed rape revealed that cadmium caused a decrease in the specific energy flow per sample cross-section. Decreases in RC/CS, ETo/CS, and in the activity of OEC were observed (Janeczko et al., 2005). Fv/Fm is known to be the least sensitive to Cd impact parameter,


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FIGURE 15.6 Leaf model showing phenomenological energy fluxes per excited cross-section. This is a cross-section of 2 barley Syrian landraces, Arabi Abiad and Arabi Aswad, grown without stress (control) and after a 7-d lead and cadmium treatment. ABS/CS0, absorption flux per CS approximated by F0; TR/CS0, trapped energy flux per CS; ET/CS0, electron transport flux per CS; DI/CS0, dissipated energy flux per CS. Each relative value is represented by the size of the proper parameters (arrow); empty circles represent reducing QA reaction centers (active); full black circles represent nonreducing QA reaction centers (inactive or silent). Color intensity of the leaves is proportional to their chlorophyll content calculated by Biolyzer software (Kalaji and Łoboda, 2007).

indicating the maximum quantum yield of PSII. Plant resistance to the unfavorable effects of Cd is related to the ability of “sweeping” ROS, launching protective mechanisms (e.g., activation of antioxidant enzymes) in particular peroxidase (Ekmekçi et al., 2008), and the synthesis of antioxidantactive compounds (e.g., glutathione) according to Streb et al. (2008).

15.4.4 Nutrient deficiency Nutrient deficiency—for example, nitrogen (N), phosphorus (P), potassium (K), calcium (Ca), magnesium (Mg), sulfur (S), or iron (Fe)—in the growth medium disrupts the functioning of the

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photosynthetic apparatus. This decreases PSII photochemical efficiency and modifies the values of the ChlF parameters (Sharma and Swarup, 1988; Smethurst et al., 2005). Figures 15.7a,b show the effect of nutrient deficiency on maize and tomato plants.

15.4.4.1 Nitrogen Nitrogen (N) availability is one of the most important factors limiting the growth of plants. This element is a component of all proteins and nucleic acids and other organic compounds such as chlorophyll, heme, alkaloids, and amines (Masclaux-Daubresse et al., 2010). It is also a basic component of many compounds involved in photosynthesis. A large part of N in plants is localized in leaf chloroplasts. The thylakoid membranes contain about 20 to 25% of the total nitrogen in leaves. Thus, deficiency of this macroelement modifies thylakoid membranes and disturbs their functioning, leading to acceleration of chloroplast aging and plastoglobule formation (Correia et al., 2005; Wu et al., 2006). Nitrogen is also an important element in RuBisCO photosynthetic complexes (Lambers et al., 1998), the CalvinBenson cycle enzymes, chlorophyll, and carotenoids (Correia et al., 2005). Nitrogen deficiency also leads to reductions in transpiration, stomatal conductance, chlorophyll and carotenoids content, and the concentration of soluble sugars (Ciompi et al., 1996; Huang et al., 2004; Pompelli et al., 2010). Insufficient N uptake also reduces the electron acceptor pool in PSII and decreases RuBisCO and phosphoenolpyruvate carboxylase (PEPCase) activity (Correia et al., 2005).

15.4.4.2 Phosphorus Phosphorus (P) is also an important element for plant growth and development. In the lithosphere, there is a great amount of this element; however, its availability to the plants is low and its uptake is often too low. Phosphorus is the main ingredient of many essential molecules involved in key enzymatic reactions such as glycolysis, starch synthesis, and CO2 utilization in plants (Marschner, 1995). Even a slight P shortage in plant tissues can cause an increase in chlorophyll content in the leaves. Major deficits cause modifications in grain and thylakoid structure and in light-harvesting complexes absorbing PAR, thus reducing PSII activity (Foyer and Spencer, 1986). Phosphorus deficiency also has a negative impact on NADPH regeneration (Marschner, 1995), reducing the quantum yield and carboxylic efficiency of photosynthesis (Rao et al., 1990), and electron transport efficiency (Lauer et al., 1989; Jacob and Lawlor, 1991; Wu et al., 2006). The JIP-test has been successfully used to evaluate the activity/efficiency of PSII in plants under P deficiency stress (Van Rensburg and Kru¨ger, 1993; Kru¨ger et al., 1997; Ouzounidou et al., 1997; Strasser, 1997; Ripley et al., 2004; Tsimilli-Michael and Strasser, 2008). Indeed, various studies have shown that JIP-test parameters are related to the gas exchange and plant growth parameters (Strasser et al., 2000; Ripley et al., 2004).

15.4.4.3 Potassium

Potassium (K) plays an important role in cellular osmoregulation. K1 ions are necessary to retain the pH gradient across the thylakoid membrane (Rampino et al., 2006). Potassium deficiency increases stomatal conductance resistance, limiting carbon dioxide diffusion through the stomata. In photosynthesis, the role of potassium in activation of numerous enzymes and in ATP synthesis is probably much more significant than in controlling the stomatal functioning (see www.ipipotash. org). Knowledge about the impact of K deficiency on photosynthetic apparatus efficiency and PSII

FIGURE 15.7 Effect of nutrient deficiency on differential plots of relative chlorophyll a fluorescence. Panel A shows leaves of maize and Planel B shows tomato plants. Changes in OJIP FR kinetics were revealed when we calculated the difference in variable fluorescence curves (ΔVt). ΔVt curves were constructed by subtracting the normalized fluorescence values (between O and P) recorded in ND plants from those recorded in control plants.

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functioning is still limited. Nevertheless, some photosynthetic parameters, such as electron transport efficiency and maximum quantum yield of PSII, are known to decrease under potassium deficiency (Schweiger et al., 1996).

15.4.4.4 Magnesium Magnesium (Mg) is the core component of the chlorophyll molecule. In nondeficient plants up to 6% of Mg21 ions are bound to chlorophyll a and b molecules (Scott and Robson, 1990a,b; Marschner, 1995). Magnesium plays an important role in packaging of thylakoids (Fork, 1986) and the chloroplast mRNA (e.g., RNA) of D1 protein in PSII (Guha et al., 2013). This element activates numerous enzymes of photosynthesis, carbohydrate accumulation and distribution processes, and phloem loading (Paknejad et al., 2007; Zahedi and Alahrnadi, 2007; Gomes et al., 2008). The healthy functioning of cyclic and noncyclic photophosphorylation, which takes place in the chloroplasts, also depends on the presence of Mg. Moreover, magnesium activates certain steps of the pentose cycle in which the reconstruction of ribulose-1,5-bisphosphate (the CO2 acceptor in photosynthesis) takes place (Peeva and Cornic, 2009). A decrease in photosynthetic efficiency is an early symptom of Mg deficiency, resulting mainly from the strong relationship of this element with the structure and functioning of chloroplasts and chlorophyll (Zahedi and Alahrnadi, 2007). However, magnesium deficiency limits CO2 assimilation intensity, even before chlorophyll is reduced. The negative influence of magnesium deficiency on chloroplast functioning can be detected by monitoring modifications in the values of ChlF parameters (Smethurst et al., 2005).

15.4.4.5 Iron Iron (Fe) plays central role for stimulating chlorophyll synthesis. Iron-containing ferredoxin and cytochromes are also important plant porphyrins, as they ensure the conversion of absorbed light energy into high-energy chemical compounds. Iron deficiency leads to modifications in the structure and the functioning of the Embryophyta photosynthetic apparatus (Ohashi et al., 2006; Hamerlynck and Huxman, 2009) and reduces photosynthetic productivity (Dobra et al., 2010) by decreasing the amount of photosynthetic units per sample cross-section (Silva et al., 2010). One of the most typical symptoms of Fe deficiency is chlorosis caused by a decrease in chlorophyll content in leaves (Abadıá and Abadıá, 1993; Morales et al., 1994; Bertamini et al., 2002; Molassiotis et al., 2006; Oukarroum et al., 2012). Chlorotic leaves were characterized by a decrease in PSII activity and electron transport efficiency. A significant decrease in PSII performance is caused by a reduction in the amount of the D1 and 33 kDa proteins in the OEC (Bertamini et al., 2002). Further, modifications of the PSII to the PSI ratio in the thylakoid and the membrane lipid structure were observed (Ohashi et al., 2006). Some researchers reported that Fe deficiency causes qualitative and quantitative modifications in some protein complexes such as PSI CC, LHCI 680, D1, CP43, and LHCII (Bertamini et al., 2002; Ferraro et al., 2003). Other researchers, based on ChlF measurement techniques, reported that iron deficiency induces the formation of new pigment protein and decreases PSII efficiency due to the partial detachment of the internal LHCII and RCs (Morales et al., 2001). Reduced values of ChlF the parameters Fv/Fm and Fv/F0 indicate a decrease in PSII efficiency induced by iron deficiency (Bertamini et al., 2002; Molassiotis et al., 2006).


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15.4.4.6 Sulfur Sulfur (S) is a significant element for plant growth and development (Hura et al., 2007). It is absorbed from the environment in ionic form, SO422, reduced in the leaves (involving ATP), and then attached to sulfonic amino acids groups (e.g., cysteine, cystine, and methionine) (Hell and Rennenberg, 1998; Guo´th et al., 2009a,b). Sulfur also plays an important role in the formation of carbohydrates and fats (Monteiro and Prado, 2006), photosynthesis and biosynthesis of chlorophyll, and numerous proteins (Yin et al., 2006; Zhou et al., 2007). It plays an important role in heavy metal and xenobiotics detoxification and is considered of high importance in redox reactions (Matorin et al., 1982; Medrano et al., 2002; Chaves and Oliveira, 2004; Guo´th et al., 2009b). Sulfur deficiency causes a reduction in the assimilation area and in chlorophyll a and b content (Wright et al., 2009). Research on barley plants showed no correlation between sulfur availability and the values of the ChlF parameters such as photochemical quenching and electron transport efficiency (Liu et al., 2009). A very recent work from D’Hooghe et al. (2013) showed the effect of S limitation on the photosynthetic machinery. Sulfur limitation leads to photosynthesis and carbon metabolism disturbances that may be responsible for the oxidative stress observed in the young leaves of oilseed rape. Despite this, induction of proteins involved in oxidative stress resistance and energy production showed that the leaf capacity to capture and use photosynthetic active radiations for ATP production remains efficient for as long as possible (Figure 15.8).

15.4.4.7 Calcium Calcium (Ca) plays a role in maintaining cell structure, stress resistance (against drought, low and high temperatures, pathogen infection), and intracellular signal transduction (Van Rensburg and Kru¨ger, 1993). Cellular calcium is also a regulator that is directly involved in the several steps of the photosynthetic process. It is a regulator of the activity of phosphatases, which are involved in the cycle of CO2 reduction, and controls chloroplast NAD1 kinase through the calmodulin protein (Mullet and Whitsitt, 1996). Moreover, Ca takes part in OEC in the PSII, in the functioning of PSII reaction centers, and in electron transport (Hussein et al., 2009). Calcium ions (e.g., magnesium and chloride ions) play an important role in the synthesis of the oxygen-evolving complex (Liu et al., 2009). Calcium-deficient olive trees Olea europaea L. have a reduced PSII maximal photochemical productivity compared to nondeficient trees. Calcium deficiency has a negative effect on light energy absorption and distributions between PSII and PSI, electron transport, and oxygen evolution (Lauriano et al., 2006). Most previous research suggested that more attention should be paid to the role of calcium in both light-dependent and light-independent reactions of photosynthesis (Hussein et al., 2009).

15.4.5 Photosynthetically active radiation Photosynthetically active radiation (PAR) of 400 to 700 nm is the most important source of energy for plants. However, a too high or too low PAR intensity may become a stress factor, causing photoinhibition and disturbing the functioning of the photosynthetic apparatus (Howarth and Durako, 2013), as shown in Figure 15.9. During the daytime, PAR is constantly changing and plants try to keep a balance between converting radiation energy and protecting the photosynthetic apparatus against photoinhibition and repairing possible damage (Demmig-Adams et al., 1995; Bertamini and Nedunchezhian, 2003). Despite awareness of the damaging effect of light stress on

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FIGURE 15.8 Putative sequence of events provoked by a 35-d S limitation on the electron transfer chain and ATP synthase in a young leaf chloroplast. Proteins, processes (18), or biochemical compounds that are effectively repressed or induced by S restriction are indicated, respectively, by dotted or plain blue lines, while those that are postulated to be repressed or induced are shown by black lines. In Control, the electron transfer chain produced NADPH required for CO2 assimilation. After 35 d under low S conditions, we observed: (1) a repression of ferredoxin-NADP reductase (FNR) and plastocyanin (PC), which could cause a perturbation of the electron transfer and a lower production of NADPH 1 H1; (2) the decline in CO2 assimilation, probably linked to NADPH 1 H1 depletion; (3) an intercellular CO2 accumulation concomitant with the photosynthesis reduction; (4) the lower abundance of FNR may also result in the transfer of electrons to O2 by Ferredoxin (Fdx), producing O2•2; (5) a higher abundance of Cu-Zn superoxide dismutase (SOD), which suggests that the O22 detoxification into H2O2 could be increased; (6) an accumulation of H2O2, probably due to an ineffective detoxification process such as the repression of glutathione S-transferase, which leads to an oxidative stress; (7) an accumulation of water-soluble chlorophyll binding protein (WSCP), while the chlorophyll content is maintained, may signify that chlorophylls are protected against oxidative stress and that photosystems remain efficient; (8) an accumulation of ATP synthase F1 complex, which in association with the H1 accumulation in the lumen due to proper functioning of photosystems and electron chains, suggests that ATP production is favored. CF0, membrane-embedded subunit of ATP synthase; CF1, catalytic subunit of ATP synthase; Cyt b6f, cytochrome b6f complex; LHC, light harvesting complex; PQ, plastoquinone. Source: Courtesy of D’Hooghe et al. (2013).


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FIGURE 15.9 Transient chlorophyll a fluorescence induction curves of two Syrian landraces (Arabi Abiad and Arabi Aswad) grown under low- and high-light stresses for 7 d. Source: Adapted from Kalaji et al. (2012).

gas exchange, chlorophyll content, chloroplast ultrastructure, and enzymatic activity, the response of the photosynthetic apparatus to this kind of stress still has not been sufficiently studied. Light absorption in plants is controlled by the heat dissipation of absorbed photon energy, ensuring the quanta of energy necessary to create the products of photochemical reactions used in the process of CO2 assimilation (Demmig-Adams et al., 1995; Ruban and Horton, 1995; Horton et al., 1996). In high radiation conditions, the light-harvesting complexes are supplied with an excessive amount of photons causing an excess of excited states in PSII reaction centers. This leads to photoinhibition of the light-dependent reactions of photosynthesis, which can be detected by changes in some measured chlorophyll fluorescence parameters (Figure 15.10). The photoinhibition is due to photodamage or D1 protein deficiency, which occurs when denaturation occurs at a higher rate than synthesis. The main cause of photoinhibition may be the formation of photochemically inactive PSII reaction centers, which transform excitation energy into heat (Bertamini and Nedunchezhian, 2003; Redondo-Go´mez et al., 2009). There are two types of known photoinhibition—total and transient. Total photoinhibition is the result of photodamage of the photosynthetic apparatus in plants growing under dim light after exposure to strong light. In contrast, transient photoinhibition is connected to energy dispersion (dissipation) and appears mainly in plants that grow in full sun conditions (Osmond, 1994; Cai and Xu, 2002).

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FIGURE 15.10 Changes in the relative levels of fluorescence emitted as minimal fluorescence (F0), maximum fluorescence (Fm), and the ratio of variable to maximum fluorescence (Fv/Fm). Graphics are of mature and young leaves of V. vinifera L. at different time intervals. Data are given in percentage of untreated controls. Control values for F0, Fm, and Fv/Fm were 2.7, 12.8, 0.789 for mature leaves and 2.7, 14.2, 0.809 for young leaves. Source: Courtesy of Bertamini and Nedunchezhian (2003).


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ChlF parameters are a useful tool to monitor PSII reaction to changes in light intensity (Cai and Xu, 2002; Sofo et al., 2009) and spectral composition (Gilbert et al., 2009). For example, an increase in nonphotochemical quenching was noted in olive plants (Olea europaea L.) exposed to strong light. This shows that the plants were able to control photoexcitation more effectively due to the xanthophyll cycle mechanism of heat dissipation (Johnson et al., 1993; Demmig-Adams et al., 1995). Further, olive trees growing in dim light used the light energy more efficiently. This was evidenced by an increase in photochemical quenching and a decrease in heat dissipation. These observations were confirmed by the analysis of the fluorescence induction curve for plants growing in dim light. Reduced respiration suggested that shaded plants used a greater amount of absorbed light energy for the photosynthesis process (Sofo et al., 2009).

15.4.6 Temperature In certain latitudes, low temperature is a major factor limiting crop yield (Yang et al., 2009). In the Northern Hemisphere, low temperatures during the winter and early spring are usually followed by intense PAR. These conditions can lead to degradation of the thylakoid structure and distortion in light-dependent photosynthetic reactions (Murkowski, 2002). Moreover, the light-independent reac¨ quist et al., 1987; Yu et al., tions of photosynthesis are extremely inhibited by low temperatures (O 2002). A decrease in photosynthetic efficiency during photoinhibition can be an effective regulatory mechanism, avoiding damage to PSI and PSII (D’Ambrosio et al., 2006). Low temperatures decrease photosynthesis due to partial stomatal closure, slowdown of electron transport, inhibition of carbohydrate metabolism, and interference of phloem loading (Savitch et al., 1997; Allen and Ort, 2001; Huang and Guo, 2005). Cold stress affects photosynthetic apparatus by causing distortion in sugar synthesis, reducing the utilization of phosphates, and reducing phosphorylation efficiency due to electron transport slowdown (Savitch et al., 1997). This can cause ¨ quist a decrease in the ADP/ATP ratio and an increase in the probability of photoinhibition (O et al., 1987; Labate and Leegood, 1988; Godde and Bornman, 2004). Research conducted on Pelargonium cuttings exposed to low temperature stress confirmed a decrease in the maximum quantum yield of PSII and the increase in nonphotochemical quenching (Druege and Kadner, 2008). In addition, a decrease in the following parameters were noted in bitter melon plants (Momordica charantia L.) exposed to cold stress: chlorophyll content, OEC efficiency on the donor side of PSII, photochemical quenching, and efficiency of open PSII reaction centers (Yang et al., 2009). Some plant species are known for their tolerance to low temperatures. In such conditions, they are characterized by less photoinhibition of PSII; for example, pea plants show only small modifications in the values of ChlF parameters to cold stress (Streb et al., 2008). Heat stress in plants is one of the main factors limiting productivity and biomass production (Boyer, 1982). Certainly, exposure to high temperatures is known as one of the most important external influences affecting the overall process of photosynthesis (Bukhov and Mohanty, 1999) and as the most sensitive of plant cell processes to high temperatures (Yordanov et al., 1986; Sharkey and Schrader, 2006). Heat stress causes changes in the reductionoxidation properties of PSII acceptors and reduces the efficiency of photosynthetic electron transport in both photosystems (Murkowski, 2002). Heat stress affects the values of ChlF parameters. For example, in response to high temperature stress, apples Malus x Domestica Borkh showed a decrease in both the ratio of reduced acceptors

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Fluorescence intensity (relative unit)

(plastoquinone), QA2 to RC, and the ratio of reduced acceptors (plastoquinone), QB2 to QA2. A decrease in the maximum quantum yield of PSII and an increase in the minimal fluorescence value were also noted by Chen et al. (2009), as shown in Figure 15.11. High temperature stress in South African succulents caused the loss of RuBisCO catalytic efficiency and a decrease in the PSII performance index. These changes were related to the area of active PSII RCs and to the slowdown of electron transport per leaf-excited photosynthetic area (Musil et al., 2009). The shape of the O-J-I-P curve is also influenced by high temperature stress. A decrease in Fm and an increase in F0 have also been observed. The increase in F0 may relate to the release of LHC II from the PSII complex and inactivation of PSII photochemical reactions, or an inhibition of electron flow from reduced transfer of QA to QB (Ducruet and Lemoine, 1985). Yamane et al. (1997, 1998) observed the increase of F0 in spinach and rice. This phenomenon was due to irreversible dissociation of LHC II from the PSII complex and the partially reversible inactivation of PSII. The decrease in the fluorescence Fm level may be related to denaturation of chlorophyll proteins (Yamane et al., 1997).

1.2 1.0 0.8

25 °C

44 °C

35 °C 40 °C

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(a)

(b)

42 °C

0.6 0.4 0.2 0.0 100 101 102 103 104 105 106 107 100 101 102 103 104 105 106 107 3.0 (c) (d) 2.5

Wt

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500

1000

1500

2000 0

500

1000

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Time (μs)

FIGURE 15.11 Chlorophyll a fluorescence transient plotted on a logarithmic scale in the sun-exposed peel (a and c) and the shaded peel (b and d) of Fuji apple in response to temperature treatments for 30 min in the dark. Wt denotes the ratio of variable fluorescence at K-step to the amplitude FJ 2 F0, which was calculated as: Wt 5 (Ft 2 F0)4(FJ 2 F0). Source: Courtesy of Chen et al. (2009).


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The well-explored heat stress symptom is K peak (at 300 μs) and is thought to indicate the imbalance between electron transport in the OEC complex from pheophytin to primary electron acceptor QA (Strasser et al., 2000; Lazár, 2006). Indeed, the OEC at the donor side of PSII is sensitive to heat stress. In wheat, a treatment at 35 C did not harm photosynthetic efficiency, while 45 C caused irreversible damage to the OEC (Schreiber et al., 2012). The direct cause of the ChlF curve peak at point K is the outflow of electrons from P680 to PSII acceptors, which overcompensates the inflow of electrons from the donor side of PSII to P680. The change of K peak is also affected by changes in the energetic relationships between photosystems II (De Ronde et al., 2004). An increase in the FK/FJ ratio, presented by Srivastava and Strasser (1995) to describe heat stress in pea leaves, showed that heat stress inhibits the donation of electrons by the OEC. The fast ChlF technique is a useful tool to monitor PSII thermostability. The most efficient approach is to estimate the critical temperature—that is, the threshold level above which there is a sharp increase/decrease of the observed parameter (Brestic and Zivcak, 2013). Decreases of Fv/Fm were observed in numerous indigenous plant species from South Africa, as well as increases in variable fluorescence in the K-step that appears at lower temperatures than the increase of F0. PSII temperature tolerance can also be evaluated by testing one temperature level. However, experiments with wheat genotypes indicated that the segregation of genotypes by thermal tolerance was successful only if the threshold temperature level was applied—at too low or too high testing temperatures there were no differences between genotypes (Zivcak et al., 2008a). PSII thermotolerance depends on plant species and the physiological status of the plant. For example, PSII thermostability in wheat under field conditions changes during the vegetation period (Brestic et al., 2013) and is increased when the maximum air temperature crossed B30 C. Further, moderate temperatures did not cause PSII thermostability to return to the initial level. The thermostability of OEC (as indicated by the K-step) was enhanced more than the thermostability indicated by the F0 level (Brestic et al., 2012). Some genotypes can serve as donors of enhanced heat tolerance in crop-breeding programs. For example, the response of heat-treated common bean (Phaseolus vulgaris L.) lines and their recovery were observed by changes in ChlF induction and analyzed by means of the JIP-test (Stefanov et al., 2011). PSII thermostability of 30 genotypes of winter wheat plants (T. aestivum L.) with different geographic origins were identified using fast ChlF kinetics (Brestic et al., 2012). These examples also demonstrated a possible practical application of the ChlF technique.

15.4.7 Ozone Ozone (O3) is one of the most harmful phytotoxic air pollutants (Matyssek et al., 1997; Degl’Innocenti et al., 2007) mainly due to its oxidizing potential, which in plants regulates the production of ROS. Photosynthesis is especially sensitive to ozone (Heath, 1994; Schraudner et al., 1997) because it decreases the photosynthetic efficiency directly, affecting stomatal conductance (Robinson et al., 1998). It also acts indirectly by reducing the speed of the electron transport and disturbing the biochemical activity of the Calvin cycle (Calatayud and Barreno, 2001; Calatayud et al., 2002; Degl’Innocenti et al., 2002, 2007). According to Bussotti et al. (2011), the first impact of O3 on the photosynthetic apparatus is the reduction of PSI density and a decreased capability of the final electron acceptors (ferredoxin and NADP1) and ribulose-1,5-bisphosphate to maintain electron transport. As a result, the CalvinBenson

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cycle is not supplied, which leads to an imbalance between electrons sent by the electron transport chain (ETC) and those reaching the acceptors beyond PSI. Electrons that cannot reach acceptors can pass the excitation energy to oxygen molecules producing ROS, which cause photooxidation. Protective mechanisms against this kind of stress involve dissipation of excessive energy, expressed as a reduction of values of Fm, Fv/Fm, and RC/CS parameters, and nonphotochemical quenching (Degl’Innocenti et al., 2007; Chaudhary et al., 2013); regulation of OEC activity is revealed as an early occurrence of the K-band (Bussotti et al., 2011). Plant responses to ozone stress differ among species and even among cultivars of the same species (Guidi et al., 2000; Degl’Innocenti et al., 2007).

15.4.8 Herbicides Herbicides are substances used to reduce unwanted weeds so that crop yield increases. They disrupt the physiological processes of both the target plants and the crops on which they are applied. Herbicides affect PSII by binding the active ingredient to the specific D1 protein and blocking electron transport. The starvation and the overproduction of ROS, causing damage to membrane lipids, have also been reported (Schuler and Rand, 2008). One such biologically active herbicide is isoproturon used for annual grass (e.g., barley and wheat) protection. This compound is a photosynthesis inhibitor (Achhireddy et al., 1985; Dopierała, 2008) and causes disruption in the synthesis of pigments, leading to chlorosis (see www.bayercropscience.pl). The analysis of ChlF signals shown in plants treated with isoproturon indicates PSII inactivation and severe inhibition of electron transport (Dewez et al., 2008).

15.5 Conclusion and future prospects In nature, plants are exposed to many adverse factors that interfere with the photosynthetic process, leading to declines in growth, development, and yield. Photosynthetic performance and responses to environmental constraints have been assessed through biophysical, biochemical, physiological, ecological, and agronomic studies. In addition to the different, mostly time-consuming methods, noninvasive techniques based on chlorophyll a fluorescence allow valuable information on photochemical properties of leaves to be obtained rapidly. Despite its apparent simplicity, the analysis of fluorescence provides detailed information on the status and function of the photosystem II (PSII) reaction centers, antenna, and both the donor and acceptor sides of PSII. Further development of portable devices may facilitate widespread application of this method in the near future. Application of the chlorophyll fluorescence technique is very promising. It can be exploited in precision agriculture, plant phenotyping, and advanced plant breeding programs. The technique also can be employed to identify/predict a specific stressor effect on vitality, performance and growth of plants or nutrient deficiency, drought, salinity, fungi, and other stressor effects without any chemical or other destructive impact on samples. In addition, it may be able to be used to estimate the proper harvesting time for fruits and crops without any chemical analysis. The National Aeronautics and Space Administration (NASA) plans to use this tool to detect the existence of life on other planets. A measured signal of chlorophyll fluorescence means chlorophyll existence, which in turn means photosynthesis and life. Many national alarm systems to control biological threats in water ecosystems also can be built on the basis of measurements of chlorophyll fluorescence signals from algae or phytoplankton.

Abbreviations

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Abbreviations AASatomic absorption spectroscopy ABAabscisic acid ABSabsorption flux ABS/CSabsorption of photon flux per cross-section of a sample BoRelative amount of QB-nonreducing PSII centers Chlchlorophyll ChlFchlorophyll fluorescence CScross-section of the sample Cyt b6fcytochrome b6f DCMU(3-(3,4-dichlorophenyl)-1,1dimethylurea, Diuron) DFdelayed (chlorophyll) fluorescence DFIdrought factor index DI/CSdissipation of energy per crosssection ETelectron transport flux ETCelectron transport chain ET/CSelectron transport flux per crosssection of a sample F0minimal (chlorophyll) fluorescence Fdferredoxin FLfluorescence Fmmaximal fluorescence FNRferredoxin-NADP 1 oxidoreductase FRfluorescence rise Fvvariable fluorescence I820 nmtransmission at 820 nm LEDlight-emitting diode LHC (II)light-harvesting complex (of PSII), M-PEAmultifunction plant efficiency analyzer, Hansatech, UK MR820modulated reflection at 820 nm Nturnover number of QA2 NADPHnicotinamide adenine dinucleotide phosphate, reduced

NDnutrient deficiency/deficient OECoxygen evolving complex P680 excited PSII reaction center P700PSI reaction center PAHpolycyclic aromatic hydrocarbons PARphotosynthetically active radiation PCplastocyanin PCAprincipal component analysis PEAplant efficiency analyzer PEPCasephosphoenolpyruvate carboxylase PFprompt (chlorophyll) fluorescence Pheopheophytin PIperformance index PQplastoquinone PSI, PSIIphotosystem I, II QAprimary plastoquinone electron acceptor of PSII QBsecondary plastoquinone electron acceptor RCreaction center RCsisilent reaction center RC/CSdensity of active PSII reaction centers per cross-section of a sample REreduction of PSI end electron acceptors per cross-section a sample ROSreactive oxygen species RuBisCORibulose-1,5-bisphosphate carboxylase/oxygenase TR/CS trapping of excitation energy per cross-section of sample TyrZtyrosine 161 of PSII D1 protein VJvariable (chlorophyll) fluorescence at 2 ms VKthe variable fluorescence at 0.3 ms ΔVamplitude of variable fluorescence

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References Abadıá, J., Abadıá, A., 1993. Iron and plant pigments. In: Barton, L.L., Hemming, B.C. (Eds.), Iron Chelation in Plants and Soil Microorganisms. Academic, New York, pp. 327343. Achhireddy, N.R., Singh, M., Achhireddy, L.L., Nigg, H.N., Nagy, S., 1985. Isolation and partial characterization of phytotoxic compounds from lantana (Lantana camara L.). J. Chem. Ecol. 11 (8), 979988. Allen, D.J., Ort, D.R., 2001. Impacts of chilling temperatures on photosynthesis in warm-climate plants. Trends Plant Sci. 6 (1), 3642. Antosiewicz, D.M., 2005. Study of calcium-dependent lead-tolerance on plants differing in their level of Cadeficiency tolerance. Environ. Pollut. 134 (1), 2334. Ashraf, M., Foolad, M., 2007. Roles of glycine betaine and proline in improving plant abiotic stress resistance. Environ. Exp. Bot. 59 (2), 206216. Ashraf, M., Harris, P., 2004. Potential biochemical indicators of salinity tolerance in plants. Plant Sci. 166 (1), 316. Belkhodja, R., Morales, F., Abadia, A., Gomez-Aparisi, J., Abadia, J., 1994. Chlorophyll fluorescence as a possible tool for salinity tolerance screening in barley (Hordeum vulgare L.). Plant Physiol. 104 (2), 667673. Bertamini, M., Nedunchezhian, N., 2003. Photoinhibition of photosynthesis in mature and young leaves of grapevine (Vitis vinifera L.). Plant Sci. 164 (4), 635644. Bertamini, M., Muthuchelian, K., Nedunchezhian, N., 2002. Iron deficiency induced changes on the donor side of PS II in field grown grapevine (Vitis vinifera L. cv. Pinot noir) leaves. Plant Sci. 162 (4), 599605. ¨ quist, G., 1993. Chlorophyll fluorescence as a tool in photosynthesis research. Bolha`r-Nordenkampf, H., O In: Hall, D.O., Scurlock, J.M.O., Bolha`r-Nordenkampf, H.R., Leegood, R.C., Long, S.P. (Eds.), Photosynthesis and Production in a Changing Environment: A Field and Laboratory Manual. Chapman and Hall, London, UK, pp. 193206. Boureima, S., Oukarroum, A., Diouf, M., Cisse, N., Van Damme, P., 2012. Screening for drought tolerance in mutant germplasm of sesame (Sesamum indicum) probing by chlorophyll a fluorescence. Environ. Exp. Bot. 81, 3743. Boyer, J.S., 1982. Plant productivity and environment. Science 218, 443448. Brestic, M., Zivcak, M., 2013. PSII fluorescence techniques for measurement of drought and high temperature stress signal in crop plants: protocols and applications. Molecular Stress Physiology of Plants. Springer, pp. 87131. Brestic, M., Zivcak, M., Kalaji, H.M., Carpentier, R., Allakhverdiev, S.I., 2012. Photosystem II thermostability in situ: environmentally induced acclimation and genotype-specific reactions in Triticum aestivum L. Plant Physiol. Biochem. 57, 93105. Brestic, M., Zivcak, M., Olsovska, K., Repkova, J., 2013. Involvement of chlorophyll a fluorescence analyses for identification of sensitiveness of the photosynthetic apparatus to high temperature in selected wheat genotypes. Photosynthesis Research for Food, Fuel and the Future. Springer, Berlin Heidelberg, pp. 510513. Bukhov, N.G., Mohanty, P., 1999. Elevated temperature stress effects on photosystems: characterization and evaluation of the nature of heat induced impairments. In: Singhai, G.S., Renger, G., Sopory, S.K., Irrgang, K.D., Govindjee (Eds.), Concepts in Photobiology: Photosynthesis and Photomorphogenesis. Narosa Publishing House, New Delhi, India, pp. 617648. Buonasera, K., Lambreva, M., Rea, G., Touloupakis, E., Giardi, M., 2011. Technological applications of chlorophyll a fluorescence for the assessment of environmental pollutants. Anal. Bioanal. Chem. 401 (4), 11391151. ˙ Burzyński, M., Zurek, A., 2007. Effects of copper and cadmium on photosynthesis in cucumber cotyledons. Photosynthetica 45 (2), 239244.

References

373

Bussotti, F., Desotgiu, R., Cascio, C., Pollastrini, M., Gravano, E., Gerosa, G., et al., 2011. Ozone stress in woody plants assessed with chlorophyll a fluorescence. A critical reassessment of existing data. Environ. Exp. Bot. 73, 1930. Cai, S.-Q., Xu, D.-Q., 2002. Light intensity-dependent reversible down-regulation and irreversible damage of PSII in soybean leaves. Plant Sci. 163 (4), 847853. Calatayud, A., Barreno, E., 2001. Chlorophyll a fluorescence, antioxidant enzymes and lipid peroxidation in tomato in response to ozone and benomyl. Environ. Pollut. 115 (2), 283289. Calatayud, A., Ramirez, J.W., Iglesias, D.J., Barreno, E., 2002. Effects of ozone on photosynthetic CO2 exchange, chlorophyll a fluorescence and antioxidant systems in lettuce leaves. Physiol. Plant. 116 (3), 308316. Ceppi, M.G., Oukarroum, A., C ¸ içek, N., Strasser, R.J., Schansker, G., 2012. The IP amplitude of the fluorescence rise OJIP is sensitive to changes in the photosystem I content of leaves: a study on plants exposed to magnesium and sulfate deficiencies, drought stress and salt stress. Physiol. Plant. 144 (3), 277288. Cha-um, S., Charoenpanich, A., Roytrakul, S., Kirdmanee, C., 2009. Sugar accumulation, photosynthesis and growth of two indica rice varieties in response to salt stress. Acta Physiol. Plant. 31 (3), 477486. Chaudhary, N., Singh, S., Agrawal, S.B., Agrawal, M., 2013. Assessment of six Indian cultivars of mung bean against ozone by using foliar injury index and changes in carbon assimilation, gas exchange, chlorophyll fluorescence and photosynthetic pigments. Environ. Monit. Assess. 185 (9), 77937807. Chaves, M., Oliveira, M., 2004. Mechanisms underlying plant resilience to water deficits: prospects for watersaving agriculture. J. Exp. Bot. 55 (407), 23652384. Chen, L.-S., Li, P., Cheng, L., 2009. Comparison of thermotolerance of sun-exposed peel and shaded peel of “Fuji” apple. Environ. Exp. Bot. 66 (1), 110116. Chernev, P., Goltsev, V., Zaharieva, I., Strasser, R.J., 2006. A highly restricted model approach quantifying structural and functional parameters of photosystem II probed by the chlorophyll a fluorescence rise. Ecol. Eng. Environ. Prot. 5, 1929. Ciompi, S., Gentili, E., Guidi, L., Soldatini, G.F., 1996. The effect of nitrogen deficiency on leaf gas exchange and chlorophyll fluorescence parameters in sunflower. Plant Sci. 118 (2), 177184. Codrea, M.C., Nevalainen, O.S., Tyystja¨rvi, E., Vandeven, M., Valcke, R., 2004. Classifying apples by the means of fluorescence imaging. Int. J. Pattern Recognit. Artif. Intell. 18 (02), 157174. Cornic, G., Massacci, A., 1996. Leaf photosynthesis under drought stress. In: Baker, N.R. (Ed.), Photosynthesis and the Environment. Kluwer Academic Publishers, pp. 347366. Correia, C.M., Pereira, J.M.M., Coutinho, J.F., Bjo¨rn, L.O., Torres-Pereira, J.M.G., 2005. Ultraviolet-B radiation and nitrogen affect the photosynthesis of maize: a Mediterranean field study. Eur. J. Agron. 22 (3), 337347. D’Ambrosio, N., Arena, C., De Santo, A.V., 2006. Temperature response of photosynthesis, excitation energy dissipation and alternative electron sinks to carbon assimilation in Beta vulgaris L. Environ. Exp. Bot. 55 (3), 248257. D’Hooghe, P., Escamez, S., Trouverie, J., Avice, J.-C., 2013. Sulphur limitation provoke physiological and leaf proteome changes in oilseed rape that lead to perturbation of sulphur, carbon and oxidative metabolisms. BMC Plant Biol. 13, 23. Dai, Y., Shen, Z., Liu, Y., Wang, L., Hannaway, D., Lu, H., 2009. Effects of shade treatments on the photosynthetic capacity, chlorophyll fluorescence, and chlorophyll content of Tetrastigma hemsleyanum Diels et Gilg. Environ. Exp. Bot. 65 (23), 177182. De Ronde, J., Cress, W., Kru¨ger, G., Strasser, R., Van Staden, J., 2004. Photosynthetic response of transgenic soybean plants, containing an Arabidopsis P5 CR gene, during heat and drought stress. J. Plant Physiol. 161 (11), 12111224. DeEll, J.R., Toivonen, P.M., 2003. Practical Applications of Chlorophyll Fluorescence in Plant Biology. Springer, pp 259.

374


Degl’Innocenti, E., Guidi, L., Soldatini, G., 2002. Effect of chronic O3 fumigation on the activity of some Calvin cycle enzymes in two poplar clones. Photosynthetica 40 (1), 121126. Degl’Innocenti, E., Guidi, L., Soldatini, G.F., 2007. Effects of elevated ozone on chlorophyll a fluorescence in symptomatic and asymptomatic leaves of two tomato genotypes. Biol. Plant. 51 (2), 313321. Demmig-Adams, B., Adams, W.I., Logan, B., Verhoeven, A., 1995. Xanthophyll cycle-dependent energy dissipation and flexible photosystem II efficiency in plants acclimated to light stress. Funct. Plant Biol. 22 (2), 249260. Devi, S., Prasad, M., 1996. Influence of ferulic acid on photosynthesis of maize: analysis of CO2 assimilation, electron transport activities, fluorescence emission and photophosphorylation. Photosynthetica 32 (1), 117127. Devine, M., Duke, S.O., Fedtke, C., 1992. Physiology of Herbicide Action. PTR Prentice Hall. Dewez, D., Didur, O., Vincent-Héroux, J., Popovic, R., 2008. Validation of photosynthetic-fluorescence parameters as biomarkers for isoproturon toxic effect on alga Scenedesmus obliquus. Environ. Pollut. 151 (1), 93100. Dobra, J., Motyka, V., Dobrev, P., Malbeck, J., Prasil, I.T., Haisel, D., et al., 2010. Comparison of hormonal responses to heat, drought and combined stress in tobacco plants with elevated proline content. J. Plant Physiol. 167 (16), 13601370. Dopierała, U., 2008. Effectiveness of herbicides control of Tripleurospermum indorom (L.) Schultz-Bip. from the region of Copper Foundry “Głogo´w” action. Ecol. Chem. Eng., A 15 (12), 4145. Druege, U., Kadner, R., 2008. Response of post-storage carbohydrate levels in pelargonium cuttings to reduced air temperature during rooting and the relationship with leaf senescence and adventitious root formation. Postharvest Biol. Technol. 47 (1), 126135. Ducruet, J.M., Lemoine, Y., 1985. Increased heat sensitivity of the photosynthetic apparatus in triazineresistant biotypes from different plant species. Plant Cell Physiol. 26, 419429. Ekmekçi, Y., Tanyolac, D., Ayhan, B., 2008. Effects of cadmium on antioxidant enzyme and photosynthetic activities in leaves of two maize cultivars. J. Plant Physiol. 165 (6), 600611. Ferraro, F., Castagna, A., Soldatini, G.F., Ranieri, A., 2003. Tomato (Lycopersicon esculentum M.) T3238FER and T3238fer genotypes. Influence of different iron concentrations on thylakoid pigment and protein composition. Plant Sci. 164 (5), 783792. Flexas, J., Escalona, J.M., Evain, S., Gulıás, J., Moya, I., Osmond, C.B., Medrano, H., 2002. Steady-state chlorophyll fluorescence (Fs) measurements as a tool to follow variations of net CO2 assimilation and stomatal conductance during water-stress in C3 plants. Physiol. Plant. 114 (2), 231240. Fork, D.C., 1986. Changes in the content and form of magnesium in photosynthesis. Annu. Rev. Plant Physiol. Plant Mol. Biol. 37, 335361. Foyer, C., Spencer, C., 1986. The relationship between phosphate status and photosynthesis in leaves. Planta 167 (3), 369375. Fracheboud, Y., Leipner, J., 2003. The application of chlorophyll fluorescence to study light, temperature, and drought stress. Practical Applications of Chlorophyll Fluorescence in Plant Biology. Springer, pp. 125150. Fricke, W., Peters, W.S., 2002. The biophysics of leaf growth in salt-stressed barley. A study at the cell level. Plant Physiol. 129 (1), 374388. Gilbert, M., Po¨rs, Y., Grover, K., Weingart, I., Skotnica, J., Grimm, B., et al., 2009. Intra-and interspecific differences of 10 barley and 10 tomato cultivars in response to short-time UV-B radiation: a study analysing thermoluminescence, fluorescence, gas-exchange and biochemical parameters. Environ. Pollut. 157 (5), 16031612. Godde, D., Bornman, J., 2004. Regulation of photosynthesis in higher plants. In: Archer, M.D., Barber, J. (Eds.), Molecular to Global Photosynthesis. Imperial College Press, London, pp. 4951.

References

375

Goltsev, V., Chernev, P., Zaharieva, I., Lambrev, P., Strasser, R.J., 2005. Kinetics of delayed chlorophyll a fluorescence registered in milliseconds time range. Photosynth. Res. 84, 209215. Goltsev, V., Zaharieva, I., Chernev, P., Strasser, R.J., 2009. Delayed chlorophyll fluorescence as a monitor for physiological state of photosynthetic apparatus. Biotechnol. Biotechnol. Equip. 23, 452457 (special edition). Goltsev, V., Gurmanova, M., Kouzmanova, M., Yordanov, I., Qiang, S., Pentland, A., et al., 2010. Analysis of dark drops, dark-induced changes in chlorophyll fluorescence during the recording of the OJIP transient. In: Kuang, T., Lu, C., Zhang, L. (Eds.), Photosynthesis Research for Food, Fuel and Future. Springer-Verlag, Berlin, Heidelberg, pp. 179183. Goltsev, V., Zaharieva, I., Chernev, P., Kouzmanova, M., Kalaji, H.M., Yordanov, I., et al., 2012. Droughtinduced modifications of photosynthetic electron transport in intact leaves: analysis and use of neural networks as a tool for a rapid non-invasive estimation. Biochim. Biophys. Acta 1817 (8), 14901498. Gomes, F.P., Oliva, M.A., Mielke, M.S., de Almeida, A-AF, Leite, H.G., Aquino, L.A., 2008. Photosynthetic limitations in leaves of young Brazilian Green Dwarf coconut (Cocos nucifera L. “nana”) palm under well-watered conditions or recovering from drought stress. Environ. Exp. Bot. 62 (3), 195204. Gomes, M.T.G., da Luz, A.C., dos Santos, M.R., do Carmo Pimentel Batitucci, M., Silva, D.M., Falqueto, A. R., 2012. Drought tolerance of passion fruit plants assessed by the OJIP chlorophyll a fluorescence transient. Sci. Hortic. 142, 4956. González-Cruz, J., Pastenes, C., 2012. Water-stress-induced thermotolerance of photosynthesis in bean (Phaseolus vulgaris L.) plants: the possible involvement of lipid composition and xanthophyll cycle pigments. Environ. Exp. Bot. 77, 127140. Govindjee, 1995. Sixty-three years since Kautsky: chlorophyll a fluorescence. Aust. J. Plant Physiol. 22, 131160. Guenther, J.E., Melis, A., 1990. The physiological significance of photosystem II heterogeneity in chloroplasts. Photosynth. Res. 23 (1), 105109. Guha, A., Sengupta, D., Reddy, A.R., 2013. Polyphasic chlorophyll a fluorescence kinetics and leaf protein analyses to track dynamics of photosynthetic performance in mulberry during progressive drought. J. Photochem. Photobiol. B, Biol. 119, 7183. Guidi, L., Di Cagno, R., Soldatini, G.F., 2000. Screening of bean cultivars for their response to ozone as evaluated by visible symptoms and leaf chlorophyll fluorescence. Environ. Pollut. 107 (3), 349355. Guissé, B., Srivastava, A., Strasser, R., 1995. The polyphasic rise of the chlorophyll a fluorescence (OKJIP) in heat stressed leaves. Arch. Sci. Geneve 48, 147160. ´ ., Csiszár, J., Horváth, F., Pécsváradi, A., Cseuz, L., Erdei, L., 2009a. Chlorophyll Guo´th, A., Tari, I., Gallé, A a fluorescence induction parameters of flag leaves characterize genotypes and not the drought tolerance of wheat during grain filling under water deficit. Acta Biol. Szeged. 53, 17. ´ ., Csiszár, J., Pécsváradi, A., Cseuz, L., Erdei, L., 2009b. Comparison of the Guo´th, A., Tari, I., Gallé, A drought stress responses of tolerant and sensitive wheat cultivars during grain filling: changes in flag leaf photosynthetic activity, ABA levels, and grain yield. J. Plant Growth Regul. 28 (2), 167176. Hamerlynck, E.P., Huxman, T.E., 2009. Ecophysiology of two Sonoran Desert evergreen shrubs during extreme drought. J. Arid Environ. 73 (45), 582585. Hankamer, B., Barber, J., Boekema, E.J., 1997. Structure and membrane organization of photosystem II in green plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 48, 641671. Havaux, M., 1992. Stress tolerance of photosystem II in vivo antagonistic effects of water, heat, and photoinhibition stresses. Plant Physiol. 100 (1), 424432. Havaux, M., 1993. Rapid photosynthetic adaptation to heat stress triggered in potato leaves by moderately elevated temperatures. Plant Cell Environ. 16 (4), 461467. He, Y., Zhu, Z., Yang, J., Ni, X., Zhu, B., 2009. Grafting increases the salt tolerance of tomato by improvement of photosynthesis and enhancement of antioxidant enzymes activity. Environ. Exp. Bot. 66 (2), 270278.

376


Heath, R., 1994. Possible mechanisms for the inhibition of photosynthesis by ozone. Photosynth. Res. 39 (3), 439451. Hell, R., Rennenberg, H., 1998. The plant sulphur cycle. Sulphur in Agroecosystems. Springer, pp. 135173. Horton, P., Ruban, A., Walters, R., 1996. Regulation of light harvesting in green plants. Annu. Rev. Plant Biol. 47 (1), 655684. Howarth, J.F., Durako, M.J., 2013. Diurnal variation in chlorophyll fluorescence of Thalassia testudinum seedlings in response to controlled salinity and light conditions. Mar. Biol. 115. Hsu, B.D., Lee, Y.S., Jang, J.R., 1989. A method for analysis of fluorescence induction curve from DCMUpoisoned chloroplasts. Biochim. Biophys. Acta 975, 4449. Huang, M., Guo, Z., 2005. Responses of antioxidative system to chilling stress in two rice cultivars differing in sensitivity. Biol. Plant. 49 (1), 8184. Huang, Z.-A., Jiang, D.-A., Yang, Y., Sun, J.-W., Jin, S.-H., 2004. Effects of nitrogen deficiency on gas exchange, chlorophyll fluorescence, and antioxidant enzymes in leaves of rice plants. Photosynthetica 42 (3), 357364. Hura, T., Grzesiak, S., Hura, K., Thiemt, E., Tokarz, K., We˛dzony, M., 2007. Physiological and biochemical tools useful in drought-tolerance detection in genotypes of winter triticale: accumulation of ferulic acid correlates with drought tolerance. Ann. Bot. 100 (4), 767775. Hussein, M.M., Abd El-Kader, A.A., Mona, A.M.S., 2009. Mineral status of plant shoots and grains of barley under foliar fertilization and water stress. Res. J. Agric. Biol. Sci. 5, 108115. Jacob, J., Lawlor, D., 1991. Stomatal and mesophyll limitations of photosynthesis in phosphate deficient sunflower, maize and wheat plants. J. Exp. Bot. 42 (8), 10031011. Jajoo, A., 2013. Changes in photosystem II in response to salt stress. Ecophysiology and Responses of Plants under Salt Stress. Springer, pp. 149168. Jalink, H., Van der Schoor, R., Frandas, A., Van Pijlen, J.G., Bino, R.J., 1998. Chlorophyll fluorescence of Brassica oleracea seeds as a non-destructive marker for seed maturity and seed performance. Seed Sci. Res. 8 (4), 437443. Janeczko, A., Koscielniak, J., Pilipowicz, M., Szarek-Lukaszewska, G., Skoczowski, A., 2005. Protection of winter rape photosystem 2 by 24-epibrassinolide under cadmium stress. Photosynthetica 43 (2), 293298. Jedmowski, C., Ashoub, A., Bru¨ggemann, W., 2013. Reactions of Egyptian landraces of Hordeum vulgare and Sorghum bicolor to drought stress, evaluated by the OJIP fluorescence transient analysis. Acta Physiol. Plant. 35 (2), 345354. Johnson, G., Young, A., Scholes, J., Horton, P., 1993. The dissipation of excess excitation energy in British plant species. Plant Cell Environ. 16 (6), 673679. Joshi, M.K., Mohanty, P., 2004. Chlorophyll a fluorescence as a probe of heavy metal ion toxicity in plants. Chlorophyll a Fluorescence; A Signature of Photosynthesis. Springer, pp. 637661. Kalaji, H.M., Łoboda, T., 2007. Photosystem II of barley seedlings under cadmium and lead stress. Plant Soil Environ. 53, 511516. Kalaji, H.M., Carpentier, R., Allakhverdiev, S.I., Bosa, K., 2012. Fluorescence parameters as early indicators of light stress in barley. J. Photochem. Photobiol. B, Biol. 112, 16. Kalaji, M., Pietkiewicz, S., 2004. Some physiological indices to be exploited as a crucial tool in plant breeding. Plant Breed. Seeds Sci. 49, 1939. Kalaji, M., Rutkowska, A., 2004. Reactions of photosynthetic apparatus of maize seedlings to salt stress. Zesz Probl Post Nauk Rol 496, 545558. Kalaji, M.H., Guo, P., 2008. Chlorophyll fluorescence: a useful tool in barley plant breeding programs. In: Sanchez, A., Gutierrez, S.J. (Eds.), Photochemistry Research Progress. Nova Science Publishers Inc., New York, pp. 439463.

References

377

Kalaji, M.H., Łoboda, T., 2009. Chlorophyll Fluorescence Studies of the Physiological Condition of Plants. Publisher SGGW, Warsaw Poland (in Polish). Kalaji, M.H., Govindjee, Bosa, K., Koscielniak, J., Zuk-Golaszewska, K., 2011. Effects of salt stress on Photosystem II efficiency and CO2 assimilation of two Syrian barley landraces. Environ. Exp. Bot. 73, 6472. Kautsky, H., Hirsch, A., 1931. Neue Versuche zur Kohlensaureassimilation. Naturwissenschaften 19, 964. Kru¨ger, G.H.J., Tsimilli-Michael, M., Strasser, R.J., 1997. Light stress provokes plastic and elastic modifications in structure and function of photosystem II in camellia leaves. Physiol. Plant. 101, 265277. Krupa, Z., Baszynski, T., 1995. Some aspects of heavy metals toxicity towards photosynthetic apparatus— direct and indirect effects on light and dark reactions. Acta Physiol. Plant. 17 (2), 177190. Kuckenberg, J., Tartachnyk, I., Noga, G., 2008. Evaluation of fluorescence and remission techniques for monitoring changes in peel chlorophyll and internal fruit characteristics in sunlit and shaded sides of apple fruit during shelf-life. Postharvest Biol. Technol. 48 (2), 231241. Kuckenberg, J., Tartachnyk, I., Noga, G., 2009. Temporal and spatial changes of chlorophyll fluorescence as a basis for early and precise detection of leaf rust and powdery mildew infections in wheat leaves. Precision Agric. 10 (1), 3444. Ku¨pper, H., Ku¨pper, F., Spiller, M., 1996. Environmental relevance of heavy metal-substituted chlorophylls using the example of water plants. J. Exp. Bot. 47 (2), 259266. Labate, C.A., Leegood, R.C., 1988. Limitation of photosynthesis by changes in temperature. Planta 173 (4), 519527. Lambers, H., Chapin, F.S., Pons, T.L., 1998. Plant Physiological Ecology. Springer, Dordrecht. Larré, C., Fernando, J., Marini, P., Bacarin, M., Peters, J., 2013. Growth and chlorophyll a fluorescence in Erythrina crista-galli L. plants under flooding conditions. Acta Physiol. Plant. 35 (5), 14631471. Lauer, M.J., Pallardy, S.G., Blevins, D.G., Randall, D.D., 1989. Whole leaf carbon exchange characteristics of phosphate deficient soybeans (Glycine max L.). Plant Physiol. 91 (3), 848854. Lauriano, J.A., Ramalho, J.C., Lidon, F.C., Céu matos, M., 2006. Mechanisms of energy dissipation in peanut under water stress. Photosynthetica 44 (3), 404410. Lazár, D., 2006. The polyphasic chlorophyll a fluorescence rise measured under high intensity of exciting light. Funct. Plant Biol. 33 (1), 930. Lazár, D., Jablonsky´, J., 2009. On the approaches applied in formulation of a kinetic model of photosystem II: different approaches lead to different simulations of the chlorophyl a fluorescence transients. J. Theor. Biol. 257 (2), 260269. Lichtenthaler, H.K., Rinderle, U., 1988. The role of chlorophyll fluorescence in the detection of stress conditions in plants. CRC Crit. Rev. Anal. Chem. 19 (1), 2985. Liu, W.-J., Chen, Y.-E., Tian, W.-J., Du, J.-B., Zhang, Z.-W., Xu, F., et al., 2009. Dephosphorylation of photosystem II proteins and phosphorylation of CP29 in barley photosynthetic membranes as a response to water stress. Biochim. Biophys. Acta 1787 (10), 12381245. Lu, C., Zhang, J., 1999. Effects of water stress on photosystem II photochemistry and its thermostability in wheat plants. J. Exp. Bot. 50 (336), 11991206. Mallick, N., Mohn, F., 2003. Use of chlorophyll fluorescence in metal-stress research: a case study with the green microalga Scenedesmus. Ecotoxicol. Environ. Saf. 55 (1), 6469. Marschner, H., 1995. Mineral Nutrition of Higher Plants. Academic Press, San Diego. Masclaux-Daubresse, C., Daniel-Vedele, F., Dechorgnat, J., Chardon, F., Gaufichon, L., Suzuki, A., 2010. Nitrogen uptake, assimilation and remobilization in plants: challenges for sustainable and productive agriculture. Ann. Bot. 105 (7), 11411157.

378


Mathur, S., Allakhverdiev, S.I., Jajoo, A., 2011. Analysis of high temperature stress on the dynamics of antenna size and reducing side heterogeneity of Photosystem II in wheat leaves (Triticum aestivum). Biochim. Biophys. Acta 1807 (1), 2229. Matorin, D., Ortoidze, T., Nikolaev, G., Venediktov, P., Rubin, A., 1982. Effects of dehydration on electron transport activity in chloroplasts [peas]. Photosynthetica 16 (2), 226233. Matyssek, R., Havranek, W.M., Wieser, G., Innes, J.L., 1997. Ozone and the forests in Austria and Switzerland. In: Sandermann, H., Wellburn, A., Heath, R. (Eds.), Forest Decline and Ozone, vol. 127. Ecological Studies. Springer, Berlin Heidelberg, pp. 95134. Maxwell, K., Johnson, G.N., 2000. Chlorophyll fluorescence—a practical guide. J. Exp. Bot. 51 (345), 659668. Medrano, H., Escalona, J., Bota, J., Gulias, J., Flexas, J., 2002. Regulation of photosynthesis of C3 plants in response to progressive drought: stomatal conductance as a reference parameter. Ann. Bot. 89 (7), 895905. Mehta, P., Allakhverdiev, S.I., Jajoo, A., 2010a. Characterization of photosystem II heterogeneity in response to high salt stress in wheat leaves (Triticum aestivum). Photosynth. Res. 105 (3), 249255. Mehta, P., Jajoo, A., Mathur, S., Bharti, S., 2010b. Chlorophyll a fluorescence study revealing effects of high salt stress on Photosystem II in wheat leaves. Plant Physiol. Biochem. 48 (1), 1620. Melis, A., 1985. Functional properties of Photosystem IIβ in spinach chloroplasts. Biochim. Biophys. Acta 808 (2), 334342. Melis, A., Homann, P.H., 1975. Kinetic analysis of the fluorescence induction in 3-(3, 4-dichlorophenyl)-1, 1-dimethylurea poisoned chloroplasts. Photochem. Photobiol. 21 (6), 431437. Melis, A., Homann, P.H., 1976. Heterogeneity of the photochemical centers in system II of chloroplasts. Photochem. Photobiol. 23, 343350. Merz, D., Geyer, M., Moss, D.A., Ache, H.-J., 1996. Chlorophyll fluorescence biosensor for the detection of herbicides. Fresenius J. Anal. Chem. 354 (3), 299305. Mishra, S., Dubey, R., 2005. Heavy metal toxicity induced alterations in photosynthetic metabolism in plants. In: Pessarakli, M. (Ed.), Handbook of Photosynthesis, vol. 28. CRC Press, Boca Raton, pp. 827844. Mohammed, G., Binder, W., Gillies, S., 1995. Chlorophyll fluorescence: a review of its practical forestry applications and instrumentation. Scand. J. For. Res. 10 (14), 383410. Molassiotis, A., Tanou, G., Diamantidis, G., Patakas, A., Therios, I., 2006. Effects of 4-month Fe deficiency exposure on Fe reduction mechanism, photosynthetic gas exchange, chlorophyll fluorescence and antioxidant defense in two peach rootstocks differing in Fe deficiency tolerance. J. Plant Physiol. 163 (2), 176185. Monteiro, J., Prado, C., 2006. Apparent carboxylation efficiency and relative stomatal and mesophyll limitations of photosynthesis in an evergreen cerrado species during water stress. Photosynthetica 44 (1), 3945. Morales, F., Abadıá, A., Belkhodja, R., Abadıá, J., 1994. Iron deficiency-induced changes in the photosynthetic pigment composition of field-grown pear (Pyrus communis L) leaves. Plant Cell Environ. 17 (10), 11531160. Morales, F., Moise, N., Quı´lez, R., Abadıá, A., Abadıá, J., Moya, I., 2001. Iron deficiency interrupts energy transfer from a disconnected part of the antenna to the rest of Photosystem II. Photosynth. Res. 70 (2), 207220. Moustakas, M., Lanaras, T., Symeonidis, L., Karataglis, S., 1994. Growth and some photosynthetic characteristics of field grown Avena sativa under copper and lead stress. Photosynthetica 30, 389396. Mullet, J.E., Whitsitt, M.S., 1996. Plant cellular responses to water deficits. Plant Growth Regulator 20, 119124. Munné-Bosch, S., Falara, V., Pateraki, I., Lo´pez-Carbonell, M., Cela, J., Kanellis, A.K., 2009. Physiological and molecular responses of the isoprenoid biosynthetic pathway in a drought-resistant Mediterranean shrub, Cistus creticus exposed to water deficit. J. Plant Physiol. 166 (2), 136145.

References

379

Murata, N., Mohanty, P., Hayashi, H., Papageorgiou, G., 1992. Glycine betaine stabilizes the association of extrinsic proteins with the photosynthetic oxygen-evolving complex. FEBS Lett. 296 (2), 187189. Murkowski, A., 2002. The Impact of Stress Factors in the Luminescence of Photosynthetic Apparatus of Chlorophyll in Plants. The Bohdan Dobrzański Institute of Agrophysics of the Polish Academy of Sciences, Lublin, Poland (in Polish). Musil, C., Van Heerden, P., Cilliers, C., Schmiedel, U., 2009. Mild experimental climate warming induces metabolic impairment and massive mortalities in southern African quartz field succulents. Environ. Exp. Bot. 66 (1), 7987. Nedbal, L., Trtilek, M., Kaftan, D., 1999. Flash fluorescence induction: a novel method to study regulation of photosystem II. J. Photochem. Photobiol. B, Biol. 48 (23), 154157. Nedbal, L., Soukupová, J., Whitmarsh, J., Trtı´lek, M., 2001. Postharvest imaging of chlorophyll fluorescence from lemons can be used to predict fruit quality. Photosynthetica 38 (4), 571579. Ohashi, Y., Nakayama, N., Saneoka, H., Fujita, K., 2006. Effects of drought stress on photosynthetic gas exchange, chlorophyll fluorescence and stem diameter of soybean plants. Biol. Plant. 50 (1), 138141. ¨ quist, G., Greer, D., O ¨ gren, E., 1987. Light stress at low temperature. In: Kyle, J., Osmond, C.B., Arntzen, O C.J. (Eds.), Photoinhibition. Elsevier, Amsterdam, pp. 6787. Osmond, C., 1994. What is photoinhibition? Some insights from comparisons of shade and sun plants. In: Baker, N.R., Bowyer, J.R. (Eds.), Photoinhibition of Photosynthesis: From Molecular Mechanisms to the Field. Bios Scientific Publishers, Oxford, UK, pp. 124. Oukarroum, A., El Madidi, S., Strasser, R.J., 2006. Drought stress induced in barley cultivars (Hordeurn vulgare L.) by polyethylene glycol, probed by germination, root length and chlorophyll a fluorescence rise (OJIP). Arch. Sci. 59 (1), 6574. Oukarroum, A., Madidi, S.E., Schansker, G., Strasser, R.J., 2007. Probing the responses of barley cultivars (Hordeum vulgare L.) by chlorophyll a fluorescence OLKJIP under drought stress and re-watering. Environ. Exp. Bot. 60 (3), 438446. Oukarroum, A., Schansker, G., Strasser, R.J., 2009. Drought stress effects on photosystem I content and photosystem II thermotolerance analyzed using Chl a fluorescence kinetics in barley varieties differing in their drought tolerance. Physiol. Plant. 137 (2), 188199. Oukarroum, A., El Madidi, S., Strasser, R., 2012. Exogenous glycine betaine and proline play a protective role in heat-stressed barley leaves (Hordeum vulgare L.): a chlorophyll a fluorescence study. Plant Biosyst. 146 (4), 10371043. Ouzounidou, G., Moustakas, M., Strasser, R.J., 1997. Sites of action of copper in the photosynthetic apparatus of maize leaves: kinetic analysis of chlorophyll fluorescence, oxygen evolution, absorption changes and thermal dissipation as monitored by photoacoustic signals. Funct. Plant Biol. 24 (1), 8190. Paknejad, F., Nasri, M., Moghadam, H.R.T., Zahedi, H., Alahmadi, M.J., 2007. Effects of drought stress on chlorophyll fluorescence parameters, chlorophyll content and grain yield of wheat cultivars. J. Biol. Sci. 7, 841847. Pál, M., Horváth, E., Janda, T., Páldi, E., Szalai, G., 2006. Physiological changes and defense mechanisms induced by cadmium stress in maize. J. Plant Nutr. Soil Sci. 169 (2), 239246. Papageorgiou, G.C., Govindjee, 2004. Chlorophyll a Fluorescence: A signature of Photosynthesis. Springer, Dordrecht. Papageorgiou, G.C., Govindjee, 2011. Photosystem II fluorescence: slow changes—Scaling from the past. J. Photochem. Photobiol. B, Biol. 104 (12), 258270. Peeva, V., Cornic, G., 2009. Leaf photosynthesis of Haberlea rhodopensis before and during drought. Environ. Exp. Bot. 65 (23), 310318. Percival, G.C., Keary, I.P., AI-Habsi, S., 2006. An assessment of the drought tolerance of Fraxinus genotypes for urban landscape plantings. Urban For. Urban Greening 5 (1), 1727.

380


Pereira, E.G., Oliva, M.A., Kuki, K.N., Cambraia, J., 2009. Photosynthetic changes and oxidative stress caused by iron ore dust deposition in the tropical CAM tree Clusia hilariana. Trees 23 (2), 277285. Pompelli, M.F., Martins, S.C., Antunes, W.C., Chaves, A.R., DaMatta, F.M., 2010. Photosynthesis and photoprotection in coffee leaves is affected by nitrogen and light availabilities in winter conditions. J. Plant Physiol. 167 (13), 10521060. Prasil, O., Adir, N., Ohad, I., 1992. Dynamics of photosystem II: mechanism of photoinhibition and recovery process. Top. Photosyn. 11, 295348. Qiu, Z., Wang, L., Zhou, Q., 2013. Effects of bisphenol A on growth, photosynthesis and chlorophyll fluorescence in above-ground organs of soybean seedlings. Chemosphere 90, 12741280. Rampino, P., Pataleo, S., Gerardi, C., Mita, G., Perrotta, C., 2006. Drought stress response in wheat: physiological and molecular analysis of resistant and sensitive genotypes. Plant Cell Environ. 29 (12), 21432152. Rao, I.M., Fredeen, A.L., Terry, N., 1990. Leaf phosphate status, photosynthesis, and carbon partitioning in sugar beet III. Diurnal changes in carbon partitioning and carbon export. Plant Physiol. 92 (1), 2936. Redondo-Go´mez, S., Mateos-Naranjo, E., Figueroa, M., 2009. Synergic effect of salinity and light-chilling on photosystem II photochemistry of the halophyte, Sarcocornia fruticosa. J. Arid Environ. 73 (4), 586589. Ripley, B.S., Redfern, S.P., Dames, J., 2004. Quantification of the photosynthetic performance of phosphorusdeficient sorghum by means of chlorophyll-a fluorescence kinetics. S. Afr. J. Sci. 100 (11 & 12), 615618. Robinson, M.F., Heath, J., Mansfield, T.A., 1998. Disturbances in stomatal behaviour caused by air pollutants. J. Exp. Bot. 49, 461469 (special issue). Roger, M.J.R., Weiss, O., 2003. Fluorescence techniques. Handbook of Plant Ecophysiology Techniques. Springer, pp. 155171. Romanowska, E., Igamberdiev, A.U., Parys, E., Gardestro¨m, P., 2002. Stimulation of respiration by Pb21 in detached leaves and mitochondria of C3 and C4 plants. Physiol. Plant. 116 (2), 148154. Romanowska, E., Wro´blewska, B., Dro˙zak, A., Siedlecka, M., 2006. High light intensity protects photosynthetic apparatus of pea plants against exposure to lead. Plant Physiol. 44 (5), 387394. Romanowska-Duda, B., Kalaji, M., Strasser, R., 2005. The use of PSII activity of Spirodela oligorrhiza plants as an indicator for water toxicity. Photosynthesis: Fundamental Aspects to Global Perspectives. Allen Press, Lawrence, pp. 585587. Roshchina, V., Melnikova, E., 1996. Microspectrofluorometry: a new technique to study pollen allelopathy. Allelopathy J. 3 (1), 5158. Ruban, A., Horton, P., 1995. Regulation of non-photochemical quenching of chlorophyll fluorescence in plants. Funct. Plant Biol. 22 (2), 221230. Rykaczewska, K., Pietkiewicz, S., Kalaji, M.H., Kotlarska-Jaros, E., Piotrowska, W., 2004. Comparative analysis of growth, yield and photosynthetic efficiency of plants of two very early potato cultivars: Ruta and Karatop Part. II. Analysis using measuring equipment. Zesz. Probl. Post. Nauk Rol. 500, 181191. Savitch, L.V., Gray, G.R., Huner, N.P., 1997. Feedback-limited photosynthesis and regulation of sucrosestarch accumulation during cold acclimation and low-temperature stress in a spring and winter wheat. Planta 201 (1), 1826. Sayed, O., 2003. Chlorophyll fluorescence as a tool in cereal crop research. Photosynthetica 41 (3), 321330. Schansker, G., Srivastava, A., Govindjee, Strasser, R.J., 2003. Characterization of the 820-nm transmission signal paralleling the chlorophyll a fluorescence rise (OJIP) in pea leaves. Funct. Plant Biol. 30 (7), 785796. Schraudner, M., Langebartels, C., Sandermann, H., 1997. Changes in the biochemical status of plant cells induced by the environmental pollutant ozone. Physiol. Plant. 100 (2), 274280.

References

381

Schreiber, U., Neubauer, C., Klughammer, C., 1989. Devices and methods for room-temperature fluorescence analysis. Philos. Trans. R. Soc. Lond., B, Biol. Sci. 323 (1216), 241251. Schreiber, U., Bilger, W., Neubauer, C., 1994. Chlorophyll fluorescence as a nonintrusive indicator for rapid assessment of in vivo photosynthesis. Ecophysiology of Photosynthesis. Springer, pp. 4970. Schreiber, U., Klughammer, C., Kolbowski, J., 2012. Assessment of wavelength-dependent parameters of photosynthetic electron transport with a new type of multi-color PAM chlorophyll fluorometer. Photosynth. Res. 113 (13), 127144. Schuler, L.J., Rand, G.M., 2008. Aquatic risk assessment of herbicides in freshwater ecosystems of South Florida. Arch. Environ. Contam. Toxicol. 54 (4), 571583. Schweiger, J., Lang, M., Lichtenthaler, H.K., 1996. Differences in fluorescence excitation spectra of leaves between stressed and non-stressed plants. J. Plant Physiol. 148 (5), 536547. Scott, B., Robson, A., 1990a. Changes in the content and form of magnesium in the first trifoliate leaf of subterranean clover under altered or constant root supply. Crop Pasture Sci. 41 (3), 511519. Scott, B., Robson, A., 1990b. Distribution of magnesium in subterranean clover (Trifolium subterraneum L.) in relation to supply. Crop Pasture Sci. 41 (3), 499510. Sharkey, T.D., Schrader, S.M., 2006. High temperature stress. Physiology and Molecular Biology of Stress Tolerance in Plants. Springer, Dordrecht, pp. 101129. Sharma, D., Swarup, A., 1988. Effects of short-term flooding on growth, yield and mineral composition of wheat on sodic soil under field conditions. Plant Soil 107 (1), 137143. Sharma, P., Dubey, R.S., 2005. Lead toxicity in plants. Braz. J. Plant Physiol. 17, 3552. Shcolnick, S., Keren, N., 2006. Metal homeostasis in cyanobacteria and chloroplasts. Balancing benefits and risks to the photosynthetic apparatus. Plant Physiol. 141 (3), 805810. Sigfridsson, K.G., Bernát, G., Mamedov, F., Styring, S., 2004. Molecular interference of Cd21 with Photosystem II. Biochim. Biophys. Acta 1659 (1), 1931. Silva, E.N., Ferreira-Silva, S.L., Fontenele, A.d.V., Ribeiro, R.V., Viégas, R.A., Silveira, J.A.G., 2010. Photosynthetic changes and protective mechanisms against oxidative damage subjected to isolated and combined drought and heat stresses in Jatropha curcas plants. J. Plant Physiol. 167 (14), 11571164. Smethurst, C.F., Garnett, T., Shabala, S., 2005. Nutritional and chlorophyll fluorescence responses of lucerne (Medicago sativa) to waterlogging and subsequent recovery. Plant Soil 270 (1), 3145. Sofo, A., Dichio, B., Montanaro, G., Xiloyannis, C., 2009. Photosynthetic performance and light response of two olive cultivars under different water and light regimes. Photosynthetica 47 (4), 602608. Souza, R.P., Machado, E.C., Silva, J.A.B., Lagoâ, A.M.M.A., Silveira, J.A.G., 2004. Photosynthetic gas exchange, chlorophyll fluorescence and some associated metabolic changes in cowpea (Vigna unguiculata) during water stress and recovery. Environ. Exp. Bot. 51 (1), 4556. Srivastava, A., Strasser, R.J., 1995. How do land plants respond to stress temperature and stress light? Arch. Sci. Geneve 48, 135146. Srivastava, A., Strasser, R.J., Govindjee, 1999. Greening of peas: parallel measurements of 77 K emission spectra, OJIP chlorophyll a fluorescence transient, period four oscillation of the initial fluorescence level, delayed light emission, and P700. Photosynthetica 37, 365392. Stefanov, D., Petkova, V., Denev, I.D., 2011. Screening for heat tolerance in common bean (Phaseolus vulgaris L.) lines and cultivars using JIP-test. Sci. Hortic. 128 (1), 16. Stirbet, A., 2013. Excitonic connectivity between photosystem II units: what is it, and how to measure it? Photosynth. Res. 126. Stirbet, A., Govindjee, 2011. On the relation between the Kautsky effect (chlorophyll a fluorescence induction) and Photosystem II: basics and applications of the OJIP fluorescence transient. J. Photochem. Photobiol. B 104 (12), 236257.

382


Stirbet, A., Govindjee, 2012. Chlorophyll a fluorescence induction: a personal perspective of the thermal phase, the J-I-P rise. Photosynth. Res. 113, 1561. Strasser, B.J., 1997. Donor side capacity of photosystem II probed by chlorophyll a fluorescence transients. Photosynth. Res. 52, 147155. Strasser, R.J., 1978. The grouping model of plant photosynthesis. In: Akoyunoglou, G. (Ed.), Chloroplast Development. Elsevier, North Holland, pp. 513524. Strasser, R.J., Stirbet, A.D., 1998. Heterogeneity of photosystem II probed by the numerically simulated chlorophyll a fluorescence rise (O-J-I-P). Math. Comput. Simul. 48 (1), 39. Strasser, R.J., Srivastava, A., Tsimilli-Michael, M., 2000. The fluorescence transient as a tool to characterize and screen photosynthetic samples. In: Younis, M., Pathre, U., Mohanty, P. (Eds.), Probing Photosynthesis: Mechanism, Regulation and Adaptation. Taylor and Francis, London, pp. 443480. Strasser, R.J., Tsimilli-Michael, M., Srivastava, A., 2004. Analysis of the chlorophyll a fluorescence transient. In: Papageorgiou, G., Govindjee (Eds.), Advances in Photosynthesis and Respiration. Chlorophyll a Fluorescence: A Signature of Photosynthesis. Springer, Dordrecht, The Netherlands, pp. 321362. Strasser, R.J., Tsimilli-Michael, M., Dangre, D., Rai, M., 2007. Biophysical phenomics reveals functional building blocks of plants systems biology: a case study for the evaluation of the impact of mycorrhization with Piriformospora indica. Advanced Techniques in Soil Microbiology. Dordrecht, Springer, pp. 319341. Strasser, R.J., Tsimilli-Michael, M., Qiang, S., Goltsev, V., 2010. Simultaneous in vivo recording of prompt and delayed fluorescence and 820-nm reflection changes during drying and after rehydration of the resurrection plant Haberlea rhodopensis. Biochim. Biophys. Acta 1797, 13131326. Strauss, A., Kru¨ger, G., Strasser, R., Heerden, P.V., 2006. Ranking of dark chilling tolerance in soybean genotypes probed by the chlorophyll a fluorescence transient OJIP. Environ. Exp. Bot. 56 (2), 147157. Streb, P., Aubert, S., Gout, E., Feierabend, J., Bligny, R., 2008. Cross tolerance to heavy-metal and coldinduced photoinhibiton in leaves of Pisum sativum acclimated to low temperature. Physiol. Mol. Biol. Plants 14 (3), 185193. Strehler, B.L., Arnold, W.A., 1951. Light production by green plants. J. Gen. Physiol. 34, 809820. Suggett, D.J., Praâésil, O., Borowitzka, M.A., 2011. Chlorophyll a Fluorescence in Aquatic Sciences: Methods and Applications. Springer, Dordrecht. Takahashi, S., Bauwe, H., Badger, M., 2007. Impairment of the photorespiratory pathway accelerates photoinhibition of photosystem II by suppression of repair but not acceleration of damage processes in Arabidopsis. Plant Physiol. 144 (1), 487494. Tomar, R.S., Jajoo, A., 2013. A quick investigation of the detrimental effects of environmental pollutant polycyclic aromatic hydrocarbon fluoranthene on the photosynthetic efficiency of wheat (Triticum aestivum). Ecotoxicology 22 (8), 13131318. Tongra, T., Mehta, P., Mathur, S., Agrawal, D., Bharti, S., Los, D.A., Allakhverdiev, S.I., Jajoo, A., 2011. Computational analysis of fluorescence induction curves in intact spinach leaves treated at different pH. Biosystems 103 (2), 158163. Tsimilli-Michael, M., Strasser, R.J., 2008. In vivo assessment of stress impact on plants’ vitality: applications in detecting and evaluating the beneficial role of Mycorrhization on host plants. In: Varma, A. (Ed.), Mycorrhiza: State of the Art, Genetics and Molecular Biology, Eco-Function, Biotechnology, EcoPhysiology, Structure and Systematics, vol. 3, Springer, pp. 679703. Tuba, Z., Saxena, D.K., Srivastava, K., Singh, S., Czebol, S., Kalaji, M.H., 2010. Chlorophyll a fluorescence measurements for validating the tolerant bryophytes for heavy metal (Pb) biomapping. Curr. Sci. 98 (11), 15051508. Van der Tol, C., Verhoef, W., Rosema, A., 2009. A model for chlorophyll fluorescence and photosynthesis at leaf scale. Agric. For. Meteorol. 149 (1), 96105.

References

383

Van Heerden, P.D.R., Swanepoel, J.W., Kru¨ger, G.H.J., 2007. Modulation of photosynthesis by drought in two desert scrub species exhibiting C3-mode CO2 assimilation. Environ. Exp. Bot. 61 (2), 124136. Van Rensburg, L., Kru¨ger, G., 1993. Differential inhibition of photosynthesis (in vivo and in vitro), and changes in chlorophyll a fluorescence induction kinetics of four tobacco cultivars under drought stress. J. Plant Physiol. 141 (3), 357365. Van Rensburg, L., Kruger, G., Eggenberg, P., Strasser, R., 1996. Can screening criteria for drought resistance in Nicotiana tabacum L be derived from the polyphasic rise of the chlorophyll a fluorescence transient (OJIP)? S. Afr. J. Bot. 62 (6), 337341. Wierzbicka, M., 1999. Comparison of lead tolerance in Allium cepa with other plant species. Environ. Pollut. 104 (1), 4152. Wright, H., DeLong, J., Lada, R., Prange, R., 2009. The relationship between water status and chlorophyll a fluorescence in grapes (Vitis spp.). Postharvest Biol. Technol. 51 (2), 193199. Wrochna, M., Gawrońska, H., Borkowska, B., Gawroński, S.W., 2007. The effect of salinity on the accumulation of biomass and chlorophyll fluorescence in plants of three varieties of ornamental amaranth Rocz AR Pozn CCCLXXXIII. Horticulture 41, 235239 (in Polish). Wu, C., Wang, Z., Sun, H., Guo, S., 2006. Effects of different concentrations of nitrogen and phosphorus on chlorophyll biosynthesis, chlorophyll a fluorescence, and photosynthesis in Larix olgensis seedlings. Front. For. China 1 (2), 170175. Wu, X., Hong, F., Liu, C., Su, M., Zheng, L., Gao, F., Yang, F., 2008. Effects of Pb21 on energy distribution and photochemical activity of spinach chloroplast. Spectrochim. Acta A Mol. Biomol. Spectrosc. 69 (3), 738742. Yamane, Y., Kashino, Y., Koike, H., Satoh, K., 1997. Increases in the fluorescence Fo level and reversible inhibition of Photosystem II reaction center by high-temperature treatments in higher plants. Photosynth. Res. 52, 5764. Yamane, Y., Kashino, Y., Koike, H., Satoh, K., 1998. Effects of high temperatures on the photosynthetic systems in spinach: oxygen-evolving activities, fluorescence characteristics and the denaturation process. Photosynth. Res. 57, 5159. Yang, J., Kong, Q., Xiang, C., 2009. Effects of low night temperature on pigments, chl a fluorescence and energy allocation in two bitter gourd (Momordica charantia L.) genotypes. Acta Physiol. Plant. 31 (2), 285293. Yang, X., Liang, Z., Wen, X., Lu, C., 2008. Genetic engineering of the biosynthesis of glycine betaine leads to increased tolerance of photosynthesis to salt stress in transgenic tobacco plants. Plant Mol. Biol. 66 (12), 7386. Yin, C., Berninger, F., Li, C., 2006. Photosynthetic responses of Populus przewalski subjected to drought stress. Photosynthetica 44 (1), 6268. Yordanov, I., Dilova, S., Petkova, R., Pangelova, T., Goltsev, V., Zuss, K.H., 1986. Mechanisms of the temperature damage and acclimation of the photosynthetic apparatus. Photobiochem. Photobiophys. 12, 147155. Yordanov, I., Tsonev, T., Goltsev, V., Kruleva, L., Velikova, V., 1997. Interactive effect of water deficit and high temperature on photosynthesis of sunflower and maize plants. 1. Changes in parameters of chlorophyll fluorescence induction kinetics and fluorescence quenching. Photosynthetica 33 (3-4), 391402. Yu, C.-W., Murphy, T.M., Sung, W.-W., Lin, C.-H., 2002. H2O2 treatment induces glutathione accumulation and chilling tolerance in mung bean. Funct. Plant Biol. 29 (9), 10811087. Zaharieva, I., Taneva, S.G., Goltsev, V., 2001. Effect of temperature on the luminescent characteristics in leaves of Arabidopsis mutants with decreased unsaturation of the membrane lipids. Bulg J. Plant Physiol. 27, 319. Zahedi, H., Alahrnadi, S.J., 2007. Effects of drought stress on chlorophyll fluorescence parameters, chlorophyll content and grain yield of wheat cultivars. J. Biol. Sci. 7 (6), 841847.

384


Zhang, R., Sharkey, T.D., 2009. Photosynthetic electron transport and proton flux under moderate heat stress. Photosynth. Res. 100 (1), 2943. Zheng, C., Jiang, D., Liu, F., Dai, T., Jing, Q., Cao, W., 2009. Effects of salt and waterlogging stresses and their combination on leaf photosynthesis, chloroplast ATP synthesis, and antioxidant capacity in wheat. Plant Sci. 176 (4), 575582. Zhou, Y., Lam, H.M., Zhang, J., 2007. Inhibition of photosynthesis and energy dissipation induced by water and high light stresses in rice. J. Exp. Bot. 58 (5), 12071217. Zivcak, M., Brestic, M., Olsovska, K., 2008a. Application of photosynthetic parameters in screening of wheat (Triticum aestivum L.) genotypes for imroved drought and high temperature tolerance. In: Allen, J.F., Gantt, E., Goldbeck, J.H., Osmond, B. (Eds.), Photosynthesis. Energy from the Sun: 14th International Congress on Photosynthesis. Springer, Dordrecht. Zivcak, M., Brestic, M., Olsovska, K., Slamka, P., 2008b. Performance Index as a sensitive indicator of water stress in Triticum aestivum. Plant Soil Environ. 54, 133139. Zivcak, M., Brestic, M., Olsovska, K., 2008c. Physiological parameters useful in screening for improved tolerance to drought in winter wheat (Triticum aestivum L.). Cereal Res. Commun. 36, 19431946. Zivcak, M., Olsovska, K., Brestic, M., Slabbert, M.M., 2013a. Critical temperature derived from the selected chlorophyll a fluorescence parameters of indigenous vegetable species of South Africa treated with high temperature. Photosynthesis Research for Food, Fuel and the Future. Springer, Berlin Heidelberg, pp. 628632. Zivcak, M., Brestic, M., Balatova, Z., Drevenakova, P., Olsovska, K., Kalaji, H.M., et al., 2013b. Photosynthetic electron transport and specific photoprotective responses in wheat leaves under drought stress. Photosynth. Res. 117, 529546. Zribi, L., Fatma, G., Fatma, R., Salwa, R., Hassan, N., Néjib, R.M., 2009. Application of chlorophyll fluorescence for the diagnosis of salt stress in tomato Solanum lycopersicum (variety Rio Grande). Sci. Hortic. 120 (3), 367372. Zushi, K., Kajiwara, S., Matsuzoe, N., 2012. Chlorophyll a fluorescence OJIP transient as a tool to characterize and evaluate response to heat and chilling stress in tomato leaf and fruit. Sci. Hortic. 148, 3946.

CHAPTER

Manipulating Osmolytes for Breeding Salinity-Tolerant Plants

16

Noushina Iqbal, Shahid Umar and Rahat Nazar

16.1 Introduction Salinity is among the important abiotic stresses that negatively affects plant growth and productivity. According to the Food and Agriculture Organization (FAO), in 2008 more than 6% of world’s total land area (800 million ha) was affected by salt. Salinity of soil is increasing on a global scale and currently affects more than 10% of arable land, which results in a decline of greater than 50% of the major crops’ average yield (Wang et al., 2009). Salinity affects almost every aspect of plant physiology at both the whole plant and cellular level through osmotic stress in an early phase and ionic stress at later stage of growth (Munns and Tester, 2008). The physiological processes affected by salinity include ionic toxicity, osmotic stress, nutrient deficiency, and oxidative stress (Munns and Tester, 2008; Daneshmand et al., 2009). It leads to the production of reactive oxygen species (ROS) (Nazar et al., 2011; Khan et al., 2012), which causes lipid peroxidation, DNA damage, inhibition of photosynthesis, and disturbance in mineral nutrient status (Greenway and Munns, 1980; Nazar et al., 2011; Turan and Tripathy, 2012). Salinity adversely affects antioxidant phenomena, nitrogen metabolism, proline (Pro) metabolism, and osmolyte accumulation (Misra and Gupta, 2005). Extensive studies have resulted in a number of strategies for salt tolerance. Parida and Das (2005) reported that plants’ ability to tolerate osmotic stress depends on multiple biochemical pathways that facilitate retention and/or acquisition of water, protect chloroplast functions, and maintain ion homeostasis. Among the various pathways involved in maintaining cellular homeostasis, the synthesis of osmotically active metabolites plays an important role. Many plant species respond rapidly to stressors by increasing the concentration of osmolytes involved in osmoregulation and in protection of proteins and membranes in conditions of low water potential (Munns and Tester, 2008). Osmolytes (e.g., Pro, valine, isoleucine, ectoine, aspartic acid, betaine, glucose, fructose, sucrose, fructans, mannitol, pinitol, and myo-inositol) accumulate in the cytoplasm of their cells under salt stress (Parida and Das, 2005). These osmolytes do not interfere with normal biochemical reactions and help retain ionic balance (Zhifang and Loescher, 2003). They maintain osmotic balance and support continued water influx (Hasegawa et al., 2000). The organic solutes have been proved to be helpful in osmoregulation (Rhodes and Hanson, 1993), enzyme activity (Mansour, 2000), detoxification of ROS (Ashraf, 1994), and protection of membrane integrity (Bohnert and Jensen, 1996).


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CHAPTER 16 Manipulating Osmolytes for Breeding Salinity-Tolerant Plants

The development of salt-tolerant plants via manipulation of osmolytes represents an alternative approach for cultivation of salinity-prone land. Salinity-tolerant plants would show enhanced growth and productivity even in an unsuitable area.

16.2 Salinity-induced ionic and osmotic stress and tolerance mechanisms The adverse effects of salinity on plant growth may be due to ion cytotoxicity and osmotic stress (Hussain et al., 2008). High salinity affects plants in several ways: water stress, ion toxicity, nutritional disorders, oxidative stress, alteration of metabolic processes, membrane disorganization, reduction of cell division and expansion, and genotoxicity (Hasegawa et al., 2000; Munns, 2002, Zhu, 2007). Together, these effects reduce plant growth, development, and survival. A primary response in salt-stressed plants is a decrease in their water potential, resulting in decreased wateruse efficiency (WUE) and overall toxic damages and yield reduction (Chaum and Kirdmanee, 2009). The osmotic effects of salinity stress result in inhibited cell expansion and division, as well as stomatal closure; this can be observed immediately after salt application and is believed to continue for the duration of exposure (Munns, 2002; Flowers, 2004). During long-term exposure to salinity, plants experience ionic stress, which can lead to premature senescence of adult leaves, and thus a reduction in the photosynthetic area available to support continued growth (Cramer and Nowak, 1992). Salt stress involves both osmotic and ionic stress (Hayashi and Murata, 1998). To alleviate the adverse effects of salinity stress, various approaches have been used. The aim is to develop salinity-tolerant crops; however, progress in breeding for salinity tolerance has been slow due to limited knowledge of the genetics of salt tolerance, involvement of several complex tolerance mechanisms, low selection efficiency, and an insufficient understanding of stress and environmental interactions (Gregorio et al., 2002). Further, the management of salinity stress has been considered difficult because of its multigenic and quantitative nature (Nazar et al., 2011). Salinity stress leads to both ionic and osmotic stress. To counteract ionic stress, the salt overly sensitive (SOS) pathway is activated to transport ions and maintain ionic homeostasis, whereas osmotic stress is reduced by maintaining osmotic homeostasis through osmolytes by activating MAPK cascades. In plants the SOS signal-transduction pathway has been studied extensively and is important for the maintenance of ion homeostasis and salt tolerance (Zhu, 2003). A diagrammatic representation of the mechanism of salt tolerance is shown in Figure 16.1. Activation of the SOS-signaling pathway has long been recognized as a key mechanism for Na1 exclusion and ion homeostasis control at the cellular level (Zhu, 2000). SOS1 is located in plasma membrane responsible for extrusion of Na1 out of the cell, while the calcium-activated SOS3SOS2 protein complex is involved in inhibiting HKT1, a low-affinity potassium transporter that transports the Na1 ion under high-salt conditions located in cytosol (Mahajan et al., 2008). The SOS2 and SOS3 genes encode a protein kinase and a Ca21-binding protein, respectively (Liu and Zhu, 1998; Halfter et al., 2000). They are later grouped into large protein families of calcineurin B-like proteins (CBL) and CBL-interacting protein kinases (CIPK); therefore, SOS2 and SOS3 are also known as CIPK24 and CBL4, respectively (Kolukisaoglu et al., 2004). The role of Ca21 in salinity tolerance via activation of the SOS pathway has been reported. After perception of salt

16.2 Salinity-induced ionic and osmotic stress and tolerance mechanisms

387

Salinity stress

Ionic stress

SOS pathway

Osmotic stress

MAPK cascades

Ca2+ spike activates SO3-SO2 Induction of osmolyte synthesis Recruit SO2 to plasma membrane

Activation of SO1 Osmotic adjustment

Na+ exclusion (Ionic adjustment)

Salinity tolerance

FIGURE 16.1 Diagrammatic representation of the salt-tolerance mechanism in plants.

stress, a Ca21 spike generated in cytoplasm of root cells activates the SOS signal-transduction cascade to protect cells from damage due to excessive ion accumulation (Halfter et al., 2000; Zhu, 2002; Guo et al., 2004; Chinnusamy et al., 2005). SOS3SOS2, or SCaBP8 (SOS3-like calciumbinding protein 8, also known as calcineurin B-like CBL10) and SOS2 interactions recruit SOS2 to the plasma membrane leading to activation of the downstream target SOS1, a Na1/H1 antiporter. This causes subsequent extrusion of excessive Na1 from the cytosol (Quintero et al., 2002, 2011; Quan et al., 2007). Osmotic homeostasis and stress damage control appear to be regulated by salt stress-induced ABA, ROS, a putative osmosensory histidine kinase (AtHK1), and MAPK cascades. A signaling cascade similar to that of the yeast mitogen-activated protein kinase-high-osmolarity glycerol 1 (MAPK-HOG1) pathway may regulate osmolyte biosynthesis (Zhu, 2002). Inactivation of ATHK1

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under high osmolarity may result in the accumulation of a nonphosphorylated active form of the response regulator, which then stimulates osmolyte biosynthesis in plants by activating an MAPK pathway(s) (Urao et al., 1999). MAPK-based signaling plays a positive role in stress-induced Pro accumulation (Kong et al., 2011; Zhang et al., 2011). Among the various strategies to develop salinity-tolerant plants, manipulation of osmolytes plays an important role. When plants are exposed to stress conditions, metabolic shifts occur and result in changes in the levels of various cellular metabolites. Guy (1990) reported that metabolites, such as soluble sugars, amino acids, organic acids, polyamines, and lipids, may contribute to salt tolerance. One important group of such metabolites is the so-called “compatible solutes,” which are small organic metabolites that are very soluble in water and are nontoxic at high concentrations. The present review focuses on the importance of these osmolytes in salinity tolerance.

16.3 General description of osmolytes Osmolytes are divided into two categories: inorganic and organic. Osmotic adjustment for growth in a saline environment may be accomplished by accumulation of inorganic and organic solutes. Inorganic ions are believed to be sequestered in the vacuoles to decrease cell water potential. The energy consumption from absorbing inorganic ions is far less than from synthesizing organic compounds (Munns, 2002). Sometimes, even though inorganic salts are potentially harmful (Collins, 2006), such salts are used as osmolytes (Galinski, 1995) or for osmotic control in vivo (Miyakawa et al., 1999; Ferraris et al., 2002). The reduction of growth induced by salinity is probably associated with the toxic effect of the accumulation of Na1 and Cl2 in plant tissues and the reduction of absorption of K1 and Ca21. A high Na1 concentration interferes with intracellular K1 and Ca21 accumulation presumably by competing for the same sites of influx (Tester and Davenport, 2003). Therefore, the key for tolerance may be synchronization between the high rate of ion transport to the shoot and ion compartmentation by the leaf cells (Munns et al., 2006). Organic solutes are assumed to be compartmentalized in the cytoplasm to balance the low osmotic potential in the vacuole (Munns and Tester, 2008). Inorganic osmolytes mainly include K, Na, Ca, Mg, and Cl (Furtana et al., 2013) and, although low cost, bring ionic toxicity when plants accumulate excess inorganic ions especially at a high concentration of Na and Cl (Martıńez et al., 2003; Ottow et al., 2005; Touchette, 2007). Thus, plants also accumulate organic osmolytes that are nontoxic even at high concentrations and are called compatible osmolytes; they contribute to a decrease in the cytoplasmic water potential. In addition to the role in osmotic adjustments, compatible solutes seem to function as a chaperone that protects enzymes and membrane structures, and as a scavenger reduces radical oxygen species under stress conditions including salinity (Bohnert and Shen, 1999). However, massive accumulation of organic solutes will cause loss of energy and carbon substances essential for plant growth and other metabolic activities (Sonnewald, 2001). To maintain osmotic adjustment and loss of energy and carbon substances, plants accumulate these organic solutes in cytoplasm, whereas inorganic osmolytes are sequestrated into vacuoles or cytoplasm (Munns and Tester, 2008).

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High salinity leads to an osmotic flux of water out of the cell thereby increasing the concentration of cellular constituents including inorganic salts (Burg et al., 2007). To maintain osmotic balance, cells restore their volume by influx of inorganic salts followed by osmotic uptake of water. Organic osmolytes accumulated later are associated with a decreasing concentration of intracellular inorganic salts. Thus, perturbing inorganic ions are replaced by compatible osmolytes (Burg and Ferraris, 2008). Compatible solute accumulation as a response to osmotic stress is a ubiquitous process in organisms from bacteria to plants and animals (Hussain et al., 2010). Naturally occurring organic osmolytes can be grouped into three classes: polyols, amino acids, and combinations of methylamines with urea (Yancey et al., 1982; Hochachka and Somero, 2002). Proline, soluble sugars, sugar alcohols, and glycinebetaine (GB) have received much attention because of their role in osmotic adjustment (Hare et al., 1998; Hasegawa et al., 2000). Increased sugar concentration under salinity stress has been reported (Dubey and Singh, 1999; Muscolo et al., 2003). Carbohydrates (e.g., raffinose or stachyose) act as an osmolyte and have been implicated in salt or osmotic stress tolerance (Gupta et al., 1993; Obendorf, 1997; Liu et al., 1998a,b; Minorsky, 2003). The accumulation of organic solutes (soluble and insoluble carbohydrates) plays an important role in increasing the internal osmotic pressure under salinity stress (Zidan and Al-Zahrani, 1994). Polyols also play an important role in the response to abiotic stress, compensating for the reduced cell water potential (Popp and Smirnoff, 1995) and as oxygen radical scavengers (Ashraf and Harris, 2004). Their hydroxyl groups may effectively replace water to establish hydrogen bonds in cases of cellular dehydration, thus helping to maintain enzyme activities and to protect membrane structures (Noiraud et al., 2001). Nature prefers organic osmolytes to inorganic osmolytes. Nearly all organisms use organic rather than inorganic solutes to protect their cells against adverse conditions. The only exceptions are certain Archea that use salt (Hochachka and Somero, 2002). Compatible osmolytes do not interfere with normal biochemical reactions and act as osmoprotectants during osmotic stress. Generally, organic osmolytes interact primarily with the peptide backbone (Bolen and Baskakov, 2001) because it is common to all proteins and is the most abundant chemical entity in the macromolecules (Harries and Ro¨sgen, 2008). Salts, however, exert predictable effects only at high concentrations. Organic osmolytes are talked about mostly in relation to maintaining osmotic adjustments under stress conditions. Ashraf and Harris (2004) studied the detection and quantification of osmolytelike nitrogenous compounds, such as Pro or GB, which play an adaptive role in mediating stressed plants’ osmotic adjustment and protecting subcellular structures. In fact, Pro and GB behave as almost omnipresent solutes, and it appears the species that are Pro accumulators show low levels of GB, and vice versa (Briens and Larher, 1982; Tipirdamaz et al., 2006). Further, in plants exposed to salinity stress, accumulation of compatible solutes—including Pro, GB, soluble sugars, and sugar alcohols—has received much attention in terms of their function in osmotic adjustment (Hare et al., 1998; Hasegawa et al., 2000). In the present chapter, therefore, organic osmolytes are discussed in particular; the most talked about among them are GB, Pro, and sugars.

16.4 The role of inorganic osmolytes in salinity tolerance Accumulation of inorganic ions is a basic mechanism to adjust the internal tissues for osmotic potential against salinity; however, they differ widely in the extent to which they

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accumulate inorganic ions (Glenn et al., 1996). Munns and Tester (2008) suggested that inorganic solutes are involved in osmotic adjustment. They reported that the presence of high concentrations of Na1 and Cl2 in the nutrient solution produced a high uptake of these ions, contributed to their increased flux into the xylem, and are thus involved in osmotic adjustment. Studies have shown that Na1, K1, and Cl2 accumulate to achieve osmotic adjustment by lowering solute potential and water potential in plant tissues of some halophytes (Yasseen and Abu-Al-Basal, 2008). Under salinity stress, high accumulation of toxic ions (e.g., Na1 and Cl2) takes place (Munns et al., 2006); this disturbs K1 uptake thereby resulting in a reduced K1/Na1 ratio (Graifenberg et al., 1995). A lower K1/Na1 ratio is an index of toxicity because Na1 impairs the activity of the K1-requiring enzyme and therefore affects growth and development (Chaparzadeh et al., 2003). Nazar et al. (2011) reported that the salt-sensitive cultivar of mungbean accumulated higher Na1 and Cl2 content than the salt-tolerant cultivar. The K1 ion plays a central role in osmotic adjustment, maintenance of turgor, and in stomatal opening of plants under stress (Maathuis and Amtmann, 1999). A high K1/Na1 ratio in plants under saline conditions has been suggested as an important selection criterion for salt tolerance (Reynolds et al., 2005). A significant positive correlation has been found between plants’ ability to retain K1 in salt-treated leaves of wheat and their salinity tolerance (Wu et al., 2013). Ethylene promotes soil-salinity tolerance via improved Na1/K1 homeostasis mediated by respiratory burst oxidase homolog F (RBOHF), an ROS-producing protein-dependent regulation of Na1 accumulation, and RBOHF-independent regulation of K accumulation (Jiang et al., 2013). The K1 ion is an important inorganic osmolyte for salt tolerance and is correlated with the ability of a plant to retain proper K1 levels (Shabala and Cuin, 2008). Shabala and Pottosin (2010) suggested that the major focus of plant physiologists and breeders under salinity stress should be on revealing the specificity of K1 channel regulation and a “fine-tuning” of all mechanisms involved in the regulation of K1 homeostasis in plants, including both plasma- and endomembrane-channels and transporters. K1 plays role in charge balance, osmotic adjustment, and enzyme catalysis, as well as in growth and development (Rigas et al., 2001; Elumalai et al., 2002). Calcium, another important osmolyte, is necessary to control K1/Na1 selective accumulation in plants, effectively reducing Na1 uptake and increasing salinity tolerance (Cramer et al., 1987; Hasegawa et al., 2000; Zhu, 2003). K1/Na1 selective accumulation is Ca21-dependent with the high-affinity system transporting predominantly K1 over Na1 when Ca21 is present (Epstein, 1961; Rains and Epstein, 1965). At high concentrations, Na1 can displace membrane-associated Ca21 (Cramer et al., 1985; Kinraide, 1999) with the potential to cause Ca21 deficiency. Greenway and Munns (1980) suggested that the Na1/Ca21 ratio of the external solution should be maintained at a constant value to avoid the confounding effects of increases in NaCl. Munns and Tester (2008) reported that supplementation of Ca21 to wheat varieties improved their salt tolerance ability by reducing Na1 uptake. Kim et al. (2007) reported that calcium sensors, CBL10, and the salt tolerance factor CIPK24 (SOS2) constitute a novel salt-tolerance pathway that regulates the sequestration of Na1 in plant cells. CIPK24 (SOS2) also interacts with CBL4 (SOS3) to regulate salt export across the plasma membrane. Thus, inorganic osmolytes help in salinity tolerance via maintaining osmotic adjustment and reducing the uptake and concentration of Na1.

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16.5 Organic osmolytes in salinity tolerance Organic osmolytes play an important role in salinity tolerance and in this section the importance of some important organic osmolytes in salinity tolerance are discussed.

16.5.1 Proline in salinity tolerance Proline (Pro) is an important osmolyte, synthesized from its precursor glutamic acid that acts as an osmoprotectant under osmotic stress conditions (Delauney and Verma, 1993; Verbruggen and Hermans, 2008; Ahmad and Sharma, 2008; Ahmad et al., 2012; Koyro et al., 2012; Rasool et al., 2013). In plants subjected to salt stress, Pro acts as a compatible osmolyte enzyme protectant, free radical scavenger, cell redox balancer, cytosolic pH buffer, and stabilizer for subcellular structures (Kishor et al., 2005; Verbruggen and Hermans, 2008). It also acts as a scavenger of ROS in plants under salt stress (Becker et al., 2009), storage of carbon and nitrogen (Hare and Cress, 1997), reduction of NaCl-induced K1 efflux from roots (Cuin and Shabala, 2005), and salt-stress signaling (Khedr et al., 2003; Szabados and Savouré, 2010). Pyrroline-5-carboxylate synthase (P5CS) and pyrroline-5-carboxylate reductase (P5CR) are two important enzymes that play important roles in the biosynthesis of proline (Ashraf and Foolad, 2007). The catabolism of proline occurs in mitochondria via the sequential action of proline dehydrogenase (PDH) or proline oxidase (POX), producing P5C from proline and P5C dehydrogenase (P5CDH), which regenerate glutamate from P5C. Alternatively, Pro can be synthesized from ornithine, which is transaminated first by ornithine-δ-aminotransferase (OAT), producing GSA and P5C; this is then converted to Pro (Delauney et al., 1993; Roosens et al., 1998). Under salt and water stress, Pro is the most common osmoprotectant produced (Hanson and Hitz, 1982; Yoshiba et al., 1995). Najafi et al. (2006) reported increased accumulation of Pro in Pisum sativum under salt stress; this has been correlated with the increased activity of D-pyrroline-5-carboxylate reductase (Madan et al., 1995) and with the low activity of Pro oxidase and Pro dehydrogenase (Girija et al., 2002). Under salt stress, Amini and Ehsanpour (2005) reported that a higher level of Pro in stems and leaves may be due to expression of gene-encoding enzymes of Pro synthesis (e.g., P5C) or a decrease in enzymes of Pro oxidation (e.g., PDH). Overexpression in transgenic tobacco of a gene encoding a P5CS from mungbean plants resulted in the accumulation of Pro up to 18-fold over control plants; this enhanced biomass production under salt stress (Kishor et al., 1995). On the other hand, antisense suppression of Pro degradation improved salt tolerance (Nanjo et al., 1999). Under salt stress, P5CS1 is induced and PDH is repressed (Peng et al., 1996; Kishor et al., 2005). Silva-Ortega et al. (2008) observed by RT-PCR analysis that the Osp5cs gene of Opuntia streptacantha was induced by salt stress and that the accumulated Pro functions as an osmolyte for intracellular osmotic adjustment; this plays a critical role in protecting photosynthetic activity. Besides, several authors found that salt-sensitive rice cultivars accumulated a higher level of Pro under salt stress than the salt-tolerant ones (Renuka Devi et al., 1996; Demiral and Tu¨rkan, 2005; Theerakulpisut et al., 2005). The relationship between high accumulation of Pro and poor growth performance in salt-sensitive rice may be related to the fact that synthesis of compatible solutes, including Pro, consumes a high energy and nitrogen source (Chen et al., 2007). Excess Pro in Arabidopsis may be toxic due to induction of apoptosis and programmed cell death and its

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conversion to pyroline-5 carboxylate that causes the production of ROS (Hellmann et al., 2000; Székely et al., 2008; Trovato et al., 2008). However, in transgenic tobacco, cotton, and potato plants, overexpression of P5CS genes has been reported to increase the levels of Pro and consequently growth and biomass production under drought and salinity stress conditions (Yamada et al., 2005; Hmida-Sayari et al., 2005; Parida et al., 2008). Proline accumulation in response to water stress and salinity is preceded by a rapid increase of the mRNA level of P5CS controlling the rate-limiting step of glutamate-derived Pro biosynthesis (Strizhov et al., 1997). It is reported to be involved in the synthesis of key proteins (dehydrins) that are necessary for stress responses (Khedr et al., 2003). Chakraborty et al. (2012) reported that the tolerant genotypes of Brassica have built-in mechanisms in the form of greater gene expression and activity of P5CS, which leads to enhanced Pro production. The Pro formed provides osmotolerance in the form of retention of moisture and membrane stability index, resulting in more yield stability. Banu et al. (2009) studied that Pro and betaine provided protection against NaCl-induced cell death by decreasing the level of ROS accumulation and lipid peroxidation. In soybean cell cultures maintained under salt stress, exogenous application of Pro increased activities of superoxide dismutase and peroxidase, which contributed to increased salt tolerance (Yan et al., 2000; Hua and Guo, 2002). In barley embryo cultures under saline conditions, exogenous application of Pro resulted in a decrease in Na1 and Cl2 accumulation and an increase in growth (Lone et al., 1987). Such ameliorative effects of Pro were thought to be due to plasma membrane stabilization (Mansour, 1998). Roy et al. (1993) furnished exogenous Pro to rice seedlings and found that Pro avoided salt stress and toxicity caused by salinity stress. Thus, their findings showed that Pro helps reduce the adverse effects of salinity stress and manipulation of genes involved in Pro biosynthesis will provide a novel strategy to develop salinity-tolerant cultivars.

16.5.2 Glycinebetaine in salinity tolerance Another important osmolyte involved in salinity tolerance is GB. Increased accumulation of betaine in plants subjected to osmotic stress supports its physiological relevance in alleviating the stress (Jones, 1984). Betaine has been shown to protect enzymes and membranes from cold (Krall et al., 1989), heat (Jolivet et al., 1982), salt (Jolivet et al., 1983), and freezing stress (Zhao et al., 1992). Organic osmolytes show lower accumulation in transgenic plants as compared to their natural accumulators and therefore contribute less to osmotic adjustment (Giri, 2011). However, to bring stress tolerance, they are also involved in ROS scavenging and macromolecules protection and act as a reservoir for carbon and nitrogen sources. Betaine may also stabilize the photosystem II (PSII) proteinpigment complex in the presence of high NaCl concentrations (Murata et al., 1992; Papageorgiou and Murata, 1995). In accordance with the importance of betaine in salinity tolerance, genetic engineering of the biosynthesis of betaine from choline has been the focus of considerable attention. This is a potential strategy for increasing stress tolerance in stress-sensitive plants that are incapable of synthesizing this compatible osmolyte (Sakamoto and Murata, 1998). Glycinebetaine is synthesized from the oxidation of choline by choline monooxygenase (CMO) (Nuccio et al., 1998) into betaine aldehyde and then an NAD1-dependent enzyme, betaine aldehyde dehydrogenase (BADH), produces GB (Osteras et al., 1998). These enzymes are mainly found in chloroplast stroma and their activity is increased in response to salt stress (Rhodes and Hanson,

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1993). Zhang et al. (2009) reported that transgenic cotton overexpressing AhCMO (CMO cloned from Atriplex hortensis) was more tolerant to salt stress as a result of the elevated accumulation of GB, which provided greater protection of the cell membrane and photosynthetic capacity than in nontransgenic cotton. Glycinebetaine helps in maintaining water status and shoot growth under salinity stress in maize (Saneoka et al., 1995). Levels of GB accumulation are correlated with the extent of salt tolerance by plants (Rhodes and Hanson, 1993). In Prosopis alba, endogenous GB increased under salinity stress, suggesting its importance in osmotic adjustment (Meloni et al., 2004). Exogenous application of GB to plants that accumulate little or none of this compound may help to reduce the adverse effects of environmental stress (Yang and Lu, 2005; Ashraf and Foolad, 2007). In maize, exogenously applied GB improved growth, leaf water content, net photosynthesis, and the apparent quantum yield of photosynthesis in stressed plants (Yang and Lu, 2005). Foliar application of GB on rice plants alleviated salt-induced inhibition of shoot growth and had significantly lower Na1 concentrations and higher K1 concentrations in shoots compared with untreated plants (Rahman et al., 2002). Low concentrations of exogenous GB significantly reduced salinityinduced K1 efflux from barley roots in a doseresponse manner (Cuin and Shabala, 2005). Meloni and Martıńez (2009) reported that GB enhanced salinity tolerance in Prosopis ruscifolia through the maintenance of K1 homeostasis by preventing NaCl-induced K1 leakage, reduction of lipid peroxidation-linked membrane deterioration, and an increase in SOD activity—a key enzyme of the ROS scavenging system. Glycinebetaine is considered to be one of the most effective osmoprotectants because it interacts with both the hydrophobic and hydrophilic domains of macromolecules without perturbing the cellular functions (Sakamoto and Murata, 2002). Glycinebetaine protects the cells from stresses by stabilizing the quaternary structure of antioxidant enzymes, biomembranes, and the oxygen-evolving PSII complex (Robinson and Jones, 1986). Betaine may also stabilize the photosystem II proteinpigment complex in the presence of high NaCl concentrations (Murata et al., 1992; Papageorgiou and Murata, 1995).

16.5.3 Carbohydrates and salinity tolerance Salinity stress affects many physiological and biochemical processes in plants. Among the major effects on plant metabolic pathways are those involving carbohydrate metabolism, with the accumulation of sugars in addition to other organic solutes (Ashraf et al., 2002). Carbohydrates are frequently associated with active osmotic adjustment (Dubey and Singh, 1999; Ashraf et al., 2002; Meloni et al., 2003) and have long been known to increase in a wide range of plants grown under saline conditions (Tattini et al., 1996; Bohnert and Shen, 1999). Carbohydrates, such as soluble sugars (e.g., glucose, fructose, sucrose, fructans), accumulate under salt stress to accommodate the ionic balance in the vacuoles (Ashraf and Harris, 2004). Morant-Manceau et al. (2004) reported that the concentration of sugar changes in response to salt stress in Triticum dicoccum. Soluble carbohydrates significantly contribute to the mechanisms of adaptation to salt stress (Kerepesi and Galiba, 2000; Parida et al., 2002). Simple sugars not only act as osmolytes but also can stabilize membranes in desiccated resurrection plants (Norwood et al., 2000). Plants subjected to salt stress accumulate sugars that help in osmoprotection, osmotic adjustment, carbon storage, radical scavenging, and stabilization of the structure of proteins such as Rubisco (Rejsiková et al., 2007). Roussos et al. (2005) reported that carbohydrates may play an osmoprotective role in jojoba under salt stress under in vitro conditions by enhancing water uptake

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from the medium up to a certain salinity level. Soluble sugars are responsible for as much as 50% of the total osmotic potential in glycophytes subjected to saline conditions (Cram, 1976). Gil et al. (2013) provided evidence for a functional role of carbohydrates in salt tolerance. They noted that the level of specific sugars and polyols increases in many halophytic taxa and such an increase in the intracellular levels of particular carbohydrates is in accordance with salt tolerance; this was also confirmed in transgenic plants overexpressing the corresponding biosynthetic enzymes. Dubey and Singh (1999) reported that the activity of sucrose phosphate synthase (SPS) increases under salt stress, whereas starch phosphorylase activity decreases. Soluble sugar accumulation may be due to transformation of starch to sugars or less consumption of carbohydrates by the tissues under saline conditions (Hare et al., 1998). In addition to increased production via induction of sucrose phosphate synthase activity (Huber and Huber, 1996; Yang et al., 2001), sucrose is generated quickly via gluconeogenesis or from catabolism of polymeric carbohydrates in response to salt or osmotic stress (Levitt, 1980). Mannitol-synthesizing species (e.g., celery) have been shown to grow well under high levels of salt stress (Everard et al., 1994), as do raffinose oligosaccharideaccumulating plants such as cabbage (Maas and Grattan, 1999; Minorsky, 2003). Munns (1993) reported that the concentration of sugars and reserve polysaccharides increases in plants exposed to salinity stress. This increase is consistent with the nonutilization of sugars in the growing tissues and a subsequent build-up in the rest of the plant under stress. Pattanagul and Thitisaksakul (2008) suggested that partitioning of sugars into starch may be involved in salinity tolerance by avoiding metabolic alterations. Simple sugars not only act as osmolytes but also can stabilize membranes in desiccated resurrection plants (Norwood et al., 2000). They contribute up to 50% of the total osmotic potential in glycophytes exposed to salt stress (Murakezy et al., 2003). There are reports indicating that the content of soluble sugar in sunflower is higher in tolerant cultivars than sensitive cultivars under salt stress (Ashraf and Fatima, 1995; Ashraf and Tufail, 1995). For most plants subjected to salt stress, the concentration of sugar (e.g., sucrose, fructose, and glucose) increases in order to overcome salt stress (Mansour, 2000; Ashraf and Harris, 2004). The role of soluble sugars in the adaptation of plants to salt stress and its accumulation can be an indicator for salt tolerance in breeding programs for some species (Ashraf and Harris, 2004). Siringam et al. (2011) reported that under salinity stress, the increase in Na1 was positively related to total soluble sugars, resulting in an osmotic adjustment of the membrane that maintains water availability. The authors suggested that the accumulation of sugars in the roots of saltsensitive rice, Pathumthani1 (PT1), may be a primary salt-defense mechanism that functions as an osmotic control. The most common compatible osmolytes in plants include sugar alcohols (e.g., mannitol, sorbitol); overexpression of these polyols was described as a potential route for improving abiotic stress tolerance in plants (Yokoi et al., 2002; Wang et al., 2003). Trehalose, a disaccharide, accumulates in many organisms under various abiotic stresses and has been reported to be both an osmolyte and an osmoprotectant (Crowe et al., 1984; Hounsa et al., 1998). It protects membranes and cell proteins that are exposed to water deficit conditions (Garcia et al., 1997) and reduces aggregation of denatured proteins (Singer and Lindquist, 1998). An increased resistance to oxidative stress also has been reported in tobacco plants accumulating mannitol in the chloroplasts (Stoop et al., 1996). Abebe et al. (2003) reported an improved tolerance to salinity in bread wheat expressing the mtlD gene (encoding mannitol-1-phosphate dehydrogenase). Ramadan et al. (2013) reported that this gene confers salt-stress protection in transgenic wheat through the induction of mannitol and the reduction of sugar accumulation in plant tissues.

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Some studies for increasing tolerance to environmental stresses, through metabolic engineering of compatible solutes, have shown that increases in soluble sugars and/or other osmolytes are responsible for increasing plants’ tolerance to abiotic stresses such as drought, salinity, and cold (Rathinasabapathi, 2000).

16.6 Conclusion and future prospects Salinity is the most common problem that threatens the growth and yield of plants. Alleviation of the adverse effects of salinity is desirable in order to protect them from great loss. Plants’ potential to tolerate salinity-induced adverse effects depends on various biochemical pathways that help in maintaining ion homeostasis, retaining water, or protecting photosynthetic ability. Among the essential pathways, osmolytes synthesis is considered very important in view of its role in salinity tolerance. Osmolytes are involved in osmoregulation and in the protection of proteins and membranes. These osmolytes are either organic or inorganic. Organic osmolytes are more important and have been widely studied. They do not interfere with normal biochemical reactions and are known to be compatible solutes that act as osmoprotectants during osmotic stress. Among the organic osmolytes, most studies focus on nitrogenous compounds, Pro, or GB, which under stress conditions help mediate osmotic adjustment and protect subcellular structures. Manipulation of inorganic or organic osmolyte concentration may provide a novel strategy for increasing salinity tolerance. The main regulatory point of the osmolyte metabolism needs to be identified in order to target up-regulation of biosynthesis through various genetic and molecular approaches. Increasing the concentration of inorganic osmolytes, or their transporters, to increase potentially important inorganic osmolytes (e.g., K1 and Ca1) may reduce the severity of high Na1. Further, manipulation of enzymes or expression of the genes of Pro synthesis may increase plants’ salt-tolerance strategy because of the role of proline in scavenging free radicals, stabilizing subcellular structures, and buffering cellular redox potential under stress. Similarly, GB also helps to protect cells from stresses by stabilizing biomembranes, the oxygen PSII complex, and the quaternary structure of antioxidant enzymes; in addition, manipulating its synthetic pathway may increase salt tolerance. Among carbohydrates, increased expression of the genes involved in mannitol or other important sugars may enhance salinity tolerance potential. Besides the osmolytes discussed in this chapter, many osmolytes are still left untouched. The main aim here was to focus on the vision that knowledge about strategies involved in salinity stress tolerance, particularly through manipulating osmolytes, may provide a novel way to increase plants’ tolerance to salinity stress.

Acknowledgments Financial assistance by a DS Kothari Post-Doctoral Fellowship to the first author is gratefully acknowledged. The author is also thankful to the Department of Botany at Jamia Hamdard, Delhi, for providing the workplace.

References Abebe, T., Guenzi, A.C., Martin, B., Cushman, J.C., 2003. Tolerance of mannitol-accumulating transgenic wheat to water stress and salinity. Plant Physiol. 131, 17481755.

396


Ahmad, P., Sharma, S., 2008. Salt stress and phyto-biochemical responses of plants. Plant Soil Environ. 54, 8999. Ahmad, P., Hakeem, K.R., Kumar, A.M., Akram, N.A., 2012. Salt-induced changes in photosynthetic activity and oxidative defense system of three cultivars of mustard (Brassica juncea L.). Afr. J. Biotechnol. 11, 26942703. Amini, F., Ehsanpour, A., 2005. Soluble proteins, proline, carbohydrates, and Na1/K1 changes in two tomato (Lycopersicon esculentum Mill.) cultivars under in vitro salt stress. Am. J. Biochem. Biotech. 1, 212216. Ashraf, M., 1994. Breeding for salinity tolerance in plants. Crit. Rev. Plant Sci. 13, 1742. Ashraf, M., Fatima, H., 1995. Responses of some salt tolerant and salt sensitive lines of safflower (Carthamus tinctorius L.). Acta. Physiol. Plant 17, 6171. Ashraf, M., Foolad, M.R., 2007. Improving plant abiotic-stress resistance by exogenous application of osmoprotectants glycinebetaine and proline. Environ. Exp. Bot. 59, 206216. Ashraf, M., Harris, P.J.C., 2004. Potential biochemical indicators of salinity tolerance in plants. Plant Sci. 166, 316. Ashraf, M., Tufail, M., 1995. Variation in salinity tolerance in sunflower (Helianthus annuus L.). J. Agron. Crop Sci. 174, 351362. Ashraf, M., Asfaq, M., Ashraf, M.Y., 2002. Effects of increased supply of potassium on growth and nutrient content in pearl millet under water stress. Biol. Plant. 45, 141144. Banu, N.A., Hoque, A., Watanabe-Sugimoto, M., Matsuoka, K., Nakamura, Y., Shimoishi, Y., et al., 2009. Proline and glycinebetaine induced antioxidant defense gene expression and suppress cell death in cultured tobacco cells under salt stress. J. Plant Physiol. 166, 146156. Becker, D.F., Zhu, W., Natarajan, S., 2009. Proline metabolism and protection against oxidative stress. Faseb J. 23, 27. Bohnert, H.J., Jensen, R.G., 1996. Strategies for engineering water-stress tolerance in plants. Trends Biotechnol. 14, 8997. Bohnert, H.J., Shen, B., 1999. Transformation and compatible solutes. Sci. Hortic. 78, 237260. Bolen, D.W., Baskakov, I.V., 2001. The osmophobic effect: natural selection of a thermodynamic force in protein folding. J. Mol. Biol. 310, 955963. Briens, M., Larher, F., 1982. Osmoregulation in halophytic higher plants: a comparative study of soluble carbohydrates, polyols, betaines and free proline. Plant Cell Environ. 5, 287292. Burg, M.B., Ferraris, J.D., 2008. Intracellular organic osmolytes: function and regulation. J. Biol. Chem. 283, 73097313. Burg, M.B., Ferraris, J.D., Dmitireva, N.I., 2007. Cellular response to hyperosmotic stresses. Physiol. Rev. 87, 14411474. Chakraborty, K., Sairam, R.K., Bhattacharya, R.C., 2012. Differential expression of salt overly sensitive pathway genes determines salinity stress tolerance in Brassica genotypes. Plant Physiol. Biochem. 51, 90101. Chaparzadeh, N., Khavari-Nejad, R.A., Navari-Izzo, F., Izzo, R., 2003. Water relations and ionic balance in Calendula officinalis L. under salinity conditions. Agrochimic XLVII, 6979. Chaum, S., Kirdmanee, C., 2009. Effect of salt stress on proline accumulation, photosynthetic ability and growth characters in two maize cultivars. Pak. J. Bot. 41, 8798. Chen, Z., Cuin, T.A., Zhou, M., Twomey, A., Naidu, B.P., Shabala, S., 2007. Compatible solute accumulation and stress-mitigating effects in barley genotypes contrasting in their salt tolerance. J. Exp. Bot. 58, 42454255. Chinnusamy, V., Jagendorf, A., Zhu, J.-K., 2005. Understanding and improving salt tolerance in plants. Crop Sci. 45, 437448. Collins, K.D., 2006. Ion hydration: implications for cellular function, polyelectrolytes, and protein crystallization. Biophys. Chem. 119, 271281.

References

397

Cram, W.J., 1976. Negative feedback regulation of transport in cells: the maintenance of turgor, volume and nutrient supply. In: Luttge, U., Pitman, M.G. (Eds.), Encyclopaedia of Plant Physiology, New Series, vol. 2. Springer-Verlag, Berlin, pp. 284316. Cramer, G.R., Nowak, R.S., 1992. Supplemental manganese improves the relative growth, net assimilation and photosynthetic rates of salt-stressed barley. Physiol. Plant. 84, 600605. Cramer, G.R., Laüchli, A., Polito, V.S., 1985. Displacement of Ca21 by Na1 from plasmalemma of root cells. A primary response to salt stress? Plant Physiol. 79, 207211. Cramer, G.R., Lynch, J.L., Laüchli, A., Epstein, E., 1987. Influx of Na1, K1, and Ca21 into roots of saltstressed cotton seedlings. Effects of supplemental Ca21. Plant Physiol. 83, 510516. Crowe, J., Crowe, L., Chapman, D., 1984. Preservation of membranes in any hydrobiotic organism: the role of trehalose. Science 223, 701703. Cuin, T.A., Shabala, S., 2005. Exogenously supplied compatible solutes rapidly ameliorate NaCl-induced potassium efflux from barley roots. Plant Cell Physiol. 46, 19241933. Daneshmand, F., Mohammad, J.A., Khosrow, M.K., 2009. Effect of acetylsalicylic acid (Aspirin) on salt and osmotic stress tolerance in Solanum bulbocastanum in vitro: enzymatic antioxidants. Am. Eurasian J. Agric. Environ. Sci. 6, 9299. Delauney, A.J., Verma, D.P., 1993. Proline biosynthesis and osmoregulation in plants. Plant J. 4, 215223. Delauney, A.J., Hu, C.-A., Kavi Kishor, P.B., Verma, D.P.S., 1993. Cloning of ornithine-δ-aminotransferase cDNA from Vigna aconitifolia by transcomplementation in Escherichia coli and regulation of proline biosynthesis. J. Biol. Chem. 268, 1867318678. Demiral, T., Tu¨rkan, I., 2005. Comparative lipid peroxidation, antioxidant defense systems and proline content in roots of two rice cultivars differing in salt tolerance. Environ. Exp. Bot. 53, 247257. Dubey, R.S., Singh, A.K., 1999. Salinity induces accumulation of soluble sugars and alters the activity of sugar metabolizing enzymes in rice plants. Biol. Plant 42, 233239. Elumalai, R.P., Nagpal, P., Reed, J.W., 2002. A mutation in the Arabidopsis KT2/KUP2 potassium transporter gene affects shoot cell expansion. Plant Cell 14, 119131. Epstein, E., 1961. The essential role of calcium in selective cation transport by plant cells. Plant Physiol. 36, 437444. Everard, J.D., Gucci, R., Kahn, S.C., Flore, A.J., Loescher, W.H., 1994. Gas exchange and carbon partitioning in the leaves of celery (Apium graveolens L.) at various levels of root zone salinity. Plant Physiol. 106, 281292. Ferraris, J.D., Williams, C.K., Persaud, P., Zhang, Z., Chen, Y., Burg, M.B., 2002. Activity of the TonEBP/ OREBP transactivation domain varies directly with extracellular NaCl concentration. Proc. Natl. Acad. Sci. USA 99, 739744. Flowers, T.J., 2004. Improving crop salt tolerance. J. Exp. Bot. 55, 307319. Food and Agricultural Organization, 2008. Land and plant nutrition management service. Available from: ,www.fao.org/ag/agl/agll/spush/.pdf.. Furtana, G.B., Dumani, H., Tipirdamaz, R., 2013. Seasonal changes of inorganic and organic osmolyte content in three endemic Limonium species of Lake Tuz (Turkey). Turk. J. Bot. 37, 455463. Galinski, E.A., 1995. Osmoadaptation in bacteria. Adv. Microb. Physiol. 37, 272328. Garcia, A.B., Almeida-Engler, J., Lyer, S., Gerats, T., Van Montagu, M., Caplan, A.B., 1997. Effects of osmoprotectants upon NaCl stress in rice. Plant Physiol. 115, 159169. Gil, R., Boscaiu, M., Lull, C., Bautista, I., Lidoń, A., Vicente, O., 2013. Are soluble carbohydrates ecologically relevant for salt tolerance in halophytes? Funct. Plant Biol. 40, 805818. Giri, J., 2011. Glycinebetaine and abiotic stress tolerance in plants. Plant Signal. Behav. 6, 17461751. Girija, C., Smith, B.N., Swamy, P.M., 2002. Interactive effects of NaCl and CaCl2 on the accumulation of proline and glycinebetaine in peanut (Arachis hypogaea L.). Environ. Exp. Bot. 47, 110.

398


Glenn, E.P., Pfister, R., Brown, J.J., Thompson, T.L., O’Leary, J.W., 1996. Na and K accumulation and salt tolerance of Atriplex canescens (Chenopodiaceae) genotypes. Am. J. Bot. 83, 9971005. Graifenberg, A., Giustiniani, L., Temperini, O., Lipucci di Paola, M., 1995. Allocation of Na, Cl, K and Ca within plant tissues in globe artichoke (Cynara scolimus L.) under saline-sodic conditions. Sci. Hortic. 63, 110. Greenway, H., Munns, R., 1980. Mechanism of salt tolerance in nonhalophytes. Annu. Rev. Plant Physiol. 31, 149190. Gregorio, G.B., Senadhira, D., Mendoza, R.D., Manigbas, N.L., Roxas, J.P., Guerta, C.Q., 2002. Progress in breeding for salinity tolerance and associated abiotic stresses in rice. Field Crops Res. 76 (23), 91101. Guo, Y., Qiu, Q.S., Quintero, F.J., Pardo, J.M., Ohta, M., Zhang, C., et al., 2004. Transgenic evaluation of activated mutant alleles of SOS2 reveals a critical requirement for its kinase activity and C-terminal regulatory domain for salt tolerance in Arabidopsis thaliana. Plant Cell 16, 435449. Gupta, A.K., Jagdeep, S., Narinder, K., Rangil, S., 1993. Effect of polyethylene glycol-induced water stress on germination and reserve carbohydrate metabolism in chickpea cultivars differing in tolerance to water deficit. Plant Physiol. Biochem. 31, 369378. Guy, C.L., 1990. Cold acclimation and freezing stress tolerance: role of protein metabolism. Annu. Rev. Plant Physiol. Plant Mol. Biol. 41, 187223. Halfter, U., Ishitani, M., Zhu, J.K., 2000. The Arabidopsis SOS2 protein kinase physically interacts with and is activated by the calcium-binding protein SOS3. Proc. Natl. Acad. Sci. USA 97, 37353740. Hanson, A., Hitz, W., 1982. Metabolics responses of mesophytes to plant water deficits. Annu. Rev. Plant Physiol. 33, 163203. Hare, P.D., Cress, W.A., 1997. Metabolic implications of stress induced proline accumulation in plants. Plant Growth Regul. 21, 79102. Hare, P.D., Cress, W.A., Van Staden, J., 1998. Dissecting the roles of osmolyte accumulation during stress. Plant Cell Environ. 21, 535554. Harries, D., Ro¨sgen, J., 2008. A practical guide on how osmolytes modulate macromolecular properties. In: Correia, J.J., Detrich, H.W. (Eds.), Methods in Cell Biology. Elsevier, Amsterdam, pp. 679735. Hasegawa, P.M., Bressan, R.A., Zhu, J.K., Bohnert, H.J., 2000. Plant cellular and molecular responses to high salinity. Ann. Rev. Plant Physiol. Plant Mol. Biol. 51, 463469. Hayashi, H., Murata, N., 1998. Genetically engineered enhancement of salt tolerance in higher plants. In: Sato, K., Murata, N. (Eds.), Stress Responses of Photosynthetic Organisms: Molecular Mechanisms and Molecular Regulation. Elsevier, Amsterdam, pp. 133148. Hellmann, H., Funk, D., Rentsch, D., Frommer, W.B., 2000. Hypersensitivity of an Arabidopsis sugar signaling mutant towards exogenous proline application. Plant Physiol. 122, 357368. Hmida-Sayari, A., Gargouri-Bouzid, R., Bidani, A., Jaoua, L., Savoure, A., Jaoua, S., 2005. Overexpression of Δ1-pyrroline-5-carboxylate synthetase increases proline production and confers salt tolerance in transgenic potato plants. Plant Sci. 169, 746752. Hochachka, P.W., Somero, G.N., 2002. Biochemical Adaptation. Mechanism and Process in Physiological Evolution. Oxford University Press, Oxford. Hounsa, C.G., Brandt, E.V., Thevelein, J., Hohmann, S., Prior, B.A., 1998. Role of trehalose in survival of Saccharomyces cerevisiae under osmotic stress. Microbiology 144, 671680. Hua, B., Guo, W.Y., 2002. Effect of exogenous proline on SOD and POD activity of soyabean callus under salt stress. Acta Agric. Boreali-Sinica 17, 3740. Huber, S.C., Huber, J.L., 1996. Role and regulation of sucrose phosphate synthase in higher plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 47, 431444. Hussain, K., Nisar, M.F., Majeed, A., Nawaz, K., Bhatti, K.H., Afghan, S., et al., 2010. What molecular mechanism is adapted by plants during salt stress tolerance? Afr. J. Biotech. 9, 416422.

References

399

Hussain, T., Chandrasekhar, M., Hazara, Z., Sultan, 2008. Recent advances in salt stress biologya review. Mol. Biol Rep. 3, 813. Jiang, C., Benfield, E.J., Cao, Y., Smith, J.A.C., Harberd, N.P., 2013. An Arabidopsis soil-salinitytolerance mutation confers ethylene-mediated enhancement of sodium/potassium homeostasis. Plant Cell 25, 35353552. Jolivet, Y., Larher, F., Hamelin, J., 1982. Osmoregulation in halophytic higher plants: the protective effect of glycinebetaine against the heat destabilization of membranes. Plant Sci. Lett. 25, 193201. Jolivet, Y., Hamelin, J., Larher, F., 1983. Osmoregulation in halophytic higher plants: the protective effects of glycinebetaine and other related solutes against the oxalate destabilization of membranes in beet root cells. Z Pflanzenphysiol. 109S, 171180. Jones, R.G.W., 1984. Phytochemical aspects of osmotic adaptation. Rec. Adv. Phytochem. 18, 5578. Kerepesi, I., Galiba, G., 2000. Osmotic and salt stress-induced alteration in soluble carbohydrate content in wheat seedlings. Crop Sci. 40, 482487. Khan, M.I.R., Iqbal, N., Masood, A., Khan, N.A., 2012. Variation in salt tolerance of wheat cultivars: role of glycinebetaine and ethylene. Pedosphere 22, 746754. Khedr, A.H.A., Abbas, M.A., Wahld, A.A.A., Qulck, W.P., Abogadallah, G.M., 2003. Proline induces the expression of salt-stress-responsive proteins and may improve the adaptation of Pancratium maritimum L. to salt-stress. J. Exp. Bot. 54, 25532562. Kim, B.G., Waadt, R., Cheong, Y.H., Pandey, G.K., Dominguez-Solis, J.R., Schu¨ltke, S., et al., 2007. The calcium sensor CBL10 mediates salt tolerance by regulating ion homeostasis in Arabidopsis. Plant J. 52, 473484. Kinraide, T.B., 1999. Interactions among Ca21, Na1 and K1 in salinity tolerance: quantitative resolution of multiple toxic and ameliorative effects. J. Exp. Bot. 50, 14951505. Kishor, P.B.K., Hong, Z., Miao, G.H., Hu, C.A.A., Verma, D.P.S., 1995. Overexpression of Δ1-pyrroline-5carboxylate synthetase increases proline production and confers osmotolerance in transgenic plants. Plant Physiol. 108, 13871394. Kishor, P.B.K., Sangam, S., Amrutha, R.N., Sri Laxmi, P., Naidu, K.R., Rao, K.R.S.S., et al., 2005. Regulation of proline biosynthesis, degradation, uptake and transport in higher plants: its implications in plant growth and abiotic stress tolerance. Curr. Sci. 88, 424438. Kolukisaoglu, U., Weinl, S., Blazevic, D., Batistic, O., Kudla, J., 2004. Calcium sensors and their interacting protein kinases: genomics of the Arabidopsis and rice CBL-CIPK signaling networks. Plant Physiol. 134, 4358. Kong, X., Pan, J., Zhang, M., Xing, X., Zhou, Y., Liu, Y., et al., 2011. ZmMKK4, a novel group C mitogenactivated protein kinase kinase in maize (Zea mays), confers salt and cold tolerance in transgenic Arabidopsis. Plant Cell Environ. 34, 12911303. Koyro, H.W., Ahmad, P., Geissler, N., 2012. Abiotic stress responses in plants: an overview. In: Ahmad, P., Prasad, M.N.V. (Eds.), Environmental Adaptations and Stress Tolerance of Plants in the Era of Climate Change. Springer, New York, pp. 128. Krall, J.P., Edwards, G.E., Andreo, C.S., 1989. Protection of pyruvate, Pi dikinase from maize against cold lability by compatible solutes. Plant Physiol. 89, 280285. Levitt, J., 1980. Responses of Plants to Environmental Stresses, Water Radiation, Salt and Other Stresses, vol. II. second ed. Academic Press, New York. Liu, J.J.J., Krenz, D.C., Galvez, A.F., de Lumen, B.O., 1998a. Galactinol synthase (GS): increased enzyme activity and levels of mRNA due to cold and desiccation. Plant Sci. 134, 1120. Liu, J.P., Zhu, J.K., 1998. A calcium sensor homolog required for plant salt tolerance. Science 280, 19431945. Liu, Q., Kasuga, M., Sakuma, Y., Abe, H., Miura, S., Yamaguchi-Shinozaki, K., et al., 1998b. Two transcription factors, DREB1 and DREB2, with an EREBP/AP2 DNA binding domain separate two cellular signal

400


transduction pathway in drought- and low-temperature-responsive gene expression, respectively, in Arabidopsis. Plant Cell 10, 13911406. Lone, M.I., Kueh, J.S.H., Wyn Jones, R.G., Bright, S.W.J., 1987. Influence of proline and glycinebetaine on salt tolerance of cultured barley embryos. J. Exp. Bot. 38, 479490. Maas, E.V., Grattan, S.R., 1999. Crop yields as affected by salinity. In: Skaggs, R.W., van Schilfgaarde, J. (Eds.), Agricultural Drainage. ASA, CSSA, SSA, Madison, WI, pp. 55108. Maathuis, F.J.M., Amtmann, A., 1999. K1 nutrition and Na1 toxicity: the basis of cellular K1/Na1 ratios. Ann. Bot. 84, 123133. Madan, S., Nainawatte, H.S., Jain, R.K., Choudhury, J.B., 1995. Proline and proline metabolizing enzymes in in-vitro NaCl tolerant Brassica juncea under salt stress. Ann. Bot. 76, 5157. Mahajan, S., Pandey, G.K., Tuteja, N., 2008. Calcium- and salt-stress signaling in plants: shedding light on SOS pathway. Arch. Biochem. Biophy. 471, 146158. Mansour, M.M.F., 1998. Protection of plasma membrane of onion epidermal cells by glycinebetaine and proline against NaCl stress. Plant Physiol. Biochem. 36, 767772. Mansour, M.M.F., 2000. Nitrogen containing compounds and adaptation of plants to salinity stress. Biol. Plant 43, 491500. Martıńez, J.P., Ledent, J.F., Bajji, M., Kinet, J.M., Lutts, S., 2003. Effect of water stress on growth, Na and K accumulation and water use efficiency in relation to osmotic adjustment in two populations of Atriplex halimus L. Plant Growth Regul. 41, 6373. Meloni, D.A., Martıńez, C.A., 2009. Glycinebetaine improves salt tolerance in vinal (Prosopis ruscifolia Griesbach) seedlings. Braz. J. Plant Physiol. 21, 233241. Meloni, D.A., Oliva, M.A., Martıńez, C.A., Cambraia, J., 2003. Phytosynthesis and activity of superoxide dismutase, peroxidase and glutathione reductase in cotton under salt stress. Environ. Exp. Bot. 49, 6976. Meloni, D.A., Gulota, M.R., Martıńez, C.A., Oliva, M.A., 2004. The effect of salt stress on growth, nitrate reduction and proline and glycinebetaine accumulation in Prosopis alba. Braz. J. Plant Physiol. 16, 3946. Minorsky, P.V., 2003. Raffinose oligosaccharides. Plant Physiol. 131, 11591160. Misra, N., Gupta, A.K., 2005. Effect of salt stress on proline metabolism in two high yielding genotypes of green gram. Plant Sci. 169, 331339. Miyakawa, H., Woo, S.K., Dahl, S.C., Handler, J.S., Kwon, H.M., 1999. Tonicity-responsive enhancer binding protein, a rel-like protein that stimulates transcription in response to hypertonicity. Proc. Natl. Acad Sci. USA 96, 25382542. Morant-Manceau, A., Pradier, E., Tremblin, G., 2004. Osmotic adjustment, gas exchanges and chlorophyll fluorescence of a hexaploid triticale and its parental species under salt stress. J. Plant Physiol. 161, 2533. Munns, R., 1993. Physiological processes limiting plant growth in saline soils: some dogmas and hypotheses. Plant Cell Environ. 16, 1524. Munns, R., 2002. Comparative physiology of salt and water stress. Plant Cell Environ. 25, 239250. Munns, R., James, R.A., Lauchli, A., 2006. Approaches to increasing the salt tolerance of wheat and other cereals. J. Exp. Bot. 57, 10251043. Munns, R., Tester, M., 2008. Mechanism of salinity tolerance. Annu. Rev. Plant Biol. 59, 651681. Murakezy, P., Nagy, Z., Duhazé, C., Bouchereau, A., Tuba, Z., 2003. Seasonal changes in the levels of compatible osmolytes in three halophytic species of inland saline vegetation in Hungary. J. Plant Physiol. 160, 395401. Murata, N., Mohanty, P.S., Hayashi, H., Papageorgiou, G.C., 1992. Glycinebetaine stabilizes the association of extrinsic proteins with the photosynthetic oxygen-evolving complex. FEBS Lett. 296, 187189. Muscolo, A., Panuccio, M.R., Sidari, M., 2003. Effects of salinity on growth, carbohydrate metabolism and nutritive properties of kikuyu grass (Pennisetum clandestinum Hochst). Plant Sci. 164, 11031110. Najafi, F., Khavari, R.A., Rastgar, J.F., Sticklen, M., 2006. Physiological changes in Pea (Pisum sativum L. cv. Green Arrow) under NaCl salinity. Pak. J. Biol. Sci. 9, 974978.

References

401

Nanjo, T., Kobayashi, M., Yoshiba, Y., Kakubari, Y., Yamaguchi Shinozaki, K., Shinozaki, K., 1999. Antisense suppression of proline degradation improves tolerance to freezing and salinity in Arabidopsis thaliana. FEBS Lett. 461, 205210. Nazar, R., Iqbal, N., Syeed, S., Khan, N.A., 2011. Salicylic acid alleviates decreases in photosynthesis under salt stress by enhancing nitrogen and sulfur assimilation and antioxidant metabolism differentially in two mungbean cultivars. J. Plant Physiol. 168, 807815. Noiraud, N., Maurousset, L., Lemoine, R., 2001. Transport of polypols in higher plants. Plant Physiol. Biochem. 39, 717728. Norwood, M., Truesdale, M.R., Richter, A., Scott, P., 2000. Photosynthetic carbohydrate metabolism in the resurrection plant Craterostigma plantagineum. J. Exp. Bot. 51, 159165. Nuccio, M.L., Russell, B.L., Nolte, K.D., Rathinasabapathi, B., Gage, D.A., Hanson, A.D., 1998. The endogenous choline supply limits glycine betaine synthesis in transgenic tobacco expressing choline monooxygenase. Plant J. 16, 487496. Obendorf, R.L., 1997. Oligosaccharides and galactosyl cyclitols in seed desiccation tolerance. Seed Sci. Res. 7, 6374. Osteras, M., Boncompagni, E., Vincent, N., Poggi, M.C., Le Rudulier, D., 1998. Presence of a gene encoding choline sulfatase in Sinorizobium meliloti bet operon: choline-O-sulfate is metabolized into glycinebetaine. Proc. Natl. Acad. Sci. USA 95, 1139411399. Ottow, E.A., Brinker, M., Teichmann, T., Fritz, E., Kaiser, W., Brosché, M., et al., 2005. Populus euphratica displays apoplastic sodium accumulation, osmotic adjustment by decreases in calcium and soluble carbohydrates, and develops leaf succulence under salt stress. Plant Physiol. 139, 17621772. Papageorgiou, G.C., Murata, N., 1995. The unusually strong stabilizing effects of glycinebetaine on the structure and function in the oxygen-evolving photosystem II complex. Photosynth. Res. 44, 243252. Parida, A.K., Das, B., 2005. Salt tolerance and salinity effects on plants. Ecotoxicol. Environ. Saf. 60, 324334. Parida, A.K., Das, B., Das, P., 2002. NaCl stress causes changes in photosynthetic pigments, proteins and other metabolic components in the leaves of a true mangrove, Bruguiera parviflora, in hydroponic culture. Plant Biol. 45, 2836. Parida, A.K., Dagaonkar, V.S., Phalak, M.S., Aurangabadkar, L.P., 2008. Differential responses of the enzymes involved in proline biosynthesis and degradation in drought tolerant and sensitive cotton genotypes during drought stress and recovery. Acta Physiol. Plant 30, 619627. Pattanagul, W., Thitisaksakul, M., 2008. Effect of salinity stress on growth and carbohydrate metabolism in three rice (Oryza sativa L.) cultivars differing in salinity tolerance. Ind. J. Exp. Biol. 46, 736742. Peng, Z., Lu, Q., Verma, D.P.S., 1996. Reciprocal regulation of Δ1-pyrroline-5-carboxylate synthetase and proline dehydrogenase genes controls proline levels during and after osmotic stress in plants. Mol. Gen. Genet. 253, 334341. Popp, M., Smirnoff, N., 1995. Polyol accumulation and metabolism during water deficit. In: Smirnoff, N. (Ed.), Environment and Plant Metabolism: Flexibility and Acclimation. Bios Scientific, Oxford, pp. 199215. Quan, R.D., Lin, H., Mendoza, L., Zhang, Y., Cao, W., Yang, Y., et al., 2007. SCABP8/CBL10, a putative calcium sensor, interacts with the protein kinase SOS2 to protect Arabidopsis shoots from salt stress. Plant Cell 19, 14151431. Quintero, F.J., Ohta, M., Shi, H., Zhu, J.-K., Pardo, J.M., 2002. Reconstitution in yeast of the Arabidopsis SOS signaling pathway for Na1 homeostasis. Proc. Natl. Acad. Sci. USA 99, 90619066. Quintero, F.J., Martinez-Atienza, J., Villalta, I., Jiang, X., Kim, W.-Y., Ali, Z., et al., 2011. Activation of the plasma membrane Na1/H1 antiporter Salt-Overly-Sensitive 1 (SOS1) by phosphorylation of an autoinhibitory C-terminal domain. Proc. Natl. Acad. Sci. USA 108, 26112616.

402


Rahman, M., Miyake, H., Takeoka, Y., 2002. Effects of exogenous glycinebetaine on growth and ultrastructure of salt-stressed rice seedlings (Oryza sativa L.). Plant Prod. Sci. 5, 3344. Rains, D.W., Epstein, E., 1965. Transport of sodium in plant tissues. Science 148, 1611. Ramadan, A.M., Eissa, H.F., Hassanein, S.E., Abdel Azeiz, A.Z., Saleh, O.M., Mahfouz, H.T., et al., 2013. Increased salt stress tolerance and modified sugar content of bread wheat stably expressing the mtlD gene. Life Sci. J. 10, 23482362. Rasool, S., Hameed, A., Azooz, M.M., Rehman, M., Siddiqi, T.O., Ahmad, P., 2013. Salt stress: causes, types and responses of plants. In: Ahmad, P., Azooz, M.M., Prasad, M.N.V. (Eds.), Ecophysiology and Responses of Plants under Salt Stress. Springer, New York, USA, pp. 124. Rathinasabapathi, B., 2000. Metabolic engineering for stress tolerance: installing osmoprotectant synthesis pathways. Ann. Bot. 86, 709716. Rejsiková, A., Patková, L., Eva Stodulková, E., Lipavská, H., 2007. The effect of abiotic stresses on carbohydrate status of olive shoots (Olea europaea L.) under in vitro conditions. J. Plant Physiol. 164, 174184. Renuka Devi, P.S., Sabu, A., Sheeja, T.E., Nambisan, P., 1996. Proline accumulation and salt tolerance in rice. In: Ravishankar, G.A., Venkataraman, L. (Eds.), Recent Advances in Biotechnological Applications of Plant Tissue and Cell Culture. Oxford and IBH Publishing, New Delhi, India, pp. 410414. Reynolds, M.P., Mujeeb-Kazi, A., Sawkins, M., 2005. Prospects of utilizing plant-adaptive mechanisms to improve wheat and other crops in drought- and salinity-prone environment. Ann. Appl. Biol. 146, 239259. Rhodes, D., Hanson, A.D., 1993. Quaternary ammonium and tertiary sulfonium compounds in higher plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 44, 375384. Rigas, S., Debrosses, G., Haralampidis, K., Vicente-Agullo, F., Feldmann, K.A., Grabov, A., et al., 2001. TRH1 encodes a potassium transporter required for tip growth in Arabidopsis root hairs. Plant Cell 13, 139151. Robinson, S.P., Jones, J.P., 1986. Accumulation of glycinebetaine in chloroplasts provides osmotic adjustment during salt stress. Aust. J. Plant Physiol. 13, 659668. Roosens, NHCJ, Thu, T.T., Iskandar, H.M., Jacobs, M., 1998. Isolation of the ornithine-δ-aminotransferase cDNA and effect of salt stress on its expression in Arabidopsis thaliana. Plant Physiol. 117, 263271. Roussos, P.A., Vemmos, S.N., Pontikis, C.A., 2005. The role of carbohydrates on salt tolerance of Jojoba [Sim mondsia chinensis (Link)] explants in vitro. Eur. J. Hort. Sci. 70, S278S282. Roy, D., Basu, N., Bhunia, A., Banerjee, S.K., 1993. Counteraction of exogenous L-proline with NaCl in saltsensitive cultivar of rice. Biol. Plant 35, 6972. Sakamoto, A., Murata, N., 1998. Metabolic engineering of rice leading to biosynthesis of glycinebetaine and tolerance to salt and cold. Plant Mol. Biol. 38, 10111019. Sakamoto, A., Murata, N., 2002. The role of glycinebetaine in the protection of plants from stress: clues from transgenic plants. Plant Cell Environ. 25, 63171. Saneoka, H., Nagasaka, C., Hahn, D.T., Yang, W.J., Premachandra, G.S., Joly, R.J., et al., 1995. Salt tolerance of glycinebetaine-deficient and -containing maize lines. Plant Physiol. 107, 631638. Shabala, S., Cuin, T.A., 2008. Potassium transport and plant salt tolerance. Physiol. Plant. 133, 651669. Shabala, S., Pottosin, I.I., 2010. Potassium and potassium-permeable channels in plant salt tolerance. In: Demidchik, V., Maathuis, F. (Eds.), Ion Channels and Plant Stress Responses, Signaling and Communication in Plants. Springer Verlag, Berlin/Heidelberg, pp. 87110. Silva-Ortega, C.O., Ochoa-Alfaro, A.E., Reyes-Aguero, J.A., Aguado Santacruz, G.A., Jimenez-Bremont, J.F., 2008. Salt stress increases the expression of P5CS gene and induces proline accumulation in cactus pear. Plant Physiol. Biochem. 46, 8292. Singer, M.A., Lindquist, S., 1998. Multiple effects of trehalose on protein folding in vitro and in vivo. Mol. Cell 1, 639648.

References

403

Siringam, K., Juntawong, N., Cha-um, S., Kirdmanee, C., 2011. Salt stress induced ion accumulation, ion homeostasis, membrane injury and sugar contents in salt-sensitive rice (Oryza sativa L. spp. indica) roots under isosmotic conditions. Afr. J. Biotech. 10, 13401346. Sonnewald, U., 2001. Sugar sensing and regulation of photosynthetic carbon metabolism. In: Aro, E.M., Andersson, B. (Eds.), Advances in Photosynthesis and Respiration. Kluwer, Dordrecht, pp. 109120. Stoop, J.M.H., Williamson, J.D., Pharr, D.M., 1996. Mannitol metabolism in plants: a method for coping with stress. Trends Plant Sci. 1, 139144. Strizhov, N., Abraham, E., Okresz, L., Balickling, S., Zilberstein, A., Schell, J., et al., 1997. Differential expression of two P5CS genes controlling proline accumulation during salt-stress requires ABA and is regulated by ABA1, ABI1and AXR2 in Arabidopsis. Plant J. 12, 557569. Szabados, L., Savouré, A., 2010. Proline: a multifunctional amino acid. Trends Plant Sci. 15, 8997. ´ brahám, E., Cséplo, A ´ ., Rigo, G., Zsigmond, L., Csiszár, J., et al., 2008. Duplicated P5CS genes Székely, G., A of Arabidopsis play distinct roles in stress regulation and developmental control of proline biosynthesis. Plant J. 53, 1128. Tattini, M., Gucci, R., Romani, A., Baldi, A., Everard, D., 1996. Changes in non-structural carbohydrates in olive (Olea europaea) leaves during root zone salinity stress. Physiol. Plant 98, 117124. Tester, M., Davenport, R., 2003. Na1 tolerance and Na1 transport in higher plants. Ann. Bot. 91, 503527. Theerakulpisut, P., Bunnag, S., Kong-ngern, K., 2005. Genetic diversity, salinity tolerance and physiology responses to NaCl of Six rice (Oryza sativa L.) cultivars. Asian J. Plant Sci. 4, 562573. Tipirdamaz, R., Gagneul, D., Duhaze, C., Ainouche, A., Monnier, C., Ozkum, D., et al., 2006. Clustering of halophytes from an inland salt marsh in Turkey according to their ability to accumulate sodium and nitrogenous osmolytes. Environ. Exp. Bot. 57, 139153. Touchette, B.W., 2007. Seagrass-salinity interactions: physiological mechanisms used by submersed marine angiosperms for a life at sea. J. Exp. Mar. Biol. Ecol. 350, 194215. Trovato, M., Mattioli, R., Costantino, P., 2008. Multiple roles of proline in plant stress tolerance and development. Rend Lincei 19, 325346. Turan, S., Tripathy, B.C., 2012. Salt and genotype impact on antioxidative enzymes and lipid peroxidation in two rice cultivars during de-etiolation. Protoplasma 250, 209222. Urao, T., Yakubov, B., Satoh, R., Yamaguchi-Shinozaki, K., Seki, M., Hirayama, T., et al., 1999. A transmembrane hybrid-type histidine kinase in Arabidopsis functions as an osmosensor. Plant Cell 11, 17431754. Verbruggen, N., Hermans, C., 2008. Proline accumulation in plants: a review. Amino Acids 35, 753759. Wang, W., Vinocur, B., Altman, A., 2003. Plant responses to drought, salinity and extreme temperatures: towards genetic engineering for stress tolerance. Planta 218, 114. Wang, W.-B., Kim, Y.-H., Lee, H.-S., Kim, K.-Y., Deng, X.-P., Kwak, S.-S., 2009. Analysis of antioxidant enzyme activity during germination of alfalfa under salt and drought stresses. Plant Physiol. Biochem. 47, 570577. Wu, H., Shabala, L., Barry, K., Zhou, M., Shabala, S., 2013. Ability of leaf mesophyll to retain potassium correlates with salinity tolerance in wheat and barley. Physiol. Plant 149, 515527. Yamada, M., Morishita, H., Urano, K., Shiozaki, N., Yamaguchi-Shinozaki, K., Shinozaki, K., et al., 2005. Effects of free proline accumulation in petunias under drought stress. J. Exp. Bot. 56, 19751981. Yan, H., Gang, L.Z., Zhao, C.Y., Guo, W.Y., 2000. Effects of exogenous proline on the physiology of soyabean plantlets regenerated from embryos in vitro and on the ultrastructure of their mitochondria under NaCl stress. Soybean Sci. 19, 314319. Yancey, P.H., Clark, M.E., Hand, S.C., Bowlus, R.D., Somero, G.N., 1982. Living with water stress: evolution of osmolyte systems. Science 217, 12141222. Yang, S.X., Zhao, Y.X., Zhang, Q., He, Y.K., Zhang, H., Luo, D., 2001. HAL1 mediate salt adaptation in Arabidopsis thaliana. Cell Res. 11, 142148.

404


Yang, X., Lu, C., 2005. Photosynthesis is improved by exogenous glycinebetaine in salt-stressed maize plants. Physiol. Plant 124, 343352. Yasseen, B.T., Abu-Al-Basal, M.A., 2008. Ecophysiological of Limonium axillare and Avicennia marina from the coastline of Arabian Gulf-Qatar. J. Coastal Conserv. Plann. Manag. 12, 3542. Yokoi, S., Bressan, R.A., Hasegawa, P.M., 2002. Salt stress tolerance of plants. Japan International Research Centre for Agricultural Sciences (JIRCAS) Working Report. 2533. Yoshiba, Y., Kiyosue, T., Katagiri, T., Ueda, H., Mizoguchi, T., Yamaguchi Shinozaki, K., et al., 1995. Correlation between the induction of a gene for Δ1-pyrroline-5-carboxylate synthetase and the accumulation of proline in Arabidopsis thaliana under osmotic stress. Plant J. 75, 751760. Zhang, G., Chen, M., Li, L., Xu, Z., Chen, X., Guo, J., et al., 2009. Overexpression of the soybean GmERF3 gene, an AP2/ERF type transcription factor for increased tolerances to salt, drought, and diseases in transgenic tobacco. J. Exp. Bot. 60, 37813796. Zhang, L., Xi, D., Li, S., Gao, Z., Zhao, S., Shi, J., et al., 2011. A cotton group C MAP kinase gene, GhMPK2, positively regulates salt and drought tolerance in tobacco. Plant Mol. Biol. 77, 1731. Zhao, Y., Aspinall, D., Paleg, L.G., 1992. Protection of membrane integrity in Medicago sativa L. by glycinebetaine against the effects of freezing. J. Plant Physiol. 140, 541543. Zhifang, G., Loescher, W.H., 2003. Expression of a celery mannose 6-phosphate reductase in Arabidopsis thaliana enhances salt tolerance and induces biosynthesis of both mannitol and a glucosyl-mannitol dimer. Plant Cell Environ. 26, 275283. Zhu, J.K., 2000. Genetic analysis of plant salt tolerance using Arabidopsis. Plant Physiol. 124, 941948. Zhu, J.K., 2002. Salt and drought stress signal transduction in plants. Annu. Rev. Plant Biol. 53, 247273. Zhu, J.K., 2003. Regulation of ion homeostasis under salt stress. Curr. Opin. Plant Biol. 6, 441445. Zhu, J.K., 2007. Plant Salt Stress. In: O’Daly, A. (Ed.), Encyclopedia of Life Sciences. John Wiley and Sons, Ltd., New York, pp. 13. Zidan, M.A., Al-Zahrani, H.S., 1994. Effect of NaCl on the germination of seedling and some metabolic changes in Sweet Basil (Ocimum basilicum). Pak. J. Sci. Ind. Res. 37, 541543.

CHAPTER

Osmolyte Dynamics: New Strategies for Crop Tolerance to Abiotic Stress Signals

17

Resham Sharma, Renu Bhardwaj, A.K. Thukral, Neha Handa, Ravdeep Kaur and Vinod Kumar

17.1 Introduction Constantly fluctuating climate and abiotic stresses, such as water deficit, temperature variations, extreme soil salinity, and heavy metal and pesticide toxicity, are serious threats to normal plant growth and development; they are the cause of major crop productivity losses across various geographic zones worldwide (Osakabe et al., 2013, Chamoli and Verma, 2014). Adding to this, modern agricultural practices including monoculturing and excessive use of chemical fertilizers, herbicides, and pesticides end up as perils rather than assets; this is because they persist as xenobiotics that harm delicate ecological components, resulting in more damage than protection (Damalas et al., 2011; Abro et al., 2013; Costa et al., 2014). Understandably, agrarian economies need to develop crop plants tolerant to such environmental stresses for normal growth and balanced functioning. For this reason, genes responsible for active expression of antioxidants, enzymes, osmoprotectants, transporters, and so on have been identified and expressed in the past decade with a very high frequency (Krasensky and Jonak, 2012). By adopting this commendable method, development of transgenic plants through target genetic engineering and exogenous application of osmoprotectants is being achieved (Chen et al., 2014). Another strategy is the application of chemicals and phytohormones (e.g., nitrous/nitric oxide, salicylic acid, polyamines, brassinosteroids, cytokinins) to increase osmoprotectant expression in crop plants (Duque et al., 2013; Farooq et al., 2013). The novelty of osmoprotectants is their ability to maintain ionic and turgor balances in plant cells, and their heightened accumulation under stress followed by degradation when optimum conditions are achieved (Pinto-Marijuan and Munné-Bosch, 2013). This characteristic feature needs to be introduced into plant species that do not naturally possess them when exposed to abiotic stress. As depicted in Figure 17.1, recent studies indicate that it is better to lump all transgenic and RNA-sensing classes of crop development strategies into what is called “omics”; these include fields such as genomics, transcriptomics, metabolomics, and others. This allows researchers to get a better grasp of gene expression, protein modification, and metabolite composition technologies for osmoprotectants that highlight abiotic stress responses in crops (Urano et al., 2010; Silva et al., 2011). This chapter is an effort to cover the different roles played by

P. Ahmad (Ed): Emerging Technologies and Management of Crop Stress Tolerance, Volume 2. DOI: http://dx.doi.org/10.1016/B978-0-12-800875-1.00017-X © 2014 Elsevier Inc. All rights reserved.

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CHAPTER 17 Osmolyte Dynamics: New Strategies for Crop Tolerance

Temperature

Pesticides

Heavy metals

Exogenous application of osmolytes

Crop plants under abiotic stress

Water deficit

Salinity

Exogenous Gene induction OMICS application of for osmolytes in (To understand phytohormones non-accumulators osmotic to induce osmolytes (Transgenic approach) responses) Plant conditioning and breeding (Resistant/high yielding crop varities)

FIGURE 17.1 Major crop rescue strategies via osmoprotectant activation under abiotic stresses.

osmoprotectants in various plant stress adaptations and the possibility of crop improvement, as well as the degree of effectiveness achieved by promoting stress tolerance using these methods.

17.2 Osmoprotectants in plants Osmoprotectants or compatible solutes are tiny molecules that make osmotic adjustments between the cell’s surroundings and its cytoplasm; they are selectively released from the protein interface as a result of their tendency to form hydrophilic complexes that in turn stabilize stress inducers (Lang, 2007; Krasensky and Jonak, 2012). To enhance the stress-remediating potential of osmolytes, their engineering into plant genomes has long been considered as one successful approach to apply for normal plant physiological functioning and crop improvement under extreme conditions (Rathinasabapathi, 2000; Rontein et al., 2002)., The three major classes of osmoprotectants in plants that have been reported are briefly discussed in the following subsections.

17.2.1 Sugars and polyols Sugars, mainly composed of complex saccharides and sugar alcohols or polyols (highly soluble, sixcarbon, nonreducing sugars with 2OH groups), are the major classes of essential biomolecules that act as structural components and signaling and transport molecules (Noiraud et al., 2001). They are widely discussed as compatible solutes or osmoprotectants and antioxidants under various abiotic stresses and are known to provide innate immunity to plants as well (Moghaddam and Ende, 2012; Kido et al., 2013). Polyols (e.g., mannitol, inositol, glycerol, ribitol) play similar roles due to the presence of hydroxyl groups that form hydration spheres around macromolecules, prohibiting their metabolic inactivation under osmotic stress (Williamson et al., 2002; Janska et al., 2010). Their protective roles in plants are described next.

17.2 Osmoprotectants in plants

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17.2.1.1 Fructans Fructans are water-soluble storage oligosaccharides primarily consisting of fructose units synthesized in plant vacuoles that act as compatible solutes (Valluru and Van den Ende, 2008). Depending on the linkage between fructosyl residues and the spatial arrangement of glucose residues, the fructans are divided into five major categories as shown in Figure 17.2. Fructosyl transferases (FTs) catalyze synthesis of fructans by transferring fructose units from sucrose to a growing fructan chain, followed by incorporation of FTs back into fructans (Krasensky and Jonak, 2012). Fructans accumulate under abiotic stresses, stabilizing cell and organelle membranes and preventing electrolytic leakage of water molecules across them (Peshev et al., 2013; Ahanger et al., 2014). They achieve this by inserting a part of the polysaccharide chain in between the phospholipid mono- and bilayers, thereby fortifying the membranes and acting as effective cryoprotectants (Livingston et al., 2009; Bhandari and Nayyar, 2014; Swati Megha and Basu, 2014).

17.2.1.2 Raffinose family oligosaccharides Raffinose family oligosaccharides (RFOs) are a group of soluble, nonreducing trisaccharide sugars (e.g., raffinose, stachylose, verbascose, and ajugose) that are actively accumulated under drought and dehydration in plants (Palma et al., 2014; Pirzadah et al., 2014). Raffinose exists ubiquitously while stachylose and other highly polymerized RFOs (e.g., verbascose and ajugose) exist in the vacuoles of certain plants (El Sayed et al., 2013). The first step toward their synthesis is formation of galactinol from myo-inositol and uridine diphosphate galactose in the presence of galactinol synthetase. Galactinol Synthetase

UDP 2 Galactose 1 Myo-inositol ! Galactinol 1 UDP 1 H1 This is followed by donation of galactosyl moiety to sucrose and raffinose in the case of raffinose and stachylose synthesis, respectively (Van den Ende, 2013). The same as fructans, RFOs generally act as storage and transport carbohydrates in plants. Expression of galactinol and RFOsynthesizing enzymes elevates during the oxidative burst in plants due to various environmental stresses, which in turn raises endogenous RFOs and galactinol levels (Nishizawa-Yokoi et al., 2008). Numerous reports have been cited for RFO accumulation during salinity, drought, and

Fructans

Inulin type, e.g., asteraceae

Levan type, e.g., poaceae

Branched, e.g., cereals

Inulin neoseries, e.g., asparagus, agave

Levan neoseries, e.g., oats, lolium

FIGURE 17.2 Classification of fructans. Source: Modified from Livingston et al. (2009).

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temperature stress in plants (Kempa et al., 2007; Peters et al., 2007; Usadel et al., 2008; Kim et al., 2010; Gangola et al., 2013). Like fructans, RFOs function as osmoprotectants by acting as phloemmobile signaling compounds, stabilizing membranes and scavenging reactive oxygen species (ROS) (Nishizawa et al., 2008; Conde et al., 2011; Van den Ende, 2013).

17.2.1.3 Trehalose Trehalose is a nonreducing disaccharide that accumulates in bacteria, algae, fungi, yeast, invertebrates, and some resurrection plants in response to drought, salinity, temperature variations, and heavy metal stresses (Jang et al., 2003; Cortina and Culianez-Macia, 2005). Trehalose contains two glucose units that are linked by α, α-1, and 1-glycosidic bonds (Redillas et al., 2012). It is synthesized from glucose6-phosphate and uridine diphosphoglucose in a two-step process. The first step is catalyzed by the enzyme trehalose phosphate synthetase (TPS), resulting in the formation of trehalose-6-phosphate that is further catalyzed by trehalose-6-phosphate phosphatase to trehalose (Penna, 2003). It protects proteins and membranes against denaturation and membrane fusion in stressed plants (Iturriaga et al., 2009). Incorporation of trehalose biosynthetic genes (TPP and TPS) from microbes into transgenic plants has been shown to increase accumulation of trehalose and other soluble sugars, providing increased resistance to several abiotic stresses (Jang et al., 2003; Karim et al., 2007; Miranda et al., 2007; Iordachescu and Imai, 2008; Garg et al., 2012; Redillas et al., 2012).

17.2.1.4 Mannitol Mannitol is a reduced form of mannose that acts as a chemical chaperone under stress and is the most abundant polyol in plants. It is synthesized in vascular plants from mannose-6-phosphate by simultaneous action of nicotinamide adenine dinucleotide phosphate (NADPH)-dependent mannose-6-phosphate reductase (M6PR) and mannose-6-phosphate phosphatase (Conde et al., 2011). The NAD-dependent enzyme mannitol-1-phosphate dehydrogenase (mtlD) oxidizes mannitol back to mannose (Reis et al., 2012).

17.2.1.5 Myo-inositol Myo-inositol is a cyclic polyol containing cyclohexanehexol as its main component. It acts as a substrate for synthesis for the RFOs. Myo-inositols are synthesized in a two-step process, as follows: Step 1 L-myo-inositol 1-phosphate synthetase ðMIPSÞ D-glucose-6-P ! D-myo-inositolð1Þ-monophosphate Step 2 L-myo-inositol 1-phosphate phosphatase ðIMPÞ D-Myo-inositolð1Þ-monophosphate ! Myo-inositol Myo-inositol and its methylated derivatives (e.g., D-pintol and D-ononitol) accumulate in halophytes under salt stress (Sengupta et al., 2008). More recently, it was observed that myo-inositol derivatives regulate stress responses by serving as compatible solutes and signaling molecules (Kido et al., 2013).


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17.2.1.6 Sorbitol Sorbitol is one of the main photosynthetic end products and serves as a storage and transport sugar in most plant families (Li et al., 2012). Synthesis of sorbitol takes place by catalysis of glucose via NADP-dependent sorbitol-6-phosphate dehydrogenase (S6PDH). Sorbitol is further degraded to fructose by NAD1 sorbitol dehydrogenase in sink tissues (Liang et al., 2012). It plays an important role in osmotic adjustment in cell cytoplasm under various abiotic stresses such as salinity, chilling, and drought (Reis et al., 2012). Step 1 Sorbitol-6-phosphate dehydrogenase Glucose-6-phosphate ! Sorbitol-6-phosphate Step 2 Sorbitol-6-phosphate

Sorbitol-6-phosphatase

!

Sorbitol

Gao and coworkers (2001) found that transgenic Diospyros kaki Thunb. trees overexpressing sorbitol6-phosphate dehydrogenase had photosystem II that was affected less under salinity stress. Exogenous sorbitol application had positive effects on growth of salt-stressed plants and also reduced stress-induced H2O2 and MDA content in salt-sensitive rice seedlings (Theerakulpisut and Gunnula, 2012).

17.2.1.7 Glycerol Glycerol is a simple polyol with three hydroxyl groups. Its backbone is focal to all triglycerides. Many marine algae are known to accumulate glycerol under abiotic stresses (Rathinasabapathi, 2000). These are known to offer osmotic buffering and membrane protection (Ashraf and Foolad, 2007). Glycerol-stimulating genes have been incorporated into tobacco plants to counter abiotic stresses (Chamoli and Verma, 2014).

17.2.2 Amino acids, peptides, and amines Plants respond to environmental fluctuations via accumulation of various amino acids (e.g., asparagine, glycine, histidine, serine, peptides), glutathione and phytochelatins, and amines (e.g., spermine, spermidine, putrescine, nicotianamine, mugineic acid) (Less and Galili, 2008). These osmolytes are directly linked to metabolic pathways and help in regulation of cytosolic pH, ionic homeostasis, free radical removal and stabilization of organelles, and macromolecules such as protein complexes and membranes (Bray et al., 2000; Szabados and Savouré, 2010). Cysteine (Cys) is a sulfur-containing amino acid involved in synthesis of methionine, vitamins, and cofactors, and it is directly linked to osmoregulation in plants under stress (Anjum et al., 2012). Histidine (His) in its free form is a well-known metal chelator, especially for nickel because it has high-affinity and detoxification properties. By doing so, it maintains osmotic balance in the cells under stress (Kerkeb and Kramer, 2003). γ-Aminobutyric acid (GABA) is a well-known nonprotein amino acid involved in the carbonnitrogen metabolism, signaling, and osmotic adjustments (Sharma and Dietz, 2006; Seher et al., 2013).

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The foremost amino acid with the maximum reports for osmoprotectants under abiotic stress is proline (Mattioli et al., 2008). As the first osmoprotectant that accumulates in the cytoplasm in response to any abiotic stress and in addition to being an osmolyte, proline plays other important roles too: a signaling molecule, a metal chelator, an antioxidant defense molecule, and a buffering agent to control the redox potential across stressed cells (Ashraf and Foolad, 2007; Urano et al., 2010; Celik and Atak, 2012; Hayat et al., 2013). In plants, proline is synthesized by two pathways that involve glutamate and ornithine as precursor molecules. The glutamate pathway, as shown in Figure 17.3, is the major pathway for proline production during osmotic stress (Hayat et al., 2013; Rai and Penna, 2013). The ornithine pathway is activated mostly during seedling development (Figure 17.4) in some species of plants during stress-induced proline accumulation (Armengaud et al., 2004; Xue et al., 2009). Proline is synthesized from glutamate, which is converted to glutamate-1-semialdehyde by the action of the enzyme pyrroline-5-carboxylate synthetase (P5CS); in turn it is spontaneously converted to pyrroline-5-carboxylate (P5C), which is further converted to proline by the action of the enzyme P5C reductase (P5CR) (Turchetto-Zolet et al., 2009; Sharma and Vaslues, 2010; Liang et al., 2012). Proline levels were found to increase in many angiosperms under abiotic stress as reported by Mohammadkhani and Heidari (2008) and Sharma and coworkers (2011); the authors noted a positive relationship between proline accumulation and stress tolerance. This specific tendency of certain plants to accumulate proline was extolled and utilized further for crop plants that are not natural proline accumulators by using the transgenic approach and exogenous application techniques. These reports are discussed further later in the stress sections (Wang et al., 2012; Soshinkova et al., 2013; Xu et al., 2013; Surekha et al., 2014). The second most important class of osmoprotectants contains the polyamines (PA)—small aliphatic molecules involved in maintaining cellular pH—that are activated under drought and salinity stress (Macro et al., 2012). Another amino acid, 5-aminolevulinic acid (ALA), is involved in osmoprotection against cold stress and water deficit in many plants, and it has been used as an exogenous application for the same (Balestrasse et al., 2010; Korkmaz et al., 2010). Glutamate Pyrroline-5-carboxylate synthetase (P5CS)

Glutamatesemialdehyde (GSA) Spontaneously

Pyrroline-5carboxylate (P5C) Pyrroline-5-carboxylate reductase

Proline

FIGURE 17.3 Glutamate biosynthetic pathway.


411

Ornithine Ornithine delta aminotransferase

Transmination

Glutamatesemialdehyde

Pyrroline-5carboxylate (P5C)

Proline

FIGURE 17.4 Ornithine biosynthetic pathway.

17.2.3 Quaternary ammonium compounds Betaines are a group of osmotic protectants that are derivatives of amino acids containing fully methylated nitrogen atom. Glycine betaine (GB), proline betaine, β-alanine betaine, choline-O-sulfate, and 3-dimethylsulfoniopropionate are the most common types of betaines reported in stressed plants (Wani et al., 2013; Chen et al., 2014). Out of these, GB (N, N, N-trimethylglycine), which is a zwitter ion, is one of the most comprehensively studied compatible solutes. Its distribution is widely reported in bacteria, cyanobacteria, algae, fungi, animals, and many plant families (Chen and Murata, 2011). It plays an important role in maintaining cellular compatibility as well as osmoregulation in plant cells by absorbing water from the surroundings, leading to the maintenance of osmotic pressure (Giri, 2011). Two different pathways for GB biosynthesis have been recognized in living organisms as illustrated in Figure 17.5. In most microorganisms, plants, and animals, choline acts as a precursor molecule that is oxidized to form betaine aldehyde with the help of choline monooxygenase. Betaine aldehyde is further converted into glycine betaine via catalysis of betaine aldehyde dehydrogenase (Wargo, 2013). Another pathway with glycine as a precursor is reported in halophytic cyanobacteria Actinopolyspora halophila and Ectothiorhodospira halochloris (Nyyssola et al., 2000). In this three-step pathway, glycinesarcosine methyltransferase (GSMT) catalyzes the conversion of glycine to N-methylglycine (sarcosine); this is further converted to N, N-dimethylglycine via dimethylglycine methyltransferase (SDMT). The methylation occurring in the second step can also be catalyzed by GSMT. N, N-dimethylglycine formed at the end of the second step is methylated to glycine betaine only with the help of SDMT (Waditee et al., 2005). Because betaines play an important role in osmoregulation, their presence has been noted in chloroplasts, cytoplasm, and vacuoles (Chen and Murata, 2011). The same as in the case of other osmoprotectant classes, GB has been induced via transgenic technology and the exogenous approach in many nonaccumulating crop species to alleviate abiotic stresses without harming yield and quality (Joseph et al., 2013; Kaya et al., 2013).

412


COO– CH2

CH2OH CH2

H–N+–H

H3C–N+–CH3

H

CH3

Glycine

Choline SAM

2H++O+ 2Fd (reduced)

Choline monooxygenase

2H2O+ 2Fd (oxidized)

GSMT

SAH COO– CH2 H–N+–H

CHO CH2

CH3 N-methylglycine (sarcosine)

H3C–N+–CH3

SAM

CH3

SDMT

SAH COO– CH2

Betaine aldehyde

H–N+–CH3

NAD++H3O Betaine aldehyde dehydrogenase NADH++H+

CH3 N, N-dimethylglycine SAM

COO– CH2 H3C–N+–CH3 CH3 Glycine betaine

SDMT

SAH COO– CH2

H3C–N+–CH3 CH3 Glycine betaine

FIGURE 17.5 The two- and three-step biosynthetic pathways of glycine betaine with choline and glycine as the respective precursors. GSMT: glycinesarcosine methyltransferase; SDMT: sarcosine dimethylglycine methyltransferase; SAM: S-adenosylmethionine; SAH: S-adenosylhomocysteine.

17.3 Metabolic expression and exogenous application of osmoprotectants under abiotic stresses The basic strategies used by most plants in antistress mechanics involves activation of osmoregulatory molecular cascades that in turn trigger the perception and transduction of stress and the expression of specific stress-related genes and metabolites; this is the basic strategy most plants use as an antistress mechanism (Figure 17.6). Recent progress in metabolomic analyses in a model crop, Arabidopsis, indicated the critical understanding of possible metabolic fluctuations in crops under varying environmental conditions (Iwaki et al., 2013). Such a study corroborates previous work and pushes forward the concept of engineering osmoprotectant genes and exogenous application of osmolytes and phytohormones for enhancing tolerance to various abiotic stresses, as discussed in the next subsections.

17.3.1 Temperature stress Temperature stress manifests itself in crop plants at two diverse levels: injuries due to heat and chilling stresses. Because plants are sessile organisms, they lack the ability to move to optimum

17.3 Metabolic expression and exogenous application

Heat/ cold stress

Osmoprotectant gene

Water deficit

Heavy metals

Salinity stress

Pesticides

OSMOTIC IMBALANCE (Hindrance in osmotic and ionic homeostasis: damaging functional and structural proteins and membranes)

Isolation

Osmoprotectant gene

413

Osmoprotectant gene Isolation

SIGNAL PERCEPTION & TRANSDUCTION Osmosensor activation (e.g. AtHK1, P5CS, ADC etc)

Isolation

Sequential tagging and molecular structural studies for osmoprotectants

GENE ACTIVATION (Osmoprotectant biosynthetic pathway activation for sugars, polyols, amino acids, betaines etc.)

Osmoprotectant gene Isolation

Re-instatement of homeostasis, functional and structural protection of proteins, enzymes and membranes

Acquired stress tolerance

PLANT STRESS TOLERANCE

FIGURE 17.6 An overview of osmolyte activation via different strategies under various abiotic stresses in plants.

environments when faced with a sudden rise or drop in temperature; as a result, growth and development are hindered significantly (Lobell and Field, 2007; Wigge, 2013). All biochemical reactions are temperature sensitive from enzymatic activity to molecular expression, so it is imperative to cover losses caused to plants under temperature stress. High temperature (HT) is a threat to crop productivity, therefore it is necessary to sustain high-yielding yet resistant plants (Wahid and Close, 2007). Cold temperature (CT) stress includes chilling and freezing. HT and CT prevent the complete genetic expression of plants resulting in inhibition of metabolic reactions and induction of osmotic and oxidative stress (Chinnusamy et al., 2007). Because of this, the geographical occurrence of plants is restricted and huge losses in agricultural productivity are foreseen (Adam and Murthy, 2014). Endogenous osmoprotectants are involved in signal cascading and transcriptional control activation to counter these biochemical and physiological aberrations that are otherwise irreversible in many plants. However, current theories propose inducing them into

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nonosmoprotectant accumulators via transgenic technology or to counter oxidative stress by exogenous application of osmolytes and phytohormones as foliar sprays into plant tissue culture trials followed by field conditioning (Bita and Gerats, 2013; Hasanuzzaman et al., 2013). Transgenic induction confirmed the positive effects of proline gene overexpression during HT stress as transformed plants showed a negative leaf osmotic potential and increased xanthophyll accumulation (Dobra et al., 2010). Similarly, high glycine betaine (GB) contents were reported in maize and sugarcane (Quan et al., 2004; Wahid and Close, 2007) under HT. On the other hand, there are plant species (e.g., rice, mustard, tobacco) that are not natural GBsugar accumulators under HT; however, the transgenic approach allowed induction of the GBtrehalosefructanbiosynthetic pathways into them (Sakamoto and Murata, 2002; Quan et al., 2004). The Raffinose family oligosaccharides (RFO) were marked for desiccation tolerance in plant seeds. RFO contents were determined based on analysis of the genes involved in their biosynthesis. Extensive sugar analysis of RFO contents in Arabidopsis thaliana under CT revealed a huge amount of raffinose and galactinol accumulation in transgenic plants. Three stress-responsive galactinol synthase (GolS) genes (AtGolS1, 2, and 3) among seven Arabidopsis GolS genes were identified. Of these, AtGolS3 was found to be CT-induced (Taji et al., 2002). Tobacco cultivars were transformed so they can overaccumulate proline, fructans, and GB by incorporation of transgene constructs from Arabidopsis spp. and Vigna spp. genes (AtP5Cs and VacP5Cs) for D1pyroline-5-carboxylate synthetase production. The gene coding of Bacillus subtilis SacB for levansucrase and Arthrobacter globiformis codA for choline oxidase were also integrated and expressed in these tobacco plants; then they were subjected to subzero temperatures and osmotic interplays. Their subsequent CT-resistant progenies were established for stable transgenic line selection (Konstantinova et al., 2002). Levels of oxidative stress markers, such as leakage of electrolytes and osmoprotectant accumulation, were recorded for freezing stress. Control tobacco plants showed marked damage; however, transformed tobacco plants showed a lower extent of oxidative damage (Parvanova et al., 2004). Many recent reports on coldheat stress have noted a rise in the cellular levels of proline, GB, sugars, and sugar alcohols; these serve as cryoprotectants to protect cellular metabolism (Bhandari and Nayyar, 2014; Pirzadah et al., 2014; Sa˘glam and Jan, 2014). An interesting study of cold stress responses in two cultivated tomato varieties, Gerry (cold stress sensitive) and T47657 (moderately cold stress tolerant), found that exogenous GB induced the expression of lypoxygenase-13 (TomLOXF) and fatty acid desaturase 7 (FAD7) genes; this led to increased membrane stability and defense mechanisms via the octadecanoid pathway or lipid peroxidation products (Karabudak et al., 2014). This is still a very potential area for further research into temperature stress induction, it needs more review.

17.3.2 Water deficit Water deficit is one of the most common forms of abiotic stress leading to reduced plant productivity (Yadav et al., 2014). Relatively long durations of water scarcity may lead to premature senescence and plant death. Plants being sedentary by nature are subject to strong selection pressures for managing variations in water availability, which includes the increasing content of organic osmolytes such as GB, proline, and pinitol (Miller et al., 2010). Under water deficit, aspargine, proline, and valine levels increase significantly in Bermuda grass, wheat, potatoes, and hot peppers


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(Sairam et al., 2002; Kerkeb and Kramer, 2003; Knipp and Honermeier, 2006; Anjum et al., 2012). Increased proline content and escalated expression of P5CS1 in transgenic Arabidopsis spp. was also recorded (Mattioli et al., 2008, 2009; Lehmann et al., 2010). Additionally, reports exist for the involvement of proline in boosting of antioxidant enzyme activity (Khedr et al., 2003; Campos et al., 2011). Plant tolerance to water stress has been determined by various biochemical pathways that cause the acquisition or retention of water, protection of chloroplast function, and maintenance of ion homeostasis (Shinozaki and Yamaguchi-Shinozaki, 2007). Biosynthesis of both polyamines and compatible osmolytes (e.g., betaines, proline, and sugars) increases under water stress (Yang et al., 2007; Kubis, 2003, 2008). In some cases, the suppression of proline biosynthesis in transgenic plants resulted in increased sensitivity to water stress (De Ronde et al., 2000). Water deficit in transgenic tobacco resulted in overexpression of proline biosynthesis enzymes (Roosens et al., 2002). Similarly, soluble sugars in arbuscular mycorrhizal plants act as osmoprotectants by providing stability to plant organelles under water deficit (Auge, 2001; Porcel and RuizLozano, 2004). In addition, soluble sugar content in arbuscular mycorrhizal associated Erythrina variegata (Monoharan et al., 2010) and Casuarina equisetifolia (Zhang et al., 2010) seemed to decrease oxidative damage linked to water stress. The enhancement of soluble sugars in the leaves of arbuscular mycorrhizal associated Citrus tangerine plants was reported under water stress by 1.37-fold to that of well-watered control plants (Wu and Xia, 2006). As discussed earlier, GB is a well-known osmoprotectant involved in the protection of proteinenzymatic activities under water stress and results in the stabilization of membranes during freezing (Subbarao et al., 2001; Xing et al., 2010). Thus, induction of GB biosynthetic genes to overexpress in plants is a commonly practiced adaptive strategy. When transformation of heterologous P5CS into the high proline-producing species of citrus (B100 μmol g21 of leaf dry weight) was done, Molinari and coworkers (2004) found that the transformed plants contained 8-fold more proline than the nontransformed plants; this resulted in an osmotic adjustment and maintenance of pressure potential under water stress. In sugarcane, GB and other osmolytes and soluble sugars play a major role in osmotic adjustment and act as oxidative damage shields for managing water stress (Wahid, 2004; Gandonou et al., 2006; Patade et al., 2008). Overexpression of the trehalose-6phosphate synthase gene OsTPS1 in transgenic rice revealed an increased tolerance to abiotic stresses compared to control plants (Li et al., 2011). Similarly, exogenous application of trehalose in maize plants alleviated drought resistance by up-regulating growth, photosynthetic and water relations, as well as antioxidant defense mechanisms (Ali and Ashraf, 2011; Theerakulpisut and Gunnula, 2012). IMT (myo-inositol methyltransferase) cDNA from Glycine max was isolated and, via RT-PCR analysis, it was revealed that GmIMT transcripts were induced by both drought and salinity stress in soybean seedlings (Ahn et al., 2011). Recently, in response to water deficit stress, transgenic Arabidopsis plants were marked for an increase in galactinol and raffinose concentrations resulting in a better ROS scavenging capacity (El Sayed et al., 2013). Under conditions of normal water supply and water stress, the isoforms of three antioxidant enzymes (i.e., APX, GR, and CAT) were differentially regulated in leaves of transgenic Swingle citrumelo plants with enhanced endogenous proline accumulation. Findings indicated that proline also caused a 2-fold increase in transcription activity of the genes—CAT2, APX1, APXcl, and cu/znSOD2—involved in antioxidant enzyme generation under water stress (Carvalho et al., 2013). Another report indicated a vacuolar H1-pyrophosphatase gene in the wheat genome

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(TaVP) with an expression that is up-regulated under drought stress and linked to sugar hyperaccumulation as a subsidiary response in targeted plant cells (Li et al., 2014b). Cumulatively, these reports convey that osmolytes are instrumental in protecting plants, especially at times of water deprivation.

17.3.3 Salinity stress Salinity stands for hyper salt accumulation in soils beyond the tolerance limits for most plants and approximately 20% of the world’s total irrigated agricultural land suffers from poor yield due to high salt content (Selvakumar et al., 2014). Salt stress affects crops under extreme saline conditions by severely impairing plants’ metabolism due to osmotic stress and loss of turgor. One of the mechanisms adopted by plants to tolerate salt stress is the accumulation of compatible solutes that help maintain osmotic homeostasis (Gill et al., 2014). Salinity stress has a marked effect on sugar and polyol accumulation. In different genotypes of seashore paspalum, sugars (e.g., glucose, sucrose, and myo-inositol) increased due to salinity stress while mannitol and sorbitol showed no effect (Lee et al., 2008). Under extreme salt stress, the accumulation of asparagine, arginine, serine, and glycine was reported in Coleus blumei Benth, Spinacia oleracea, and Oryza sativa (Martino et al., 2003; Summart et al., 2010). Sugar and starch accumulation was also reported in Solanum lycopersicum plants (especially fruits) subjected to a 160 mM concentration of NaCl stress (Yin et al., 2010). Mannitol overexpressing the M6PR gene from celery was induced in Arabidopsis, and it elevated the expression of other stress-inducible genes as well. The M6PR gene increased salt tolerance in Arabidopsis by lowering salt injury, minimizing vegetative growth inhibition, and enhancing seed production as compared to wild-type plants (Chan et al., 2011). Further study substantiated the up-regulation of the expression of a sucrose transporter in leaves and enhanced activity of ADP-glucose pyrophosphorylase (AGPase) in fruits. AGPase is responsible for catalysis of the synthesis of ADP-glucose from glucose-1-phosphate and ATP. Bread wheat cv. Giza 163 was made salt-tolerant by transforming the mtlD gene (encoding mannitol-1-phosphate dehydrogenase) of E. coli (Ramadan et al., 2013). It has been observed that expression of mannitol in the transgenic plant led to enhanced grain yield in plants treated with salt (NaCl and CaCl2). Other reports indicate that the fructose, glucose, and galactronic acid content increased significantly while sorbitol, mannose, and galactose levels decreased. PcINO1 gene coding for L-myo-inositol-1-phosphate synthase (MIPS) from a halophytic variety of wild rice tolerant to salinity was induced into cultivated mustard and tobacco plants. The resulting transgenic plants showed increased salt tolerance and less oxidative damage with inositol accumulation in both roots and shoots. The yield and crop quality of transgenic plants remained uncompromised and the plants were able to grow stably, set seeds, and germinate in saline environments (Das-Chatterjee et al., 2006). Amino acids are also very sensitive to changes in salt concentrations in the soil. Proline is one of the most sensitive amino acids that accumulates in the cytosol and vacuoles in response to salt stress and offers protection against the damaging effects of 1O2 and 2OH by binding to redoxactive metal ions (Miller et al., 2010). Its increase was reported in two varieties of rice cultivars subjected to increasing NaCl concentrations (Demiral and Tu¨rkan, 2005). A marked increase in the concentration of proline was also observed in Trachyspermum ammi (L.) Sprague in response to NaCl stress (Ashraf and Orooj, 2006).


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A study conducted on two cultivers of salt-stressed Sesamum indicum showed an enhanced level of proline accumulation at the highest salt concentration in salt-tolerant cultivars; this suggested its important role in maintaining plant homeostsis (Koca et al., 2007). Similar results have been reported in Paspalum vaginatum where proline content was enhanced significantly in response to stress and was documented to be a major osmolyte for maintaining osmotic homeostasis in a variety of plant genotypes (Lee et al., 2008). Proline metabolism is also affected by salt stress. The activities of the enzymes involved in its metabolic pathways are reported to be altered to significant levels, leading to enhancement of proline accumulation in plants. Metabolic enzymes were analyzed in Oryza sativa subjected to salt stress and the authors found that the activities of the proline synthesizing enzymes (i.e., P5CS, P5CR, and ornithine-δ-aminotransferase) were increased while it decreased in proline hydrolysis enzyme proline dehydrogenase (PDH) (Bagdi and Shaw, 2013). Similar results have been reported in a study carried out on cell suspension cultures of Cucumis sativus treated with NaCl. Two types of cell cultures (i.e., acclimated and nonacclimated) were maintained. The activities of P5CS and P5CR were enhanced and PDH was reported to decline in both types of cultures. Naliwajski and Skłodowska (2014) also noted that proline content in the cultures increased significantly and acclimated cultures responded to the stress quickly. In another study carried out on Helianthus tuberosus L. by Huang et al. (2013), the effect of salt stress was observed on activities of biosynthetic enzymes and accumulation of proline. The authors found that roots, stems, and leaves of plants accumulated significant amounts of proline and reported that activities of the enzymes involved in the glutamate pathway were high in response to stress. However, those involved in the ornithine pathway and proline catabolism decreased significantly thereby indicating that the glutamate pathway is the major process activated during salt stress tolerance. Exogenous application of proline also has been reported to have a protective effect on stressed plants. Cucumis melo was subjected to 150 mM NaCl alone and in combination with 10 mM of proline. Kaya et al. (2007) observed that proline was instrumental in ameliorating the adverse effects of salt on growth, fruit yield, and other physiological parameters. A similar investigation on a saltsensitive variety, “Jinchun No. 2” of Cucumis sativus, was done by Huang and coworkers (2009). Stress was given in the form of NaCl (100 mM) and a significant change in dry weight; leaf relative water; malondialdehyde; content of K1, Na1, Cl2; and enzymes was observed. Foliar application of proline (25 ml per plant) was effective in alleviating stress and enhanced the tolerance of plants to saline conditions. Glycine betaine content was found to increase in the two cultivars of Beta vulgaris L. when exposed to saline conditions (Subbarao et al., 2001). NaCl treatment was given to plants and GB content was correlated with the amount of Na1 in the leaves, thereby indicating that salinity may be one of the factors prompting synthesis of GB in plants. Similar results have been reported by Kumar and his companions (Kumar et al., 2003) in two cultivars of Morus alba L. where the salttolerant variety was able to accumulate more betaines compared to the salt-sensitive variety; this suggests the protective role of this osmolyte. Atriplex nummularia and Atriplex semibaccata are two highly salt-tolerant plant species and were studied for the genetic basis for GB biosynthesis when subjected to high concentrations of salt (Joseph et al., 2013). The authors identified and analyzed choline monooxygenase and betaine aldehyde dehydrogenase, two enzymes involved in GB biosynthesis. They found that the expressions of both the genes encoding these enzymes were significantly up-regulated in leaf tissues and accumulated a high level of GB in both species. Exogenous application of GB to plants also enhances the defense system against salt stress. Maize

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plants subjected to NaCl stress were treated with different concentrations of GB. The plants showed higher resistance to salt stress by enhancing the activities of antioxidative enzymes and increasing pigment content. Exogenous application of GB also enhanced the endogenous GB levels, thereby highlighting its ameliorative effect (Nawaz and Ashraf, 2010). A similar study conducted by Hu et al. (2012) on Lolium perenne also confirmed the role of GB as a stress protectant. The plants were subjected to NaCl stress and application of GB to them significantly enhanced growth, relative water content, transpiration rate, pigment content, and activities of the antioxidative enzymes. The same study confirmed the role of GB in maintaining the cellular homeostasis and K1Na1 ratio. In another study carried out on salt-stressed maize treated with GB exogenously, Kaya et al. (2013) reported that foliar application fortified the antioxidative defense system of the plants and alleviated the detrimental effects of salinity. Glycine betaine has also been reported to be instrumental in affecting Ca21 signaling in stressed plants. GB pretreated tobacco plants when subjected to NaCl stress showed Ca21 efflux in epidermal cells of root; however, after 24 h of treatment, Ca21 influx was observed. The study concluded that GB induced an increase in free Ca21 ion concentration and enhanced expression of calmodulin and heat shock transcription factors in the cells, leading to increased levels of heat shock proteins (Li et al., 2014a). Transgenic studies conducted with plants also confirmed the importance of GB in salt tolerance and the technique has been successfully applied to various crops to obtain stress-resistant varieties. Usually, the genes engineered in the plants are those that encode the enzymes involved in the biosynthetic pathway. Solanum lycopersicum plants, when engineered with genes encoding betaine aldehyde dehydrogenase and choline oxidase, showed tolerance to salt stress in both seedling and mature phases (Zhou et al., 2007; Goel et al., 2011). These two genes were also reported to be introduced in S. tuberosum thereby enhancing the plant’s ability to resist oxidative, salt, and drought stresses (Ahmad et al., 2008; Zhang et al., 2011). Similarly, He et al. (2010) transformed the choline dehydrogenase endcoding gene betA in Triticum aestivum, an important enzyme in the biosynthetic pathway of GB. The authors observed that transgenic plants had a higher content of GB and showed higher germination, vigorous growth, and more photosynthesis rates under high salt concentrations. In another study, Medicago sativa plants were observed to grow vigorously under salt stress compared to wild types when a gene encoding betaine aldehyde dehydrogenase was transformed (Liu et al., 2011). Thus, GB may be of vital importance not only in normal cellular functioning but also as a stress protectant to aid in enhancing the tolerance of plants to stress. Additionally, many compounds, including some phytohormones, when applied exogenously alleviate plants’ stress from salt by increasing endogenous osmolyte accumulation (Iqbal et al., 2014). Nitric oxide (NO) helps in the maintenance of osmoregulation and ion homeostasis under salinity stress, as discussed in Farooq et al. (2013). Exogenous application of 24-epibrassinolide (EBL) on a Pusa Basmati-1 variety of rice under NaCl stress showed an improvement in proline content compared to the control plants (Sharma et al., 2013).

17.3.4 Heavy metal stress Proline, betaines, and soluble sugars are the main osmolytes reported to accumulate in crop plants growing in soils laden with heavy metals. Currently, the significance of multiple transcription factors, proteinenzyme complexes involved in osmolyte production, and osmolyte-induced specific


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gene expression in plant tolerance is a hotbed for global research (Bhardwaj et al., 2014). Early reports indicated proline to be the first accumulated osmoprotectant in response to Cd, Cu, and Zn stress in crop plants such as sunflower, wheat, and rice (Chen et al., 2001). Similarly, proline levels were found to rise in Anethum graveolens, Brassica juncea, Cynara scolymus, and Plantago psyllium under Cd, Cu, and Pb stress (Karimi et al., 2012; Aghaz et al., 2013; Mohammadi et al., 2013). Co, Cu, and Fe toxicity led to escalated GB accumulation in addition to activated antioxidant enzymes in plants (Chen and Murata, 2011; Dhir et al., 2004, 2012). A significant increase in proline, GB, and total sugar levels was observed in response to Cd, Cu, Cr, and Zn exposure in plants such as Brassica juncea L., Lactuca sativa, Salvinia natans, and Solanum lycopersicum (Aly and Mohamed, 2012; Dhir et al., 2012; Handa et al., 2013; Hashem et al., 2013; Muslu and Ergun, 2013; Sharma et al., 2013c). However now, osmolyte expressions via genetic engineering, as well as exogenous application formats, clearly symbolize their contribution to water adjustments and antioxidant induction at microcellular levels under heavy metal stress. The osmolyte-centered proteomic and metabolomic approaches are quickly evolving as significant tools to determine plants’ responses to various external stimuli including heavy metal stress (Rodziewicz et al., 2014). Earliest indications revealed metal induced proline accumulation and its protective role in transgenic plants and algae (Sharma and Dietz, 2006). Transgenic Chlamydomonas reinhardtii expressing P5CS isolated from moth bean accumulated 80% more proline than the wild type under Cd toxicity (Siripornadulsil et al., 2002). Transgenic Oryza sativa cultivar overexpressing the betaine synthesis gene BADH showed improved Cd tolerance compared to nontransgenic cultivars (Shao et al., 2008). Exogenous application of proline and GB to mung bean and tomato cultivars under Cd stress fortified the antioxidative defense mechanisms and reduced Cd-associated toxicity (Islam et al., 2009; Duman et al., 2010; Hossain et al., 2010). Similarly, exogenous application of trehalose was found to enhance Cd accumulation and an increase in antioxidative activity in duckweed (Duman et al., 2010). More recently, proline as a foliar spray was reported to alleviate Cd toxicity in Cicer arietinum by boosting its growth, photosynthetic attributes, yield, and the activity of the essential photosynthetic enzyme, carbonic anhydrase (Hayat et al., 2013). Exogenously applied GB effectively countered heavy metal toxicity in Triticum aestivum L. by enhancing root shoot length, biomass, photosynthetic pigments, and Na1 and K1 ion levels (Bhatti et al., 2013). Exogenous abscisic acid (ABA) when applied to leaves of Atractylodes macrocephala under Pb toxicity led to enhanced soluble sugar levels indicating osmolytic oxidative damage control compared to the control plants (Wang et al., 2012).

17.3.5 Pesticide toxicity It is amply clear that osmoprotectants are well documented for their role in water, salt, and temperature stress, but their importance in pesticide stress still remains to be explored thoroughly. Most studies have indicated the active accumulation of proline under pesticide stress in lower plants, and now this concept is being considered for higher crop plants as well. Cyanobacteria species have been studied extensively in this regard because they are effective “biofertilizers” and are often used for maintenance of fertility in many crop plants (e.g., rice) belonging to the food grain group. Three cyanobacterial species (i.e., Aulosira fertilissima, Anabaena variabilis, and Nostoc muscorum) were subjected to endosulfan toxicity and this led to a considerable rise in total proline content

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levels (Kumar et al., 2008). Another pertinent study pointed out the effect of pesticide stress on rising proline activity in cells of Anabaena variabilis. Under altered endosulfan treatments, the intracellular proline concentration was found to show a steady linear increase, indicating its free radical scavenging role (Syiem and Nongrum, 2011). The importance of endogenous and exogenous osmolyte accumulation and application was studied in Anabaena variabilis under the effect of varying concentrations of malathion. A marked increase in the endogenous levels of proline, sucrose, mannitol, trehalose, and glycogen was reported. Next, the effect of these osmolytes as exogenous sprays was recorded for growth and antioxidant enzyme activity in A. variabilis under malathion exposure. Interestingly, these exogenous osmolytes seemed to provide an additional protection, with the order of magnitude being trehalose . glycogen . sucrose . mannitol . proline (Ningthoujam et al., 2013). Similar results were reported by Manikar and coworkers (2013) for the role of osmoprotectants in reducing oxidative stress in combination with antioxidative enzymes, again in A. variabilis exposed to malathion. However, the focus is now shifting toward osmoprotectant interplay in crop plants under pesticide stress and the most pertinent reports for the same follow. Tomato and brinjal are well known to be highly susceptible to insect attacks so to ensure a good yield and less economic losses, heavy doses of chloropyrifos and malathion are applied to crop plants, leading to xenobiotic pollution and ROS generation; this, ultimately, causes cellular damage and plant death. Both pesticides significantly stimulated antioxidant and osmolyte activity (Mahnaz et al., 2011). A more site-specific study was done for selected osmoprotectant contents (i.e., proline, total amino nitrogen, and soluble sugars) in three crop plants—turnip, tomato, and lettuce—when irrigated with pesticide- and fertilizer-laden industrial wastewater of the El-Amia drain in Egypt. Notably, steady escalation in the activities of antioxidant enzymes, glutathione, proline, soluble sugars, and total amino nitrogen content was seen in response to irrigation with the pesticide-rich wastewater (Hashem et al., 2013). Increased proline accumulation was seen in response to exogenous application of 24-epibrassinolide under the stress induced in rice by neonicotinoid and imidacloprid (Sharma et al., 2013a). As far as the prospects of inducing the expression of osmoprotectant genes in crop plants against pesticide stress is concerned, the area is very nascent and needs pioneering efforts based on its marketing as an effective agricultural practice to reduce yield and economic losses.

17.4 Conclusion and future prospects Crop plants, the same as other plant classes, exhibit a large variety of protection mechanisms in response to abiotic stresses, often at the expense of their yield and performance. However, numerous reports indicate that osmoprotectant generation and accumulation is a novel, noninterfering mechanism against the deleterious effects of stresses while keeping quality and performance damage at bay. Recent studies show that the molecular and metabolic response of plants to a combination of abiotic stresses is the most unique and can be enhanced by inducing the expression of osmolyte synthetic genes for reducing huge losses to the agricultural sector worldwide. Additionally, exogenous application of foliar sprays rich in osmoprotectants, as well as phytohormones that induce osmoprotectant release in plants, are effective alternatives to breed crop varieties

References

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that are less susceptible to abiotic stress. Stress conditions (e.g., drought, salinity, heat, cold, heavy metal, pesticides) are still being researched especially in combination with each other. The current scenario is all about identification and characterization of known as well as new classes of osmoprotectants and to understand their basic working as stress busters in plants using omics. The research branch boasts techniques such as mass spectroscopy (MS), electrophoresis, and chromatographic advances. This is leading to further perspectives on the molecular, physiological, and metabolic aspects of stress remediation via osmoprotectants and is in turn narrowing the relevant knowledge gap between lab and field trials to develop such abiotic stress-resistant crop varieties. Another important aspect is the harnessing of amine-derived osmoregulators (e.g., 5-ALA) in photodynamic therapy and photodiagnoses applicable to cancer therapy. The amine-derived molecules are key metabolites in porphyrin precursor molecule biosynthesis that convert monooxygen into less toxic forms. The development of crop plants for further novel medical applications, such as antiaging cosmetics and disease therapy, can also be explored in the future.

References Abro, H.G., Syed, S.T., Kalhoro, N.A., Sheikh, H.G., Awan, S.M., Jessar, D.R., et al., 2013. Insecticides for control of the diamondback moth, Plutella xylostella (L.) (Lepidoptera: Plutellidae) in Pakistan and factors that affect their toxicity. Crop Prot. 52, 9196. Adam, S., Murthy, S.D.S., 2014. Effect of cold stress on photosynthesis of plants and possible protection mechanisms. In: Gaur, R.K., Sharma, P. (Eds.), Approaches to Plant Stress and their Management. Springer, India, pp. 219226. Aghaz, M., Bandehagh, A., Aghazade, E., Toorchi, M., Gholezani, K.G., 2013. Effects of cadmium stress on some growth and physiological characteristics in dill (Anethum graveolens) ecotypes. Int. J. Agric. 3, 409413. Ahanger, A.M., Tyagi, R.S., Wani, R.M., Ahmad, P., 2014. Drought tolerance: role of organic osmolytes, growth regulators, and mineral nutrients. In: Ahmad, P., Wani, R.M. (Eds.), Physiological Mechanisms and Adaptation Strategies in Plants Under Changing Environment. Springer, New York, pp. 2555. Ahmad, R., Kim, M.D., Back, K.H., Kim, H.S., Lee, H.S., Kwon, S.Y., et al., 2008. Stress-induced expression of choline oxidase in potato plant chloroplasts confers enhanced tolerance to oxidative, salt, and drought stresses. Plant Cell Rep. 27, 687698. Ahn, C., Park, U., Park, P.K., 2011. Increased salt and drought tolerance by D-ononitol production in transgenic Arabidopsis thaliana. Biochem. Biophys. Res. Commun. 415, 669674. Ali, Q., Ashraf, M., 2011. Induction of drought tolerance in maize (Zea mays L.) due to exogenous application of trehalose: growth, photosynthesis, water relations and oxidative defense mechanism. J. Agron. Crop Sci. 197, 258271. Aly, A.A., Mohamed, A.A., 2012. The impact of copper ion on growth, thiol compounds and lipid peroxidation in two maize cultivars (Zea mays L.) grown in vitro. Aust. J. Crop Sci. 6, 541549. Anjum, S.A., Farooq, M., Xie, X.Y., Liu, X.J., Ijaz, M.F., 2012. Antioxidant defense system and proline accumulation enables hot pepper to perform better under drought. Sci. Hort. 140, 6673. Armengaud, P., Thiery, L., Buhot, N., March, G., Savouré, A., 2004. Transcriptional regulation of proline biosynthesis in Medicago truncatula reveals developmental and environmental specific features. Plant Physiol. 120, 442450. Ashraf, M., Foolad, M.R., 2007. Roles of glycine betaine and proline in improving plant abiotic stress resistance. Environ. Exp. Bot. 59, 206216.

422


Ashraf, M., Orooj, A., 2006. Salt stress effects on growth, ion accumulation and seed oil concentration in an arid zone traditional medicinal plant ajwain (Trachyspermum ammi [L.] Sprague). J. Arid Environ. 64, 209220. Auge, R.M., 2001. Water relations, drought and vesicular-arbuscular mycorrhizal symbiosis. Mycorrhiza 11, 342. Bagdi, D.L., Shaw, B.P., 2013. Analysis of proline metabolic enzymes in Oryza sativa under NaCl stress. J. Environ. Biol. 34, 677681. Balestrasse, K., Tomaro, M.L., Batlle, A., Noriega, G.O., 2010. The role of 5-aminolevulinic acid in the response to cold stress in soybean plants. Phytochemistry 71, 20382045. Bhandari, K., Nayyar, H., 2014. Low temperature stress in plants: an overview of roles of cryoprotectants in defense. In: Ahmad, P., Wani, R.M. (Eds.), Physiological Mechanisms and Adaptation Strategies in Plants under Changing Environment. Springer, New York, pp. 193265. Bhardwaj, R., Sharma, I., Sharma, R., Poonam, 2014. Betaines and related osmoprotectants—significance in metabolic engineering of plant stress resistance. In: Anjum, N.A., Gill, S.S., Gill, R. (Eds.), Plant Adaptation to Environmental Change: Significance of Amino Acids and Their Derivatives. CABI, Wallingford, UK, pp. 281299. Bhatti, K.H., Anwar, S., Nawaz, K., Hussain, K., Siddiqi, E.H., Usmansharif, R., et al., 2013. Effect of exogenous application of glycinebetaine on wheat (Triticum aestivum L.) under heavy metal stress. Middle East J. Sci. Res. 14, 130137. Bita, C.E., Gerats, T., 2013. Plant tolerance to high temperature in a changing environment: scientific fundamentals and production of heat stress-tolerant crops. Crop Sci. Hortic. 4, 118. Bray, E.A., Serres, J.B., Weretilnyk, E., 2000. Responses to abiotic stresses. In: Buchanan, B.B., Gruissem, W., Jones, R.L. (Eds.), Biochemistry and Molecular Biology of Plants. American Society of Plant Biologists, Rockville, USA, pp. 11581203. Campos, M.K.F., Carvalho, K., Souza, F.S., Marur, C.J., Pereira, L.F.P., Filho, J.C.B., et al., 2011. Drought tolerance and antioxidant enzymatic activity in transgenic Swingle citrumelo plants over-accumulating proline. Environ. Exp. Bot. 72, 242250. Carvalho, D.K., Campos, K.M., Domingues, S.D., Pereira, P.F.L., Vieira, E.G.L., 2013. The accumulation of endogenous proline induces changes in gene expression of several antioxidant enzymes in leaves of transgenic Swingle citrumelo. Mol. Biol. Rep. 40, 32693279. Celik, O., Atak, C., 2012. The effect of salt stress on antioxidative enzymes and proline content of two Turkish tobacco varieties. Turk J. Biol. 36, 339356. Chamoli, S., Verma, A.K., 2014. Targeting of metabolic pathways for genetic engineering to combat abiotic stress tolerance in crop plants. In: Gaur, R.K., Sharma, P. (Eds.), Approaches to Plant Stress and Their Management. Springer, New Delhi, pp. 2337. Chan, Z., Grumet, R., Loescher, W., 2011. Global gene expression analysis of transgenic, mannitol producing, and salt-tolerant Arabidopsis thaliana indicates widespread changes in abiotic and biotic stress-related genes. J. Exp. Bot. 62, 47874803. Chen, C.T., Chen, L.M., Lin, C.C., Kao, C.H., 2001. Regulation of proline accumulation in detached rice leaves exposed to excess copper. Plant Sci. 160, 283290. Chen, T.H.H., Murata, N., 2011. Glycinebetaine protects plants against abiotic stress: mechanisms and biotechnological applications. Plant Cell Environ. 34, 120. Chen, X.M., Lung, C.S., Du, Y.Z., Chye, L.M., 2014. Engineering plants to tolerate abiotic stresses. Biocatal. Agric. Biotechnol. 3, 8187. Chinnusamy, V., Zhu, J., Zhu, J.K., 2007. Cold stress regulation of gene expression in plants. Trends Plant Sci. 12 (10), 444451. Conde, A., Silva, P., Agasse, A., Conde, C., Gero´s, H., 2011. Mannitol transport and mannitol dehydrogenase activities are coordinated in Olea europaea under salt and osmotic stresses. Plant Cell Physiol. 52 (10), 17661775.

References

423

Cortina, C., Culián˜ez-Macia`, F.A., 2005. Tomato abiotic stress enhanced tolerance by trehalose biosynthesis. Plant Sci. 169, 7582. Costa, M.E., Araujo, L.E., Maia, P.V.A., Silva, L.E.F., Bezerra, S.E.C., Silva, G.J., 2014. Toxicity of insecticides used in the Brazilian melon crop to the honey bee Apis mellifera under laboratory conditions. Apidologie 45, 3444. Damalas, C., Eleftherohorinos, A., Ilias, G., 2011. Pesticide exposure, safety issues, and risk assessment indicators. Int. J. Environ. Res. Public Health 8 (5), 14021419. Das-Chatterjee, A., Goswami, L., Maitra, S., Dastidar, K.G., Ray, S., Majumder, A.L., 2006. Introgression of a novel salt-tolerant L-myo-inositol 1-phosphate synthase from Porteresia coarctata (Roxb.) Tateoka (PcINO1) confers salt tolerance to evolutionary diverse organisms. FEBS Lett. 580 (16), 39803988. De Ronde, J.A., Spreeth, M.H., Cress, W.A., 2000. Effect of antisense L-D1-pyrroline-5-carboxylate reductase transgenic soybeen plants subjected to osmotic and drought stress. Plant Growth Regul. 32, 1326. Demiral, T., Tu¨rkan, I., 2005. Comparative lipid peroxidation, antioxidant defense systems and proline content in roots of two rice cultivars differing in salt tolerance. Environ. Exp. Bot. 53, 247257. Dhir, B., Sharmila, P., Saradhi, P.P., 2004. Hydrophytes lack potential to exhibit cadmium stress induced enhancement in lipid peroxidation and accumulation of proline. Aquat. Toxicol. 66, 141147. Dhir, B., Nasim, S., Samantary, S., Srivastava, S., 2012. Assessment of osmolyte accumulation in heavy metal exposed salvinia natans. Int. J. Bot. 8, 153158. Dobra, J., Motyka, V., Dobrev, P., Mal-beck, J., Prasil, I.T., Haisel, D., 2010. Comparison of hormonal responses to heat, drought and combined stress in tobacco plants with elevated proline content. J. Plant Physiol. 167, 13601370. Duman, F., Aksoy, A., Aydin, Z., Temizgul, R., 2010. Effects of exogenous glycine betaine and trehalose on cadmium accumulation and biological responses of an aquatic plant (Lemna gibba L.). Water Air Soil Poll. 217, 545556. Duque, A.S., Almeida, A.M., Silva, A.B., Silva, J.M., Farinha, A.P., Santos, D., et al., 2013. Abiotic stress responses in plants: unraveling the complexity of genes and networks to survive. In: Vahdati, K., Leslie, C. (Eds.), Abiotic Stress-Plant Responses and Applications in Agriculture. InTech, Rijeka, Croatia, pp. 323. El Sayed, A.I., Rafudeen, M.S., Golldack, D., 2013. Physiological aspects of raffinose family oligosaccharides in plants: protection against abiotic stress. Plant Biol. (Stuttg). Available from: http://dx.doi.org/10.1111/plb.12053. Farooq, M., Siddique, K.H.M., Schubert, S., 2013. Role of nitric oxide in improving plant resistance against salt stress. In: Ahmad, P., Azooz, M.M., Prasad, M.N.V. (Eds.), Ecophysiology and Responses of Plants Under Salt Stress, Springer, New York, pp. 413424. Gandonou, C.B., Errabii, T., Abrini, J., Idaomar, M., Senhaji, N.S., 2006. Selection of callus cultures of sugarcane (Saccharum spp.) tolerant to NaCl and their responses to salt stress. Plant Cell Tiss. Org. 87, 916. Gangola, M.P., Khedikar, Y.P., Gaur, P.M., Baga, M., Chibbar, R.N., 2013. Genotype and growing environment interaction shows a positive correlation between substrates of raffinose family oligosaccharides (RFO) biosynthesis and their accumulation in chickpea (Cicer arietinum L.) seeds. J. Agric. Food Chem. 61, 49434952. Gao, M., Tao, R., Miura, K., Dandekar, A.M., Sugiura, A., 2001. Transformation of Japanese persimmon (Diospyros kaki Thunb.) with apple cDNA encoding NADP-dependent sorbitol-6-phosphate dehydrogenase. Plant Sci. 160, 837845. Garg, A.K., Kim, J.-K., Owens, T.G., Ranwala, A.P., Choi, Y.D., Kochian, L.V., et al., 2012. Trehalose accumulation in rice plants confers high tolerance levels to different abiotic stresses. Proc. Natl. Acad. Sci. USA 99, 1589815903. Gill, S.S., Anjum, N.A., Gill, R., 2014. Target osmoprotectants for abiotic stress tolerance in crop plants— glycine betaine and proline. In: Anjum, N.A., Gill, S.S., Gill, R. (Eds.), Plant Adaptation to Environmental Change: Significance of Amino Acids and Their Derivatives. CABI, Wallingford, UK, pp. 97108.

424


Giri, J., 2011. Glycinebetaine and abiotic stress tolerance in plants. Plant Signal. Behav. 6, 17461751. Goel, D., Singh, A.K., Yadav, V., Babbar, S.B., Murata, N., Bansal, K.C., 2011. Transformation of tomato with a bacterial codA gene enhances tolerance to salt and water stresses. J. Plant Physiol. 168, 12861294. Handa, N., Sharma, R., Thukral, A.K., Bhardwaj, R., 2013. Selenium mediated stress amelioration of chromium in Brassica juncea L. plants. Biospectra 8, 155164. Hasanuzzaman, M., Nahar, K., Alam, M.D.M., Roychowdhury, R., Fujita, M., 2013. Physiological, biochemical, and molecular mechanisms of heat stress tolerance in plants. Int. J. Mol. Sci. 14, 96439684. Hashem, H.A., Hassanein, R.A., El-Deep, M.H., Shouman, A.I., 2013. Irrigation with industrial wastewater activates antioxidant system and osmoprotectant accumulation in lettuce, turnip and tomato plants. Ecotox. Environ. Safe 95, 144152. Hayat, S., Hayat, Q., Alyemeni, M.N., Ahmad, A., 2013. Proline enhances antioxidative enzyme activity, photosynthesis and yield of Cicer arietinum L. exposed to cadmium stress. Acta Bot. Croat. 72, 323335. He, C., Yang, A., Zhang, W., Gao, Q., Zhang, J., 2010. Improved salt tolerance of transgenic wheat by introducing betA gene for glycine betaine synthesis. Plant Cell Tiss. Org. Cult. 101, 6578. Hossain, M.A., Hasanuzzaman, M., Fujita, M., 2010. Up-regulation of antioxidant and glyoxalase systems by exogenous glycinebetaine and proline in mung bean confer tolerance to cadmium stress. Physiol. Mol. Biol. Plants 16, 259272. Hu, L., Hu, T., Zhang, X., Pang, H., Fu, J., 2012. Exogenous glycine betaine ameliorates the adverse effect of salt stress on perennial ryegrass. J. Am. Soc. Hortic. Sci. 137, 3846. Huang, Y., Bie, Z., Liu, Z., Zhen, A., Wang, W., 2009. Protective role of proline against salt stress is partially related to improvement of water status and peroxidise enzyme activity in cucumber. Soil Sci. Plant Nutr. 55, 698704. Huang, Z., Zhao, L., Chen, D., Liang, M., Liu, Z., Shao, H., et al., 2013. Salt stress encourages proline accumulation by regulating proline biosynthesis and degradation in Jerusalem artichoke plantlets. PLoS One 8, e62085. Iordachescu, M., Imai, R., 2008. Trehalose biosynthesis in response to abiotic stresses. J. Integr. Plant Biol. 50, 12231229. Iqbal, N., Umar, S., Khan, N.A., Khan, M.I.R., 2014. A new perspective of phytohormones in salinity tolerance: regulation of proline metabolism. Environ. Exp. Bot. 100, 3442. Islam, M.M., Hoque, M.A., Okuma, E., Banu, M.N., Shimoishi, Y., Nakamura, Y., et al., 2009. Exogenous proline and glycinebetaine increase antioxidant enzyme activities and confer tolerance to cadmium stress in cultured tobacco cells. J. Plant Physiol. 166, 15871597. Iturriaga, G., Suárez, R., Nova-Franco, B., 2009. Trehalose metabolism: from osmoprotection to signaling. Int. J. Mol. Sci. 10, 37933810. Iwaki, T., Guo, L., Ryals, A.J., Yasuda, S., Shimazaki, T., Kikuchi, A., et al., 2013. Metabolic profiling of transgenic potato tubers expressing Arabidopsis dehydration response element-binding protein 1A (DREB1A). J. Agric. Food Chem. 61 (4), 893900. Jang, I.C., Oh, S.J., Seo, J.S., Choi, W.B., Song, S.I., Kim, C.H., et al., 2003. Expression of a bifunctional fusion of the Escherichia coli genes for trehalose-6-phosphate synthase and trehalose-6-phosphate phosphatase in transgenic rice plants increases trehalose accumulation and abiotic stress tolerance without stunting growth. Plant Physiol. 131, 516524. Janska, A., Marsı´, K.P., Zelenkova, S., Ovesná, J., 2010. Cold stress and acclimation—what is important for metabolic adjustment. Plant Biol. 12, 395405. Joseph, S., Murphy, D., Bhave, M., 2013. Glycine betaine biosynthesis in saltbushes (Atriplex spp.) under salinity stress. Biologia (Bratisl). 68, 879895. ¨ zdemir, F., Tu¨rkan, I., 2014. Glycine betaine protects tomato (Solanum lycopersiKarabudak, T., Bor, M., O cum) plants at low temperature by inducing fatty acid desaturase7 and lipoxygenase gene expression. Mol. Biol. Rep. [epub ahead of print].

References

425

Karim, S., Aronsson, H., Ericson, H., Pirhonen, M., Leyman, B., Welin, B., 2007. Improved drought tolerance without undesired side effects in transgenic plants producing trehalose. Plant Mol. Biol. 64, 371386. Karimi, L.N., Khanahmadi, M., Moradi, B., 2012. Accumulation and phytotoxicity of lead in Cynara scolymus. Indian J. Sci. Technol. 5, 36343641. Kaya, C., Tuna, A.L., Ashraf, M., Altunlu, H., 2007. Improved salt tolerance of melon (Cucumis melo L.) by the addition of proline and potassium nitrate. Environ. Exp. Bot. 60, 397403. Kaya, C., So¨nmez, O., Aydemir, S., Dikilita¸s, M., 2013. Mitigation effects of glycinebetaine on oxidative stress and some key growth parameters of maize exposed to salt stress. Turk. J. Agric. For. 37, 188194. Kempa, S., Rozhon, W., Samaj, J., 2007. A plastid-localized glycogen synthase kinase 3 modulates stress tolerance and carbohydrate metabolism. Plant J. 49, 10761090. Kerkeb, L., Kramer, U., 2003. The role of free histidine in xylem loading of nickel in Alyssum lesbiacum and Brassica juncea. Plant Physiol. 131, 716. Khedr, A.H.A., Abbas, M.A., Wahid, A.A.A., Quick, W.P., Abogadallah, G.M., 2003. Proline induces the expression of salt stress responsive proteins and may improve the adaptation of Pancratium maritimum L. to salt stress. J. Exp. Bot. 54, 25532562. Kido, E.A., Ferreira Neto, J.R., Silva, R.L., Belarmino, L.C., Bezerra Neto, J.P., Soares-Cavalcanti, N.M., et al., 2013. Expression dynamics and genome distribution of osmoprotectants in soybean: identifying important components to face abiotic stress. BMC Bioinformatics 14, 111. Kim, M.D., Kim, Y.H., Kwon, S.Y., Kwak, S.S., Lee, H.S., 2010. Enhanced tolerance to methyl viologeninduced oxidative stress and high temperature in transgenic potato plants overexpressing the CuZnSOD, APX and NDPK2 genes. Physiologia plantarum. Physiol. Plant. 140 (2), 153162. Knipp, G., Honermeier, B., 2006. Effect of water stress on proline accumulation of genetically modified potatoes (Solanum tuberosum L.) generating fructans. Plant Physiol. 163, 392397. Koca, H., Bor, M., Ozdemir, F., Turkan, I., 2007. The effect of salt stress on lipid peroxidation, antioxidative enzymes and proline content of sesame cultivars. Environ. Exp. Bot. 60, 344351. Konstantinova, T., Parvanova, D., Atanassov, A., Djilianov, D., 2002. Freezing tolerant tobacco, transformed to accumulate osmoprotectants. Plant Sci. 163, 157164. Korkmaz, A., Korkmaz, Y., Demirkran, A.R., 2010. Enhancing chilling stress tolerance of pepper seedlings by exogenous application of 5-aminolevulinic acid. Environ. Exp. Bot. 67, 495501. Kosová, K., Vı´támvás, P., Prásˇil, I.T., Renaut, J., 2011. Plant proteome changes under abiotic stresscontribution of proteomics studies to understanding plant stress response. J. Proteom. 74, 13011322. Krasensky, J., Jonak, C., 2012. Drought, salt, and temperature stress-induced metabolic rearrangements and regulatory networks. J. Exp. Bot. 63, 15931608. Kubis, J., 2003. Polyamines and “scavenging system”: influence of exogenous spermidine on catalase and guaiacol peroxidase activities, and free polyamines level in barley leaves under water deficit. Acta Physiol. Plant 25, 337343. Kubis, J., 2008. Exogenous spermidine alters in different ways activities of some scavenging system enzymes, H2O2 and superoxide radical levels in water stressed cucumber leaves. J. Plant Physiol. 165, 397406. Kumar, S., Habib, K., Fatma, T., 2008. Endosulfan induced biochemical changes in nitrogen-fixing cyanobacteria. Sci. Total Environ. 403, 130138. Kumar, S.G., Reddy, A.M., Sudhakar, C., 2003. NaCl effects on proline metabolism in two high yielding genotypes of mulberry (Morus alba L.) with contrasting salt tolerance. Plant Sci. 165, 12451251. Lang, F., 2007. Mechanisms and significance of cell volume regulation. J. Am. Coll. Nutr. 26 (5S), 613S623S. Lee, G., Carrow, R.N., Duncan, R.R., Eiteman, M.A., Rieger, M.W., 2008. Synthesis of organic osmolytes and salt tolerance mechanisms in Paspalum vaginatum. Environ. Exp. Bot. 63, 1927.

426


Lehmann, S., Funck, D., Szabados, L., 2010. Proline metabolism and transport in plant development. Amino Acids 39, 949962. Less, H., Galili, G., 2008. Principal transcriptional programs regulating plant amino acid metabolism in response to abiotic stresses. Plant Physiol. 147, 316330. Li, F., Lei, H., Zhao, X., Tian, R., Li, T., 2012. Characterization of three sorbitol transporter genes in micropropagated apple plants grown under drought stress. Plant Mol. Biol. Rep. 30, 123130. Li, H.W., Zang, B.S., Deng, X.W., Wang, X.P., 2011. Overexpression of the trehalose-6-phosphate synthase gene OsTPS1 enhances abiotic stress tolerance in rice. Planta 234, 10071018. Li, M., Guo, S., Xu, Y., Meng, Q., Li, G., Yang, X., 2014a. Glycine betaine-mediated potentiation of HSP gene expression involves calcium signaling pathways in tobacco exposed to NaCl stress. Physiol. Plant. 150, 6375. Li, X., Guo, C., Gu, J., Duan, W., Zhao, M., Ma, C., et al., 2014b. Overexpression of VP, a vacuolar H 1 -pyrophosphatase gene in wheat (Triticum aestivum L.), improves tobacco plant growth under Pi and N deprivation, high salinity, and drought. J. Exp. Bot. 65 (2), 683696. Liang, D., Cui, M., Wu, S., Ma, F.W., 2012. Genomic structure, sub-cellular localization, and promoter analysis of the gene encoding sorbitol-6-phosphate dehydrogenase from apple. Plant Mol. Biol. Rep. 30, 904914. Liu, Z.-H., Zhang, H.-M., Li, G.-L., Guo, X.-L., Chen, S.-Y., Liu, G.-B., et al., 2011. Enhancement of salt tolerance in alfalfa transformed with the gene encoding for betaine aldehyde dehydrogenase. Euphytica 178, 363372. Livingston, D.P., Hincha, D.K., Heyer, A.G., 2009. Fructan and its relationship to abiotic stress tolerance in plants. Cell. Mol. Life. Sci. 66, 20072023. Lobell, D.B., Field, C.B., 2007. Global scale climate—crop yield relationships and the impacts of recent warming. Environ. Res. Lett. 2, 014002. Macro, F., Alcazar, R., Altabella, T., Carrasco, P., Gill, S.S., Tuteja, N., et al. (Eds.), 2012. Improving Crop Resistance to Abiotic Stress, vols. 1 & 2. Wiley-VCH Verlag GmbH and Co. KGaA, Weinheim, Germany. Mahnaz, N., Nivedita, G., Dhumal, K.N., 2011. Effect of chloropyrifos and malathion on antioxidant enzymes in tomato and brinjal. Int. J. Pharma Bio. Sci. 2, 202209. Manikar, N., Kumar, S., Habib, K., Fatma, T., 2013. Biochemical analysis of Anabaena variabilis exposed to malathion pesticide with special reference to oxidative stress and osmolytes. Int. J. Innov. Res. Sci. Eng. Technol. 2 (10), 54035420. Martino, C.D., Delfine, S., Pizzuto, R., Loreto, F., Fuggi, A., 2003. Free amino acids and glycine betaine in leaf osmoregulation of spinach responding to increasing salt stress. New Phytol. 158, 455463. Mattioli, R., Marchese, D., D’Angeli, S., Altamura, M.M., Costantino, P., Trovato, M., 2008. Modulation of intracellular proline levels affects flowering time and inflorescence architecture in Arabidopsis. Plant Mol. Biol. 66, 277288. Mattioli, R., Falasca, G., Sabatini, S., 2009. The proline biosynthetic genes P5CS1 and P5CS2 play overlapping roles in Arabidopsis flower transition but not in embryo development. Plant Physiol. 137, 7285. Miller, G., Suzuki, N., Ciftci-Yilmaz, S., Mittler, R., 2010. Reactive oxygen species homeostasis and signalling during drought and salinity stresses. Plant Cell Environ. 33, 453467. Miranda, J.A., Avonce, N., Suarez, R., Thevelein, J.M., Van Dijck, P., Iturriaga, G., 2007. A bifunctional TPSTPP enzyme from yeast confers tolerance to multiple and extreme abiotic-stress conditions in transgenic Arabidopsis. Planta 226, 14111421. Moghaddam, M.R.B., Ende, W.V.D., 2012. Sugars and plant innate immunity. J. Exp. Bot. 110. Mohammadi, Z., Abavi Kalat, S.M.N., Haghaghi, S., 2013. Effect of copper sulfate and salt stress on seed germination and proline content of psyllium (Plantago psyllium). Am. Eurasian J. Agric. Environ. Sci. 13, 148152.

References

427

Mohammadkhani, N., Heidari, R., 2008. Drought-induced accumulation of soluble sugars and proline in two maize varieties. World Appl. Sci. J. 3, 448453. Molinari, H.B.C., Marur, C.J., Filho, J.C.B., Kobayashi, A.K., Pileggi, M., Leite Junior, R.P., et al., 2004. Osmotic adjustment in transgenic citrus rootstock Carrizo citrange (Citrus sinensis Osb 3 Poncirus trifoliate L. Raf) overproducing proline. Plant Sci. 167, 13751381. Monoharan, P.T., Shanmugaiah, V., Balasubramanian, N., Gomathinayagam, S., Sharma, M.P., Muthuchelian, K., 2010. Influence of AM fungi on the growth and physiological status of Erythrina variegata L. grown under different water stress conditions. Eur. J. Soil Biol. 46, 151156. Muslu, A., Ergun, N., 2013. Effects of copper and chromium and high temperature on growth, proline and protein content in wheat seedlings. Bangladesh J. Bot. 42, 105111. Naliwajski, M.R., Skłodowska, M., 2014. Proline and its metabolism enzymes in cucumber cell cultures during acclimation to salinity. Protoplasma 251, 201209. Nawaz, K., Ashraf, M., 2010. Exogenous application of glycinebetaine modulates activities of antioxidants in maize plants subjected to salt stress. J. Agron. Crop Sci. 196, 2837. Ningthoujam, M., Habib, K., Bano, F., Zutshi, S., Fatma, T., 2013. Exogenous osmolytes suppresses the toxic effects of malathion on Anabaena variabilis. Ecotox. Environ. Safe 94, 2127. Nishizawa, A., Yabuta, Y., Shigeoka, S., 2008. Galactinol and raffinose constitute a novel function to protect plants from oxidative damage. Plant Physiol. 147, 12511263. Nishizawa-Yokoi, A., Yabuta, Y., Shigeoka, S., 2008. The contribution of carbohydrates including raffinose family oligosaccharides and sugar alcohols to protection of plant cells from oxidative damage. Plant Signal. Behav. 3, 10161018. Noiraud, N., Maurousset, L., Lemoine, R., 2001. Identification of a mannitol transporter, AgMaT1, in celery phloem. Plant Cell 13, 695705. Nyyssola, A., Kerovuo, J., Kaukinen, P., von Weymarn, N., Reinikainen, T., 2000. Extreme halophiles synthesize betaine from glycine by methylation. J. Biol. Chem. 275, 2219622201. Osakabe, Y., Osakabe, K., Shinozaki, K., 2013. Plant environmental stress responses for survival and biomass enhancement. In: Tuteja, N., Gill, S.S. (Eds.), Climate Change and Plant Abiotic Stress Tolerance. WileyVCH Verlag GmbH & Co. KGaA, Weinheim, Germany. Palma, F., Fátima Carvajal, F., Lluch, C., Jamilena, M., Garrido, D., 2014. Changes in carbohydrate content in zucchini fruit (Cucurbita pepo L.) under low temperature stress. Plant Sci. 217218, 7886. Parvanova, D., Ivanov, S., Konstantinova, T., Karanov, E., Atanassov, A., Tsvetkov, T., et al., 2004. Transgenic tobacco plants accumulating osmolytes show reduced oxidative damage under freezing stress. Plant Physiol. Biochem. 42, 5763. Patade, V.Y., Suprasanna, P., Bapat, V.A., 2008. Effects of salt stress in relation to osmotic adjustment on sugarcane (Saccharum officinarum L.) callus cultures. Plant Growth Regul. 55, 169173. Penna, S., 2003. Building stress tolerance through over-producing trehalose in transgenic plants. Trends Plant Sci. 8, 355357. Peshev, D., Vergauwen, R., Moglia, A., Hideg, E., Van den Ende, W., 2013. Towards understanding vacuolar antioxidant mechanisms: a role for fructans? J. Exp. Bot. 64, 10251038. Peters, S., Mundree, S.G., Thomson, J.A., Farrant, J.M., Keller, F., 2007. Protection mechanisms in the resurrection plant Xerophyta viscose (Baker): both sucrose and raffinose family oligosaccharides (RFOs) accumulate in leaves in response to water deficit. J. Exp. Bot. 58, 19471956. Pinto-Marijuan, M.P., Munné-Bosch, S., 2013. Ecophysiology of invasive plants: osmotic adjustment and antioxidants. Trends Plant Sci. 18, 660666. Pirzadah, B.T., Malik, B., Rehman, U.R., Hakeem, R.K., Qureshi, I.M., 2014. Signaling in response to cold stress. In: Hakeem, R.K., Rehman, U.R., Tahir, I. (Eds.), Plant Signaling: Understanding the Molecular Crosstalk. Springer, New Delhi, India, pp. 193226.

428


Porcel, R., Ruiz-Lozano, J.M., 2004. Arbuscular mycorrhizal influence on leaf water potential, solute accumulation, and oxidative stress in soybean plants subjected to drought stress. J. Exp. Bot. 55, 17431750. Quan, R., Shang, M., Zhang, H., Zhao, Y., Zhang, J., 2004. Engineering of enhanced glycine betaine synthesis improves drought tolerance in maize. Plant Biotech. 2, 477486. Rai, A.N., Penna, S., 2013. Molecular evolution of plant P5CS gene involved in proline biosynthesis. Mol. Biol. Rep. 40 (11), 64296435. Ramadan, A.M., Eissa, H.F., Hassanein, S.E., Azeiz, A.Z.A., Saleh, O.M., Mahfouz, H.T., et al., 2013. Increased salt stress tolerance and modified sugar content of bread wheat stably expressing the mtlD gene. Life Sci. J. 10, 23482362. Rathinasabapathi, B., 2000. Metabolic engineering for stress tolerance: installing osmoprotectant synthesis pathways. Ann. Bot. 86, 709716. Redillas, M.C.F.R., Park, S.-H., Lee, J.W., Kim, Y.S., Jeong, J.S., Jung, H., et al., 2012. Accumulation of trehalose increases soluble sugar contents in rice plants conferring tolerance to drought and salt stress. Plant Biotechnol. Rep. 6, 8996. Reis, S.P.D., Lima, A.M., Souza, CRBS, 2012. Recent molecular advances on downstream plant responses to abiotic stress. Int. J. Mol. Sci. 13, 86288647. Rodziewicz, P., Swarcewicz, B., Chmielewska, K., Wojakowska, A., 2014. Maciej Stobiecki influence of abiotic stresses on plant proteome and metabolome changes. Acta Physiol. Plant. 36, 119. Rontein, D., Basset, G., Hanson, A.D., 2002. Metabolic engineering of osmoprotectant accumulation in plants. Metab. Eng. 4, 4956. Roosens, N.H., Bitar, F., Loenders, K., Angenon, G., Jacobs, M., 2002. Overexpression of ornithine-daminotransferase increases pro-biosynthesis and osmotolerance in transgenic plants. Mol. Breed. 9, 7380. Sairam, R.K., Rao, K.V., Srivastava, G.C., 2002. Differential response of wheat genotypes to long term salinity stress in relation to oxidative stress, antioxidant activity and osmolyte concentration. Plant Sci. 163, 10371046. Sakamoto, A., Murata, N., 2002. The role of glycine betaine in the protection of plants from stress: clues from transgenic plants. Plant Cell Environ. 25, 163171. Sa˘glam, A., Jan, S., 2014. Physiological mechanisms and adaptation strategies in plants under changing environment. In: Ahmad, P., Wani, R.M. (Eds.), Importance of Protective Compounds in Stress Tolerance. Springer, New York, pp. 265284. Seher, Y., Filiz, O., Melike, B., 2013. Gamma-amino butyric acid, glutamate dehydrogenase and glutamate decarboxylase levels in phylogenetically divergent plants. Plant Syst. Evol. 299, 403412. Selvakumar, G., Kim, K., Hu, S., Sa, T., 2014. Effect of salinity on plants and the role of arbuscular mycorrhizal fungi and plant growth-promoting rhizobacteria in alleviation of salt stress. In: Parvaiz Ahmad, P., Wani, R.M. (Eds.), Physiological Mechanisms and Adaptation Strategies in Plants Under Changing Environment. Springer, New York, pp. 115144. Sengupta, S., Patra, B., Ray, S., Majumder, A.L., 2008. Inositol methyl tranferase from a halophytic wild rice, Porteresia coarctata Roxb. (Tateoka): regulation of pinitol synthesis under abiotic stress. Plant Cell Environ. 31 (10), 14421459. Shao, G., Chen, M., Wang, W., Zhang, G., 2008. The effect of salinity pretreatment on Cd accumulation and Cd-induced stress in BADH-transgenic and nontransgenic rice seedlings. J. Plant Growth Regul. 27, 205210. Sharma, I., Pati, P.K., Bhardwaj, R., 2011. Effect of 28-homobrassinolide on antioxidant defence system in Raphanus sativus L. under chromium toxicity. Ecotoxicology 20, 862874. Sharma, I., Bhardwaj, R., Pati, K.P., 2013a. Stress modulation response of 24-epibrassinolide against imidacloprid in an elite indica rice variety Pusa Basmati-1. Pesticide Biochem. Physiol. 105, 144153.

References

429

Sharma, I., Ching, E., Saini, S., Bhardwaj, R., Pati, P.K., 2013b. Exogenous application of brassinosteroid offers tolerance to salinity by altering stress responses in rice variety Pusa Basmati-1. Plant Physiol. Biochem. 69, 1726. Sharma, R., Handa, N., Sharma, M., Bhardwaj, R., Thukral, A.K., 2013c. Chelate mediated phytoextraction of copper (II) involves changes in metal uptake, osmoprotectant and photosynthetic parameters in Brassica juncea L. Biospectrum 8 (2), 165172. Sharma, S.S., Dietz, K.J., 2006. The significance of amino acids and amino acid-derived molecules in plant responses and adaptation to heavy metal stress. J. Exp. Bot. 57, 711726. Sharma, S., Verslues, P.E., 2010. Mechanisms independent of abscisic acid (ABA) or proline feedback have a predominant role in transcriptional regulation of proline metabolism during low water potential and stress recovery. Plant Cell Environ. 14, 18381851. Shinozaki, K., Yamaguchi-Shinozaki, K., 2007. Gene networks involved in drought stress response and tolerance. J. Exp. Bot. 58, 221227. Silva, R.L.O., Ferreira Neto, J.R.C., Pandolfi, V., Chabregas, S.M., Burnquist, W.L., Benko-Iseppon, A.M., et al., 2011. Transcriptomics of sugarcane osmoprotectants under drought, plants and environment. In: Vasanthaiah, K.N.H., Kambiranda, D. (Eds.), Plants and Environment. InTech Europe, Croatia. Siripornadulsil, S., Traina, S., Verma, D.P.S., Sayre, R.T., 2002. Molecular mechanisms of proline-mediated tolerance to toxic heavy metals in transgenic microalgae. Plant Cell 14, 28372847. Soshinkova, T.N., Radyukina, N.L., Korolkova, D.V., Nosov, A.V., 2013. Proline and functioning of the antioxidant system in Thellungiella salsuginea plants and cultured cells subjected to oxidative stress. Russ. J. Plant Physiol. 60 (1), 4154. Subbarao, G.V., Wheeler, R.M., Levine, L.H., Stutte, G.W., 2001. Glycine betaine accumulation, ionic and water relations of red-beet at contrasting levels of sodium supply. J. Plant Physiol. 158, 767776. Summart, J., Thanonkeo, P., Panichajakul, S., Prathepha, P., McManus, M.T., 2010. Effect of salt stress on growth, inorganic ion and proline accumulation in Thai aromatic rice, Khao Dawk Mali 105, callus culture. Afr. J. Biotechnol. 9, 145152. Surekha, C., Kumari, N.K., Aruna, L.V., Suneetha, G., Arundhati, A., Kishor, B.P., 2014. Expression of the Vigna aconitifolia P5CSF129A gene in transgenic pigeon pea enhances proline accumulation and salt tolerance. Plant Cell Tiss. Org. Cult. 116, 2736. Swati Megha, S., Basu, U., 2014. Metabolic engineering of cold tolerance in plants. Biocatal. Agric. Biotechnol. 3, 8895. Syiem, M.B., Nongrum, N.A., 2011. Increase in intracellular proline content in Anabaena variabilis during stress conditions. J. Appl. Nat. Sci. 3, 119123. Szabados, L., Savouré, A., 2010. Proline: a multifunctional amino acid. Trends Plant Sci. 15, 8997. Taji, T., Ohsumi, C., Iuchi, S., Seki, M., Kasuga, M., Kobayashi, M., et al., 2002. Important roles of droughtand cold-inducible genes for galactinol synthase in stress tolerance in Arabidopsis thaliana. Plant J. 29, 417426. Theerakulpisut, P., Gunnula, W., 2012. Exogenous sorbitol and trehalose mitigated salt stress damage in saltsensitive but not salt-tolerant rice seedlings. Asian J. Crop Sci. 4, 165170. Turchetto-Zolet, A.C., Margis-Pinheiro, M., Margis, R., 2009. The evolution of pyrroline-5-carboxylate synthetase in plants: a key enzyme in proline synthesis. Mol. Genet. Genomics 281, 8797. Urano, K., Kurihara, Y., Seki, M., Shinozaki, K., 2010. “Omics” analyses of regulatory networks in plant abiotic stress responses. Curr. Opin. Plant Biol. 13, 132138. Usadel, B., Blasing, O.E., Gibon, Y., Poree, F., Hohne, M., Gunter, M., et al., 2008. Multilevel genomic analysis of the response of transcripts, enzyme activities and metabolites in Arabidopsis rosettes to a progressive decrease of temperature in the non-freezing range. Plant Cell Environ. 31, 518547.

430


Valluru, R., Van den Ende, W., 2008. Plant fructans in stress environments: emerging concepts and future prospects. J. Exp. Bot. 59, 29052916. Van den Ende, W., 2013. Multifunctional fructans and raffinose family oligosaccharides. Front. Plant Sci. 4, 111. Waditee, R., Bhuiyan, M.N.H., Rai, V., Aoki, K., Tanaka, Y., Hibino, T., et al., 2005. Genes for direct methylation of glycine provide high levels of glycinebetaine and abiotic-stress tolerance in Synechococcus and Arabidopsis. Proc. Natl. Acad. Sci. USA 102, 13181323. Wahid, A., 2004. Analysis of toxic and osmotic effects of sodium chloride on leaf growth and economic yield of sugarcane. Bot. Bull. Acad. Sin. 45, 133141. Wahid, A., Close, T.J., 2007. Expression of dehydrins under heat stress and their relationship with water relations of sugarcane leaves. Biol. Plant 51, 104109. Wang, C., Zhang, D.W., Wang, Y.C., Zheng, L., Yang, C.P., 2012. A glycine-rich RNA-binding protein can mediate physiological responses in transgenic plants under salt stress. Mol. Biol. Rep. 39, 10471053. Wani, S.H., Singh, N.B., Haribhushan, A., Mir, J.I., 2013. Compatible solute engineering in plants for abiotic stress tolerance - role of glycine betaine. Curr. Genomics 14 (3), 157165. Wargo, M.J., 2013. Choline catabolism to glycine betaine contributes to pseudomonas aeruginosa survival during murine lung infection. PLoS One 8 (2), e56850. Wigge, P.A., 2013. Ambient temperature signalling in plants. Curr. Opin. Plant Biol. 16 (5), 661666. Williamson, J.D., Jennings, D.B., Guo, W.-W., Pharr, D.M., Ehrenshaft, M., 2002. Sugar alcohols, salt stress, and fungal resistance: polyols—multifunctional plant protection? J. Am. Soc. Hortic. 127 (4), 467473. Wu, Q.S., Xia, R.X., 2006. Arbuscular mycorrhizal fungi influence growth, osmotic adjustment and photosynthesis of citrus under well-watered and water stress conditions. J. Plant Physiol. 163, 417425. Xing, W., Huang, W., Liu, G., 2010. Effect of excess iron and copper on physiology of aquatic plant Spirodela polyrrhiza (L.) Schleid. Environ. Toxicol. 25, 103112. Xu, W.L., Zhang, D.J., Wu, Y.F., Qin, L.X., Huang, G.Q., Li, J., et al., 2013. Cotton PRP5 gene encoding a proline-rich protein is involved in fiber development. Plant Mol. Biol. 82, 353365. Xue, X., Liu, A., Hua, X., 2009. Proline accumulation and transcriptional regulation of proline biosynthesis and degradation in Brassica napus. Biochem. Mol. Biol. Rep. 42, 2834. Yadav, R.K., Sangwan, R.S., Sabir, F., Srivastava, A.K., Sangwan, N.S., 2014. Effect of prolonged water stress on specialized secondary metabolites, peltate glandular trichomes, and pathway gene expression in Artemisia annua L. Plant Physiol. Biochem. 74, 7083. Yang, J., Zhang, J., Liu, K., Wang, Z., Liu, Z., 2007. Involvement of polyamines in the drought resistance of rice. J. Exp. Bot. 58, 15451555. Yin, Y.-G., Kobayashi, Y., Sanuki, A., Kondo, S., Fukuda, N., Ezura, H., et al., 2010. Salinity induces carbohydrate accumulation and sugar-regulated starch biosynthetic genes in tomato (Solanum lycopersicum L. cv. “Micro-Tom”) fruits in an ABA- and osmotic stress-independent manner. J. Exp. Bot. 61, 563574. Zhang, N., Si, H.-J., Wen, G., Du, H.-H., Liu, B.-L., Wang, D., 2011. Enhanced drought and salinity tolerance in transgenic potato plants with a BADH gene from spinach. Plant Biotechnol. Rep. 5, 7177. Zhang, Y., Zhong, C.L., Chen, Y., Chen, Z., Jiang, Q.B., Wu, C., et al., 2010. Improving drought tolerance of Casuarina equisetifolia seedlings by arbuscular mycorrhizas under glasshouse conditions. New Forest 40, 261271. Zhou, S.-F., Chen, X.-Y., Xue, X.-N., Zhang, X.-G., Li, Y.-X., 2007. Physiological and growth responses of tomato progenies harbouring the betaine aldehyde dehydrogenase gene to salt stress. J. Integ. Plant Biol. 49, 628663.

CHAPTER

The Emerging Role of Aquaporins in Plant Tolerance of Abiotic Stress

18

ˇ Nada Surbanovski and Olga M. Grant

18.1 Introduction Plants are composed mainly of water (Larcher, 1995). Terrestrial plants thus have several ways to adapt, allowing them to maintain an adequate internal water status, despite being exposed to a relatively dry aerial environment (Jones, 1992). Several environmental stress factors perturb the thermodynamic state of water in plant cells—most obviously drought, salinity, and temperature. Limited water availability also has an impact on nutrient availability. Some pollutants alter the plantwater relationship by changing patterns of stomatal conductance or damaging the leaf waxes that would normally limit loss of water (Larcher, 1995). Although in this chapter we focus on abiotic stress, it is worth noting that pests and pathogens also often have an impact on the plantwater relationship (Nilsson, 1995). Plants’ water status depends on a balancing act between water uptake from the soil and loss to the atmosphere. Several hundred milliliters of water are required to produce a gram of plant dry matter, but around 95% of this is lost in transpiration (Kramer and Boyer, 1995). Transpiration also produces the energy gradient required for passive water absorption and the ascent of sap. Water flows through the plant via radial (through tissues) or axial (xylem vessel) transport. Axial water flow is a lowresistance path; however, transport through living tissue is more complex. Radial flow of water is possible via three routes: the apoplastic (around cells, along plant cell walls), the symplastic (through cells connected by plasmodesmata), and the transcellular (across plasma membranes of individual cells). The symplastic and transcellular pathways involve traversing cell membranes and movement through these routes often is referred to as cell-to-cell transport (Steudle, 2000). Bulk water flow associated with transpiration is thought to be mostly apoplastic, except when water flows through tissues with suberized barriers such as the exo- and endodermis of the root and bundlesheath cells in the leaf (Steudle, 2000; Koroleva et al., 2002). In addition to this, the cellto-cell pathway is thought to be important at low rates of transpiration, such as during drought, salinity, or nutrient stress, or at night (Steudle and Peterson, 1998; Tyerman et al., 2002). It has been shown that the cell-to-cell pathway can account for 35 to 80% of the water transported in a whole root system under water-sufficient conditions; while under water-deficit conditions, 60 to 80% is attributed to cellular pathways (Martre et al., 2002). A study of root water flow in barley using a range of methods (e.g., root pressure probe, root exudation, vacuum perfusion, and cell pressure probe) ruled out the possibility of a purely P. Ahmad (Ed): Emerging Technologies and Management of Crop Stress Tolerance, Volume 2. DOI: http://dx.doi.org/10.1016/B978-0-12-800875-1.00018-1 © 2014 Elsevier Inc. All rights reserved.

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apoplastic path in radial water uptake under water-sufficient conditions; the study further emphasized the importance of water transport across membranes (Knipfer and Fricke, 2010). Although water can pass through semipermeable membranes, it was postulated in the 1960s that transport of water under certain conditions must be facilitated by the opening of “water channels” (see review by Tyerman et al., 2002). Such channels were later discovered to be formed by a class of proteins, now called aquaporin proteins.

18.2 Aquaporins Aquaporins are transmembrane proteins, a member of the major intrinsic protein (MIP) family, which facilitate the passive movement of water down an existing water potential gradient. They are ubiquitous in living cells, as shown by their presence in membranes of eubacteria, eukaryota, and archea (Kozono et al., 2003). A member of the aquaporin family was first identified and sequenced in 1984 by Gorin et al. from bovine lens cells (Gorin et al., 1984), and a water channel function of this protein family was identified several years later on a homologous protein from human red blood cells—CHIP28, now called AQP1. The discovery was based on the ability of this gene to dramatically increase water permeability in Xenopus oocytes expressing its mRNA (Preston et al., 1992). Since then, aquaporins have been studied in many organisms and the discovery of a tonoplast integral protein that functions as an aquaporin (Maurel et al., 1993) triggered numerous investigations into plant aquaporin genes and opened up a novel perspective on the plantwater relationship (Maurel and Chrispeels, 2001; Tyerman et al., 2002).

18.2.1 Structure and water-conducting properties of aquaporins The secondary structure of all aquaporins consists of six transmembrane α-helices (TM1-6) connected with five loops, of which two are intracellular and three are extracellular. The C- and Ntermini are located on the cytoplasmic side of the membrane. One of the intra- and one of the extracellular loops are hydrophobic and contain a small α-helix each. At the end of each small helix is the highly conserved asparagineprolinealanine (NPA) signature motif of aquaporins (Luu and Maurel, 2005). The aquaporin molecule has obverse symmetry because the second half of the structure is essentially an inverted repeat of the topology of the first half, which results in the location of the carboxy terminus at the cytoplasmic side (Sui et al., 2001). The hydrophobic loops containing the NPA motif overlap in the middle of the lipid bilayer to form two hemipores and create a narrow channel similar in shape to an hourglass (Jung et al., 1994). A high-resolution structure of the water channel of aquaporins has been studied on AQP1 from red blood cells using X-ray and electron crystallography (Murata et al., 2000; Sui et al., 2001). The channel consists of three topological elements: an extracellular vestibule, a cytoplasmic vestibule, and an extended narrow pore or selectivity filter containing the constriction region. The topology of the constriction region is crucial to the substrate specificity of aquaporins, determining whether an aquaporin is water-selective or able to transport other solutes such as glycerol (Sui et al., 2001). One of the remarkable features of aquaporins is that they enable efficient permeation of water molecules while excluding proton flux, which would disturb the electrochemical potential across the membrane. Proton transport in bulk water requires passing of H1 from one water molecule to

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the next and involves a rearrangement of hydrogen bonds. In proteins, proton conductance occurs in a single file arrangement (“proton wire”), involving reorientation of water molecules. This, however, does not happen in aquaporins, even though water molecules move through the aquaporin pore in a single file. Starting from the NPA center, water molecules are oriented in opposite directions in the two halves of the channel, with their hydrogen atoms pointing toward the exits (Murata et al., 2000; Tajkhorshid et al., 2002). The central oxygen in the water molecule becomes hydrogen-bonded to the two asparagine residues from both NPA motifs; a different binding pattern is prohibited by the surrounding hydrophobic residues. This oxygen is therefore unavailable as a proton acceptor for the neighboring water molecules, which results in the prevention of proton transfer (Tajkhorshid et al., 2002). Aquaporin proteins assemble as homotetramers in the membrane, each individual monomer with a functioning water channel. The activity of each pore can be altered by opening and closing it (i.e., gating). Gating of aquaporins suggests a connection between cell signaling cascades and regulation of water transport. In plant aquaporins, phosphorylation of serine residues in loop B and the C-terminal region, as well as protonation of a histidine residue in loop D, are thought to promote conformational changes leading to the opening or closing of the pore (Maurel, 2007). Simulations of molecular dynamics revealed a putative additional, central pore of the tetramer, which can exhibit gas conductivity in addition to water transport (Wang and Tajkhorshid, 2007). Heteromerization, pH, calcium ions, and temperature may also play a role in gating (Chaumont et al., 2005).

18.2.2 Plant aquaporins The aquaporin family is particularly diverse and abundant in plants. While mammal species are known to have around 10 aquaporins, plant species harbor more than 30 aquaporin genes, as shown in Arabidopsis (35), maize (31), and rice (33) (Chaumont et al., 2001; Johanson and Gustavsson, 2002; Sakurai et al., 2005). Many of them, in contrast to the situation in animal cells, are located intracellularly (Maurel and Chrispeels, 2001). Some aquaporins have been shown to transport other small molecules such as glycerol, silicic acid, silicon, CO2, and hydrogen peroxide (Wallace et al., 2002; Heckwolf et al., 2011; Grégoire et al., 2012; Hooijmaijers et al., 2012; Uehlein et al., 2012; Deshmukh et al., 2013). Aquaporin proteins have been implicated in the transport of aluminum into Hydrangea sepals (Negishi et al., 2012). The structural properties of the aquaporins involved in transporting substances other than water were reviewed by Hove and Bhave (2011). Plant aquaporins are divided into four subfamilies on the basis of phylogenetic analyses, and individual aquaporin genes are often referred to as isoforms. The plasma membrane intrinsic protein (PIP) subfamily was named because its isoforms are predominantly located in the cellular membrane. This is the largest subfamily of plant aquaporins, with 13 members identified in Arabidopsis; it has been further divided into PIP1 and PIP2 subgroups with differentiation that predates the divergence of bryophytes and tracheophytes (Borstlap, 2002). From a structural point of view, PIP2 isoforms have a shorter amino-terminal extension, a longer carboxy-terminal end, and a longer first extracytosolic loop than PIP1 isoforms (Kaldenhoff and Fischer, 2006). From a functional perspective, PIP2 isoforms display considerably higher permeability (Weig et al., 1997); in fact, PIP1 isoforms showed little or no aquaporin activity when tested in Xenopus oocytes. However, in planta, PIP1 aquaporins are important for cell permeability

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as shown by lower water permeability in root cell protoplasts of tobacco and Arabidopsis PIP1 antisense plants (Kaldenhoff and Fischer, 2006). In addition, coexpression studies of PIP1 and PIP2 aquaporins in Xenopus oocytes suggested that PIP1 aquaporins may be activated by PIP2 isoforms (Mahdieh et al., 2008; Alleva et al., 2010; Bellati et al., 2010). PIP aquaporins are thought to play a key role in transcellular water transport. Although the tonoplast membrane is generally more permeable than the plasma membrane, the conductivity of isolated protoplasts has a broader range of values than isolated vacuoles, indicating that control of transcellular water flow probably resides in the plasma membrane (Martre et al., 2002). Tonoplast intrinsic proteins (TIP) were also named according to the predominant subcellular localization of their isoforms, where they mediate water exchange between cytosolic and vacuolar compartments and have been suggested to play a key role in cell osmoregulation (Maurel et al., 1997). In addition, the abundant presence of TIPs on the vacuolar membrane has been related to substantial water flux because it has been suggested that the intracellular matrix around the organelles and the longer route the water molecules may have to traverse when they are not passing through vacuoles, thus impeding the rapid flux of water (Ishibashi et al., 2011; Pou et al., 2013). Ten identified isoforms in Arabidopsis constitute a diverse subfamily, with five subgroups (TIP1TIP5) uncovered by phylogenetic studies in maize and Arabidopsis (Johanson et al., 2001). The diversification of TIP sequences is thought to have occurred relatively late in evolution— during the evolution of tracheophytes (Borstlap, 2002). Nodulin26-like intrinsic proteins (NIP) were so named because of their similarity to the first described member of the NIP subfamily—a protein expressed in the peribacteroid membrane in nitrogen-fixing nodules of soybean (Fortin et al., 1987). NIPs are known to facilitate movement of glycerol and ammonia in addition to water and are thought to have been acquired early in the evolution of plants by horizontal gene transfer of a bacterial aquaporin (Zardoya et al., 2002). In addition to these three subfamilies, another group of aquaporins—that is, small basic intrinsic proteins (SIP)—was identified by database mining and detailed phylogenetic analyses. SIP amino acid sequences are different from the other three subfamilies in many positions including those inside the pore, suggesting potential differences in the substrate selectivity of this subfamily (Johanson and Gustavsson, 2002). In Arabidopsis, three SIP homologs were identified and shown to reside mainly in the endoplasmic reticulum (Maurel et al., 2008). A novel category of major intrinsic proteins, which share weak similarities with previously identified aquaporin subfamilies, was identified in land plants and named X (for unrecognized) intrinsic proteins (XIPs) (Danielson and Johanson, 2008). Of all the flowering plants shown to have XIPs, the genus Populus carries the broadest range and the highest polymorphism of XIP isoforms (Lo´pez et al., 2012). The plasma membrane intrinsic protein and the tonoplast intrinsic protein subfamilies are thought to represent the central pathways for trans- and intracellular plant water transport; this is because of their abundance in plant tissues (Maurel, 2007) and, in case of the PIP subfamily, strict water selectivity (Wallace and Roberts, 2004).

18.2.3 Aquaporins in the plantwater relationship Studies on a number of plant species have implicated aquaporins in diverse physiological processes. These include cell expansion (Ludevid et al., 1992; Kaldenhoff et al., 1995), cell differentiation

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(Kaldenhoff et al., 1995), root hydraulic conductance (Martre et al., 2002; Siefritz et al., 2002), substantial water flow through tissues (Barrieu et al., 1998; Kirch et al., 2000; Otto and Kaldenhoff, 2000), diurnal responses (Henzler et al., 1999; Beaudette et al., 2007), embolism repair (Secchi and Zwieniecki, 2010), and responses to various stresses (Gaspar et al., 2003; Picaud et al., 2003; Jang et al., 2004; Alexandersson et al., 2005; Boursiac et al., 2005; Sakurai et al., 2005; Secchi et al., 2007). Important insights into the involvement of aquaporins in the plantwater relationship came from studies with mercury compounds (i.e., mercuric chloride, in particular) as aquaporin inhibitors. Many studies have confirmed that HgCl2 treatment impairs water transport in the plant and results in reduced hydraulic conductivity, which is attributed to the inhibition of aquaporins (Maggio and Joly, 1995; Wan and Zwiazek, 1999; Martre et al., 2001). Mercury inhibition is thought to occur through covalent modification of cysteine residues within the water pore and in other parts of the protein causing conformational changes; this results in the stoppage of water transport and can be reversed by 2-mercaptoethanol (Preston et al., 1992; Barone et al., 1998). However, some of the observed effects may not be related to impaired aquaporin activity because mercury compounds affect cysteine residues in other proteins as well (Patra and Sharma, 2000). In addition, some functionally characterized aquaporins appear to be mercury-insensitive (Biela et al., 1999). A less ambiguous insight into the function of aquaporins comes from expression studies and transgenic experiments. The tobacco PIP1 aquaporin NtAQP1 has been shown to be present in cells controlling water flow between symplast and apoplast; for example, cells associated with vascular elements, the xylem parenchyma, cells of the exo- and endodermis, and of the root cortex (Otto and Kaldenhoff, 2000). Inhibition of NtAQP1 expression in antisense transgenic plants reduced the root hydraulic conductivity by 55% compared to the control (Siefritz et al., 2002). In Arabidopsis, antisense inhibition of aquaporins of the PIP1 and/or PIP2 subclasses reduced root hydraulic conductivity by approximately 50% (Martre et al., 2002); while two allelic Arabidopsis PIP2;2 knockout mutants showed, with respect to wild-type plants, a reduction of 25 to 30% in the conductivity of root cortex cells (Javot et al., 2003). In Zea mays, ZmPIP2;1 and ZmPIP2;5 proteins were found to be present in the exodermis and endodermis cells of the root and ZmPIP2;5 also was localized on the external side of epidermal cells in root apices (Hachez et al., 2006). Studies such as these provided functional evidence that aquaporins contribute significantly to radial water movement and water uptake by roots. Some aquaporin isoforms are preferentially expressed in vascular tissue cell types; for example, high expression levels of some PIP and TIP isoforms have been reported in parenchyma cells around metaxylem in maize roots and stems (Barrieu et al., 1998) and phloem tissues of sunflower (Sarda et al., 1997). In many plant species, aquaporins are present in all leaf tissues but are preferentially expressed in the vascular bundles (Prado and Maurel, 2013). It has been proposed that aquaporins in the leaf play a role in mediating water transfer from the veins to the stomatal chamber. In sunflower, the transcript levels of a TIP aquaporin (SunTIP7) were markedly and systematically increased during stomatal closure (Sarda et al., 1997), while in grapevine (Vitis vinifera) leaves, a strong correlation was found between stomatal conductance and transcript abundance of the VvTIP2;1 isoform (Pou et al., 2013). In Arabidopsis leaves, a PIP1 aquaporin was significantly expressed in the protoxylem and protophloem of the vascular bundles as well as in the parenchyma cells surrounding them (Kaldenhoff et al., 1995; Maurel et al., 2008). Patterns of expression described previously indicate a general role of aquaporins in sap transport throughout the plant. In addition to this, a link between aquaporin expression and plant transpiration

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has been suggested. Enhanced activity of leaf aquaporins during the day may favor transport into the inner leaf tissues during maximal transpiration, which would prevent very low leaf water potentials and reduce xylem tensions and embolism (Maurel et al., 2008). Many aquaporins have a diurnal expression with a marked daytime peak (Lo´pez et al., 2003; Beaudette et al., 2007; Vandeleur et al., ˇ 2009; Surbanovski et al., 2013), suggesting that aquaporin levels may play a role in regulating water movement in accordance with the plant’s needs during the lightdark cycle. Interestingly, in rice the diurnal up-regulation of several PIP aquaporins was arrested when plants were grown at 100% relative humidity even in the presence of light, suggesting that transpirational demand itself may be involved in controlling the diurnal expression peaks (Sakurai-Ishikawa et al., 2011).

18.2.4 Aquaporins’ response to abiotic stress Aquaporins are remarkably responsive to various abiotic stresses, and a number of investigations have been conducted regarding the impact of salinity, cold, and drought on these proteins (Jang et al., 2004; Alexandersson et al., 2005; Boursiac et al., 2005; Sakurai et al., 2005; Galmés et al., 2007).

18.2.4.1 Drought Given the significant impact of drought on crop production globally (Grant, 2012), it is not surprising that there is a lot of interest in determining the impact of drought on aquaporin expression. Responses of aquaporins to drought stress are very diverse and depend on the investigated species, tissue, subfamily, isoform, and level of stress used in the study. Studies trying to relate physiological responses to water stress with expression patterns of different aquaporins have led to disparate results, mainly because the patterns of aquaporin expression are complex and different aquaporin isoforms may be involved in distinct responses (Alexandersson et al., 2005). For example, in olive trees subjected to drought treatment, the transcript levels of two PIP genes (OePIP1;1 and OePIP2;1) and one TIP gene (OeTIP1;1) diminished substantially in leaves, roots, and twigs (Secchi et al., 2006, 2007). On the other hand, in a study on recovery from xylem embolism in Populus trichocarpa, stem parenchyma cells responded to drought stress with considerable upregulation of the PIP1 subfamily but not the PIP2 subfamily (Secchi and Zwieniecki, 2010). In the root system of tobacco plants, drought stress significantly decreased PIP transcript levels of two investigated genes, NtPIP1;1 and NtPIP2;1, but increased the abundance of NtAQP1 transcripts (Mahdieh et al., 2008). A study of five PIP and two TIP aquaporins in leaves of Vitis plants showed that aquaporin expression varied depending on isoform and the plant organ investigated; however, in the leaves all genes showed a decrease of expression under moderate water stress and an increase under severe water stress (Galmés et al., 2007). Several comprehensive studies of Arabidopsis aquaporin expression showed relatively concordant results regarding response to drought stress (Weig et al., 1997; Jang et al., 2004; Alexandersson et al., 2005). These studies showed that most PIP and TIP genes were downregulated following drought stress; however, two aquaporin genes were up-regulated (AtPIP1;4 and AtPIP2;5) and another two were unaffected (AtPIP2;6 and AtSIP1;1). Common for the AtPIP1;4, AtPIP2;5, and AtPIP2;6 genes is that they were expressed at low levels in roots. A general downregulation was also observed at the protein level for PIP1 and PIP2 isoforms, showing a clear link between mRNA and protein abundance (Alexandersson et al., 2005). Many of the AtPIP and AtTIP genes that were down-regulated under drought stress were significantly coexpressed; the overall

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transcriptional response of PIPs to drought stress was preserved between five different accessions of Arabidopsis with varying water-use efficiency (WUE) and different geographical origin, suggesting a general and fundamental physiological role of this response (Alexandersson et al., 2010). It has been shown in Fragaria that down-regulation of root aquaporins can be fine-tuned to the intensity of drought stress, with the expression of abundant PIP aquaporins in the root significantly ˇ correlated to substrate moisture content (Surbanovski et al., 2013). In Arabidopsis, principal component analysis showed that most of the PIP transcriptional variation during drought stress could be explained by one variable linked to leaf water content (Alexandersson et al., 2010); however, the mechanisms underlying the correlation between water content and aquaporin transcriptional response remain to be elucidated. Causes of variation between investigations as to whether aquaporins are up- or down-regulated, in addition to differences related to the individual roles of aquaporin isoforms, may include the interaction of drought with the impact of irradiation, or the leaf developmental stage, which are known to affect aquaporin expression (Besse et al., 2011; Prado et al., 2013). It has also been suggested that differences between species in whether aquaporins are up-regulated or down-regulated may partially relate to whether the species are isohydric or anisohydric (Grant, 2012; Prado and Maurel, 2013). Under drought stress conditions, isohydric plants tend to close stomata to maintain leaf water potential, whereas anisohydric plants have less stomatal control. Tissue hydraulic performance is more important in the latter case, and there are examples of enhanced TIP expression in leaves of anisohydric species during water deficiency (Sade et al., 2012). Another example where water stress can coincide with substantial water movement through the plant is where plants are grown under low humidity; rice exposed to low humidity increased its transpiration rate 1.5- to 2-fold compared to that of rice grown under high humidity. This increased transpiration coincided with up-regulation of many PIP and TIP genes in both leaves and roots (Kuwagata et al., 2012). Separately, several rice aquaporin proteins have been found to be responsive to gradually-imposed drought, with a rapid reduction in their abundance once the plants were rewatered (Mirzaei et al., 2012). On the other hand, a reduction in the abundance of various rice aquaporin transcripts during drought has also been reported (Yooyongwech et al., 2013). Water deficit results in an increase in the synthesis of abscisic acid (ABA), which in turn induces stomatal closure (Davies et al., 2000). Although down-regulation of PIP2 aquaporins after ABA treatment has been reported in radish seedlings (Suga et al., 2002), more often aquaporin genes, when responsive, were up-regulated by this hormone (Jang et al., 2004; Guo et al., 2006; Parent et al., 2008). Jang et al. (2004) reported up-regulation for five PIP isoforms in the aerial parts and six isoforms in the root of Arabidopsis, while down-regulation was reported for one isoform in the root. A correlation between the response to salt stress and the response to ABA treatment of isoform AtPIP1;2 was observed. Isoform AtPIP2;5, however, showed a lack of correlation between responses to cold and drought stresses, which up-regulated the gene, and ABA treatment that did not elicit any response. The authors concluded that both ABA-dependent and ABAindependent signaling pathways may be involved in regulation of aquaporin expression. Shatil-Cohen et al. (2011) found that ABA fed to leaves via the petiole reduced leaf hydraulic conductance, but that ABA smeared on leaves did not. They suggested that ABA plays a role other than that of inducing stomatal closure. More recently, Pantin et al. (2013) proposed that ABA plays a dual role through its effect on guard cells and by decreasing water permeability within leaf vascular tissues. The authors also found that ABA uptake, drought, and aquaporin-blocking using HgCl2

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led to decreased osmotic water permeability of the bundle sheet cells but not of the mesophyll cells, indicating stress-regulated aquaporin activity specific to bundle sheet cells.

18.2.4.2 Salinity Salinity is another stress of increasing relevance in agronomy and is currently a focus of intensive crop science research (Plaut et al., 2013; Shabala, 2013; Shahbaz and Ashraf, 2013; Shavrukov, 2013). It has been demonstrated with many plant species that water transport activity is reduced in plant tissues under salinity stress (Azaizeh and Steudle, 1991; Boursiac et al., 2005; Lo´pezBerenguer et al., 2008; Horie et al., 2011). A study of Arabidopsis reported that as tissue water content declined during the first 2 to 5 h of salinity stress, extensive down-regulation of aquaporin gene expression occurred, probably to limit initial water loss. This was followed by up-regulation of some isoforms accompanying the recovery of tissue water content (Maathuis et al., 2003). The same study showed that both the down-regulation and subsequent up-regulation occur earlier for the PIP subfamily than for the TIP isoforms. Boursiac et al. (2005) found that in Arabidopsis all PIP and TIP aquaporin transcripts with a strong expression signal showed a 60 to 75% decrease in their abundance between 2 and 4 h following salt treatment; the authors also observed changes at the protein level and subcellular relocation of aquaporin proteins. Exposure to salt appeared to involve reactive oxygen species (ROS) signaling pathways and led to internalization of PIP proteins in order to down-regulate root water transport (Boursiac et al., 2008). The relocalization mechanism in response to salt treatment has been shown to be linked to phosphorylation of serine residues at the C-terminal end of the protein (Prak et al., 2008). Salt stress induced similar effects in other plant species. For example, maize roots responded to salinity by down-regulating PIP protein levels, which was in accordance with the hydraulic conductance decrease. Notably, ZmPIP1 isoforms were reduced to a lesser extent than the ZmPIP2 isoforms (Martıńez-Ballesta et al., 2008). In roots of barley (Hordeum vulgare), severe salinity stress significantly reduced root hydraulic conductivity (Lpr) and the accumulation of HvPIP mRNAs (Horie et al., 2011). Under relatively mild stress, however, only a moderate reduction in Lpr with no significant difference in HvPIP mRNA levels compared to the control was observed, perhaps indicating changes on the protein level. Greatly increased aquaporin cycling (i.e., repeated endocytosis and exocytosis of the proteins) has been detected in the early phase of root cell responses to salt stress (Luu et al., 2012; Martinie`re et al., 2012).

18.2.4.3 Nutrient deficiency Nutrient deficiency often occurs concurrently with drought stress because limited transpiration leads to a limited uptake of water and nutrients. Thus, for example, in Mediterranean climate zones, plants are subjected simultaneously to drought, temperature, and nutrient stress. Agronomy is highly reliant on the use of artificial fertilizer, an increasingly unsustainable situation given the energy and other resources involved in its production. For these reasons, and because understanding the impact of particular ions may enhance understanding of aquaporin regulation, there have been a few investigations of aquaporin responses to deficiency of a particular nutrient. A down-regulation of water channels under nitrogen (N) and phosphorus (P) deprivation was invoked on the basis of the insensitivity of residual root hydraulic conductivity to mercury (Clarkson et al., 2000). In Arabidopsis, calcium (Ca21) starvation evoked a general and consistent decrease in aquaporin transcripts for many isoforms in all subfamilies, but this response did not considerably

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affect the water relations at the whole plant level. However, as the activity of aquaporin proteins is negatively regulated by Ca21 ions, down-regulation may be a compensatory mechanism to limit aquaporin activity in conditions when Ca21 is unavailable (Maathuis et al., 2003). The same study showed that potassium (K1) starvation mainly affected plasma-membrane expressed aquaporins by initially inducing their expression and then down-regulating them. Coregulation of aquaporins and potassium transport systems has also been described (Liu et al., 2006).

18.2.4.4 Chilling Many agriculturally important crops (e.g., rice, soybean, maize, and cotton) are sensitive to chilling and unable to survive freezing temperatures (Larcher, 1995). In Arabidopsis after cold stress, most of the PIP genes (except AtPIP2;5) were down-regulated (Jang et al., 2004). Similarly, cold treatment markedly decreased mRNA levels of 10 aquaporin genes in roots of rice and the transcription levels recovered after warming (Sakurai et al., 2005). Another study of rice showed that some acclimation to cold was evident and possibly linked to aquaporin expression. Low temperature (10 C) treatment of the roots dramatically reduced root osmotic hydraulic conductivity within 1 h. The osmotic hydraulic conductivity gradually increased, however, during prolonged low temperature treatment, and a coordinated up-regulation of root aquaporin gene expression, particularly OsPIP2;5, was also observed (Ahamed et al., 2012). In a separate study, expression of both OsPIP2;5 and OsPIP2;4 in the roots was up-regulated after 6 days with roots at 13 C (Kuwagata et al., 2012); the authors hypothesized that low root temperature reduced water uptake, resulting in some similarity of responses with those shown under low humidity.

18.2.5 Aquaporins in tolerance of abiotic stress Studies in which overexpressing or silencing of aquaporins in plants has been investigated showed highly variable results (Aharon et al., 2003; Katsuhara et al., 2003; Lian et al., 2004). However, several studies reported aquaporin isoforms, which when overexpressed, conferred increased tolerance to water stress. In rice, the gene RWC3 (OsPIP1;3 isoform) was reported to improve tolerance through drought avoidance when expressed in drought-sensitive lines under the control of a stressinduced promoter. Overexpression of this isoform increased the Lpr, leaf water potential, and cumulative transpiration in drought-sensitive lines under drought stress induced by polyethylene glycol (PEG) 6000 treatment; the transformed plants had a normal phenotype. In addition, the same aquaporin isoform conferred an enhanced level of chilling tolerance to transgenic rice plants overexpressing it (Matsumoto et al., 2009). Another rice PIP aquaporin, OsPIP1;1, has been implicated in increased tolerance to stress— namely, overexpression of OsPIP1;1 altered many physiological features of transgenic plants in a dosage-dependent manner; however, moderate expression of OsPIP1;1 increased rice seed yield, salt resistance, root hydraulic conductivity, and seed germination rate (Liu et al., 2013). Recently in banana plants, expression of the aquaporin isoform MusaPIP1;2 was studied in the context of improved stress tolerance; the results showed that transgenic lines overexpressing MusaPIP1;2 displayed better abiotic stress survival characteristics. In addition, the transgenic banana plants had lower malondialdehyde content, elevated proline content, higher relative water content, and better photosynthetic efficiency compared to respective controls under different abiotic stress conditions.

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The transformed plants in the study had a normal phenotype, and it may prove to be a valuable tool for this important agricultural crop (Sreedharan et al., 2013). Constitutive expression of a tomato TIP, SlTIP2;2, resulted in plants transpiring more and for longer than controls, therefore reaching lower water potentials (Sade et al., 2009). This behavior is thought to be anisohydric and was beneficial for tomato, resulting in higher yields, harvest index, and plant biomass under both drought and well-watered conditions. Thus, rather than aquaporin expression depending on isohydry, as suggested earlier, isohydry may be determined by aquaporin expression. In another transgenics study, Arabidopsis overexpressing PIP1;4 and PIP2;5 did not initially show the reduction in Lpr due to root cooling that was seen in wild-type plants (Lee et al., 2012). After five days of low root temperature, Lpr was still not reduced in plants overexpressing PIP2;5; however, it did fall in plants overexpressing PIP1;4, suggesting that gating of PIP1;4 may be more sensitive to longer term cold stress. Unlike wild-type and PIP1;4 mutants, plants overexpressing PIP2;5 did not show a reduction in growth at low compared to controlled root temperatures, indicating a role of aquaporin-mediated water transport for growth in low temperature conditions. Although investigating aquaporin overexpression in homologuous systems is considered the most relevant approach, some studies with heterologous expression also have shown promising results. For example, overexpression of a TIP, TsTIP1;2, from the halophyte Thellungiella salsuginea in Arabidopsis increased tolerance to drought, salt, and oxidative stresses (Wang et al., 2013).

18.3 Conclusion and future prospects Novel technologies have allowed characterization of changes in transcript abundance in response to stress in a range of important plant species. In addition to expression studies, assessments of protein abundance, gating, and subcellular relocalization for individual isoforms should be integrated with physiological and biochemical investigations in order to unravel the importance of aquaporins in plant stress tolerance. For example, di Pietro et al. (2013) recently highlighted the importance of the phosphorylation status of aquaporins, rather than aquaporin abundance, in response to a range of environmental stresses; regulation of aquaporin trafficking is also emerging as an important mechanism for controlling the water permeability of membranes (Chaumont et al., 2005; Luu and Maurel, 2013). However, signaling pathways that regulate aquaporins on different levels and, ˇ particularly under various stress conditions (see Jang et al., 2004; Surbanovski et al., 2013), need further investigation. As with any studies of plant behavior in response to stress, it is essential that research on aquaporins takes into account the degree of stress; the rate at which that stress is imposed; and, where relevant, the rate of recovery (Sade et al., 2012). Stresses of similar duration, rate, and severity as to which plants are exposed in the field, and recovery in similar conditions as experienced in field crops, need to be the focus of new research efforts (Maurel et al., 2008). Additionally, the interaction of irradiance, leaf water status, and leaf developmental stage on leaf hydraulic conductivity (Prado and Maurel, 2013) complicates assessment of the impact of changes in any one factor. Similarly, root hydraulic conductance is affected by a range of variables. Therefore, it is critical that future investigations about the role of aquaporins in hydraulic conductance carefully monitor

References

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the plants’ environment, development, and physiology in parallel with molecular and biochemical assays. While this is challenging, it can also be seen as an ideal opportunity to integrate the wealth of diverse expertise currently present across the plant sciences. Finally, transgenic studies with aquaporins in homologous systems are beginning to play a major role in determining the effect of these highly responsive genes on plant growth and survival under stressful conditions. As suggested by Maurel et al. (2008) with respect to water stress, but of equal relevance to the other stress factors discussed in this chapter, the potential of manipulating aquaporin expression for biotechnological improvement of crops growing under abiotic stress must be thoroughly considered.

References Ahamed, A., Murai-Hatano, M., Ishikawa-Sakurai, J., Hayashi, H., Kawamura, Y., Uemura, M., 2012. Cold stress-induced acclimation in rice is mediated by root-specific aquaporins. Plant Cell. Physiol. 53, 14451456. Aharon, R., Shahak, Y., Wininger, S., Bendov, R., Kapulnik, Y., Galili, G., 2003. Overexpression of a plasma membrane aquaporin in transgenic tobacco improves plant vigor under favorable growth conditions but not under drought or salt stress. Plant Cell 15, 439447. Alexandersson, E., Fraysse, L., Sjo¨vall-Larsen, S., Gustavsson, S., Fellert, M., Karlsson, M., et al., 2005. Whole gene family expression and drought stress regulation of aquaporins. Plant Mol. Biol. 59, 469484. Alexandersson, E., Danielson, J.A.H., Rade, J., Moparthi, V.K., Fontes, M., Kjellbom, P., et al., 2010. Transcriptional regulation of aquaporins in accessions of Arabidopsis in response to drought stress. Plant J. 61, 650660. Alleva, K., Marquez, M., Villarreal, N., Mut, P., Bustamante, C., Bellati, J., et al., 2010. Cloning, functional characterization, and co-expression studies of a novel aquaporin (FaPIP2;1) of strawberry fruit. J. Exp. Bot. 61, 39353945. Azaizeh, H., Steudle, E., 1991. Effects of salinity on water transport of excised maize (Zea mays L.) roots. Plant Physiol. 97, 11361145. Barone, L.M., Mu, H.H., Shih, C.J., Kashlan, K.B., Wasserman, B.P., 1998. Distinct biochemical and topological properties of the 31- and 27-kilodalton plasma membrane intrinsic protein subgroups from red beet. Plant Physiol. 118, 315322. Barrieu, F., Chaumont, F., Chrispeels, M.J., 1998. High expression of the tonoplast aquaporin ZmTIP1 in epidermal and conducting tissues of maize. Plant Physiol. 117, 11531163. Beaudette, P.C., Chlup, M., Yee, J., Emery, R.J.N., 2007. Relationships of root conductivity and aquaporin gene expression in Pisum sativum: diurnal patterns and the response to HgCl2 and ABA. J. Exp. Bot. 58, 12911300. Bellati, J., Alleva, K., Soto, G., Vitali, V., Jozefkowicz, C., Amodeo, G., 2010. Intracellular pH sensing is altered by plasma membrane PIP aquaporin co-expression. Plant Mol. Biol. 74, 105118. Besse, M., Knipfer, T., Verdeil, J.L., Jahn, T.P., Fricke, W., 2011. Developmental pattern of aquaporin expression in barley (Hordeum vulgare L.) leaves. J. Exp. Bot. 62, 41274142. Biela, A., Grote, K., Otto, B., Hoth, S., Hedrich, R., Kaldenhoff, R., 1999. The Nicotiana tabacum plasma membrane aquaporin NtAQP1 is mercury-insensitive and permeable for glycerol. Plant J. 18, 565570. Borstlap, A.C., 2002. Early diversification of plant aquaporins. Trend Plant Sci. 7, 529530.

442


Boursiac, Y., Chen, S., Luu, D.T., Sorieul, M., van den Dries, N., Maurel, C., 2005. Early effects of salinity on water transport in Arabidopsis roots. Molecular and cellular features of aquaporin expression. Plant Physiol. 139, 790805. Boursiac, Y., Boudet, J., Postaire, O., Luu, D.-T., Tournaire-Roux, C., Maurel, C., 2008. Stimulus-induced downregulation of root water transport involves reactive oxygen species-activated cell signalling and plasma membrane intrinsic protein internalization. Plant J. 56, 207218. Chaumont, F., Barrieu, F., Wojcik, E., Chrispeels, M.J., Jung, R., 2001. Aquaporins constitute a large and highly divergent protein family in maize. Plant Physiol. 125, 12061215. Chaumont, F., Moshelion, M., Daniels, M.J., 2005. Regulation of plant aquaporin activity. Biol. Cell. 97, 749764. Clarkson, D.T., Carvajal, M., Henzler, T., Waterhouse, R.N., Smyth, A.J., Cooke, D.T., et al., 2000. Root hydraulic conductance: diurnal aquaporin expression and the effects of nutrient stress. J. Exp. Bot. 51, 6170. Danielson, J.A.H., Johanson, U., 2008. Unexpected complexity of the Aquaporin gene family in the moss Physcomitrella patens. BMC. Plant Biol. 8, 45. Davies, W.J., Bacon, M.A., Thompson, D.S., Sobeih, W., Rodrı´guez, L.G., 2000. Regulation of leaf and fruit growth in plants growing in drying soil: exploitation of the plants’ chemical signalling system and hydraulic architecture to increase the efficiency of water use in agriculture. J. Exp. Bot. 51, 16171626. Deshmukh, R.K., Vivancos, J., Guérin, V., Sonah, H., Labbé, C., Belzile, F., et al., 2013. Identification and functional characterization of silicon transporters in soybean using comparative genomics of major intrinsic proteins in Arabidopsis and rice. Plant Mol. Biol. 83, 303315. di Pietro, M., Vialaret, J., Li, G.W., Hem, S., Prado, K., Rossignol, M., et al., 2013. Coordinated posttranslational responses of aquaporins to abiotic and nutritional stimuli in Arabidopsis roots. Mol. Cell. Proteom. 12, 38863897. Fortin, M.G., Morrison, N.A., Verma, D.P., 1987. Nodulin-26, a peribacteroid membrane nodulin is expressed independently of the development of the peribacteroid compartment. Nucleic Acids Res. 15, 813824. Galmés, J., Pou, A., Alsina, M.M., Toma`s, M., Medrano, H., Flexas, J., 2007. Aquaporin expression in response to different water stress intensities and recovery in Richter-110 (Vitis sp.): relationship with ecophysiological status. Planta 226, 671681. Gaspar, M., Bousser, A., Sissoeff, I., Roche, O., Hoarau, J., Mahe, A., 2003. Cloning and characterization of ZmPIP1-5b, an aquaporin transporting water and urea. Plant Sci. 165, 2131. Gorin, M.B., Yancey, S.B., Cline, J., Revel, J.P., Horwitz, J., 1984. The Major Intrinsic Protein (MIP) of the bovine lens fiber membrane: characterization and structure based on cDNA cloning. Cell 39, 4959. Grant, O.M., 2012. Understanding and exploiting the impact of drought stress on plant physiology. In: Ahmad, P., Prasad, M.N.V. (Eds.), Abiotic Stress Responses in Plants—Metabolism, Productivity and Sustainability. Springer, New York, pp. 89104. Grégoire, C., Remus-Borel, W., Vivancos, J., Labbé, C., Belzile, F., Belanger, R.R., 2012. Discovery of a multigene family of aquaporin silicon transporters in the primitive plant Equisetum arvense. Plant J. 72, 320330. Guo, X., Zhu, Q., Zhu, J., Shen, Y., 2006. Effects of irrigation treatment on pear trees on the Loess Plateau in western Shanxi Province. J. Beijing Forest Univ. 28, 118122. Hachez, C., Moshelion, M., Zelazny, E., Cavez, D., Chaumont, F., 2006. Localization and quantification of plasma membrane aquaporin expression in maize primary root: a clue to understanding their role as cellular plumbers. Plant Mol. Biol. 62, 305323. Heckwolf, M., Pater, D., Hanson, D.T., Kaldenhoff, R., 2011. The Arabidopsis thaliana aquaporin AtPIP1;2 is a physiologically relevant CO2 transport facilitator. Plant J. 67, 795804.

References

443

Henzler, T., Waterhouse, R.N., Smyth, A.J., Carvajal, M., Cooke, D.T., Schaffner, A.R., et al., 1999. Diurnal variations in hydraulic conductivity and root pressure can be correlated with the expression of putative aquaporins in the roots of Lotus japonicus. Planta 210, 5060. Hooijmaijers, C., Rhee, J.Y., Kwak, K.J., Chung, G.C., Horie, T., Katsuhara, M., et al., 2012. Hydrogen peroxide permeability of plasma membrane aquaporins of Arabidopsis thaliana. J. Plant Res. 125, 147153. Horie, T., Kaneko, T., Sugimoto, G., Sasano, S., Panda, S.K., Shibasaka, M., et al., 2011. Mechanisms of water transport mediated by PIP aquaporins and their regulation via phosphorylation events under salinity stress in barley roots. Plant Cell. Physiol. 52, 663675. Hove, R.M., Bhave, M., 2011. Plant aquaporins with non-aqua functions: deciphering the signature sequences. Plant Mol. Biol. 75, 413430. Ishibashi, K., Kondo, S., Hara, S., Morishita, Y., 2011. The evolutionary aspects of aquaporin family. Amer. J. Physiol.—Regul., Integr. Comp. Physiol. 300, R566R576. Jang, J.Y., Kim, D.G., Kim, Y.O., Kim, J.S., Kang, H., 2004. An expression analysis of a gene family encoding plasma membrane aquaporins in response to abiotic stresses in Arabidopsis thaliana. Plant Mol. Biol. 54, 713725. Javot, H., Lauvergeat, V., Santoni, V., Martin-Laurent, F., Gu¨çlu¨, J., Vinh, J., et al., 2003. Role of a single aquaporin isoform in root water uptake. Plant Cell 15, 509522. Johanson, U., Gustavsson, S., 2002. A new subfamily of major intrinsic proteins in plants. Mol. Biol. Evol. 19, 456461. Johanson, U., Karlsson, M., Johansson, I., Gustavsson, S., Sjovall, S., Fraysse, L., et al., 2001. The complete set of genes encoding major intrinsic proteins in Arabidopsis provides a framework for a new nomenclature for major intrinsic proteins in plants. Plant Physiol. 126, 13581369. Jones, H.G., 1992. Plants and Microclimate: A Quantitative Approach to Environmental Plant Physiology. Cambridge University Press, Cambridge, UK. Jung, J.S., Preston, G.M., Smith, B.L., Guggino, W.B., Agre, P., 1994. Molecular structure of the water channel through aquaporin chip. The hourglass model. J. Biol. Chem. 269, 1464814654. Kaldenhoff, R., Fischer, M., 2006. Aquaporins in plants. Acta. Physiol. 187, 169176. Kaldenhoff, R., Kolling, A., Meyers, J., Karmann, U., Ruppel, G., Richter, G., 1995. The blue light responsive AthH2 gene of Arabidopsis thaliana is primarily expressed in expanding as well as in differentiating cells and encodes a putative channel protein of the plasmalemma. Plant J. 7, 8795. Katsuhara, M., Koshio, K., Shibasaka, M., Hayashi, Y., Hayakawa, T., Kasamo, K., 2003. Over-expression of a barley aquaporin increased the shoot/root ratio and raised salt sensitivity in transgenic rice plants. Plant Cell. Physiol. 44, 13781383. Kirch, H.-H., Vera-Estrella, R., Golldack, D., Quigley, F., Michalowski, C.B., Barkla, B.J., et al., 2000. Expression of water channel proteins in Mesembryanthemum crystallinum. Plant Physiol. 123, 111124. Knipfer, T., Fricke, W., 2010. Root pressure and a solute reflection coefficient close to unity exclude a purely apoplastic pathway of radial water transport in barley (Hordeum vulgare). New Phytol. 187, 159170. Koroleva, O.A., Tomos, A.D., Farrar, J., Pollock, C.J., 2002. Changes in osmotic and turgor pressure in response to sugar accumulation in barley source leaves. Planta 215, 210219. Kozono, D., Ding, X.D., Iwasaki, I., Meng, X.Y., Kamagata, Y., Agre, P., et al., 2003. Functional expression and characterization of an archaeal aquaporin—AqpM from Methanothermobacter marburgensis. J. Biol. Chem. 278, 1064910656. Kramer, P.J., Boyer, J.S., 1995. Water Relations of Plants and Soils. Academic Press, Boston. Kuwagata, T., Ishikawa-Sakurai, J., Hayashi, H., Nagasuga, K., Fukushi, K., Ahamed, A., et al., 2012. Influence of low air humidity and low root temperature on water uptake, growth and aquaporin expression in rice plants. Plant Cell. Physiol. 53, 14181431. Larcher, W., 1995. Physiological Plant Ecology. Springer, London.

444


Lee, S.H., Chung, G.C., Jang, J.Y., Ahn, S.J., Zwiazek, J.J., 2012. Overexpression of PIP2;5 aquaporin alleviates effects of low root temperature on cell hydraulic conductivity and growth in Arabidopsis. Plant Physiol. 159, 12911291. Lian, H.L., Xin, Y., Ye, Q., Ding, X.D., Kitagawa, Y., Kwak, S.S., et al., 2004. The role of aquaporin RWC3 in drought avoidance in rice. Plant Cell. Physiol. 45, 810810. Liu, C.W., Fukumoto, T., Matsumoto, T., Gena, P., Frascaria, D., Kaneko, T., et al., 2013. Aquaporin OsPIP1;1 promotes rice salt resistance and seed germination. Plant Physiol. Biochem. 63, 151158. Liu, H.Y., Sun, W.N., Su, W.A., Tang, Z.C., 2006. Co-regulation of water channels and potassium channels in rice. Physiol. Plant 128, 5869. Lo´pez, D., Bronner, G., Brunel, N., Auguin, D., Bourgerie, S., Brignolas, F., et al., 2012. Insights into Populus XIP aquaporins: evolutionary expansion, protein functionality, and environmental regulation. J. Exp. Bot. 63, 22172230. Lo´pez, F., Bousser, A., Sissoe¨ff, I., Hoarau, J., Mahé, A., 2003. Characterization in maize of ZmTIP2-3, a root-specific tonoplast intrinsic protein exhibiting aquaporin activity. J. Exp. Bot. 55, 539541. Lo´pez-Berenguer, C., Martıńez-Ballesta, M.C., Garcia-Viguera, C., Carvajal, M., 2008. Leaf water balance mediated by aquaporins under salt stress and associated glucosinolate synthesis in broccoli. Plant Sci. 174, 321328. Ludevid, D., Hofte, H., Himelblau, E., Chrispeels, M.J., 1992. The expression pattern of tonoplast intrinsic protein gamma-TIP in Arabidopsis thaliana is correlated with cell enlargement. Plant Physiol. 100, 16331639. Luu, D.-T., Maurel, C., 2005. Aquaporins in a challenging envrionment: molecular gears for adjusting plant water status. Plant Cell. Environ. 28, 8596. Luu, D.T., Maurel, C., 2013. Aquaporin trafficking in plant cells: an emerging membrane-protein model. Traffic 14, 629635. Luu, D.T., Martinie`re, A., Sorieul, M., Runions, J., Maurel, C., 2012. Fluorescence recovery after photobleaching reveals high cycling dynamics of plasma membrane aquaporins in Arabidopsis roots under salt stress. Plant J. 69, 894905. Maathuis, F.J.M., Filatov, V., Herzyk, P., Krijger, G.C., Axelsen, K.B., Chen, S.X., et al., 2003. Transcriptome analysis of root transporters reveals participation of multiple gene families in the response to cation stress. Plant J. 35, 675692. Maggio, A., Joly, R.J., 1995. Effects of mercuric chloride on the hydraulic conductivity of tomato root systems (evidence for a channel-mediated water pathway). Plant Physiol. 109, 331335. Mahdieh, M., Mostajeran, A., Horie, T., Katsuhara, M., 2008. Drought stress alters water relations and expression of PIP-type aquaporin genes in Nicotiana tabacum plants. Plant Cell. Physiol. 49, 801813. Martıńez-Ballesta, MdC, Bastıás, E, Zhu, C., Scha¨ffner, A.R., González-Moro, B., González-Murua, C., et al., 2008. Boric acid and salinity effects on maize roots. Response of aquaporins ZmPIP1 and ZmPIP2, and plasma membrane H1-ATPase, in relation to water and nutrient uptake. Physiol. Plant 132, 479490. Martinie`re, A., Li, X., Runions, J., Lin, J., Maurel, C., Luu, D.T., 2012. Salt stress triggers enhanced cycling of Arabidopsis root plasma-membrane aquaporins. Plant Signal Behav. 7, 529532. Martre, P., North, G.B., Nobel, P.S., 2001. Hydraulic conductance and mercury-sensitive water transport for roots of Opuntia acanthocarpa in relation to soil drying and rewetting. Plant Physiol. 126, 352362. Martre, P., Morillon, R., Barrieu, F., North, G.B., Nobel, P.S., Chrispeels, M.J., 2002. Plasma membrane aquaporins play a significant role during recovery from water deficit. Plant Physiol. 130, 21012110. Matsumoto, T., Lian, H., Su, W.A., Tanaka, D., Liu, C.W., Iwasaki, I., et al., 2009. Role of the aquaporin PIP1 subfamily in the chilling tolerance of rice. Plant Cell. Physiol. 50, 216229. Maurel, C., 2007. Plant aquaporins: novel functions and regulation properties. FEBS Lett. 581, 22272236.

References

445

Maurel, C., Chrispeels, M.J., 2001. Aquaporins. A molecular entry into plant water relations. Plant Physiol. 125, 135138. Maurel, C., Reizer, J., Schroeder, J.I., Chrispeels, M.J., 1993. The vacuolar membrane-protein gamma-tip creates water specific channels in Xenopus-oocytes. EMBO J. 12, 22412247. Maurel, C., Tacnet, F., Guclu, J., Guern, J., Ripoche, P., 1997. Purified vesicles of tobacco cell vacuolar and plasma membranes exibit dramatically different water permeability and water channel activity. Proc. Natl. Acad. Sci. USA 94, 71037108. Maurel, C., Verdoucq, L., Luu, D.-T., Santoni, V., 2008. Plant aquaporins: membrane channels with multiple integrated functions. Ann. Rev. Plant Biol. 59, 595624. Mirzaei, M., Pascovici, D., Atwell, B.J., Haynes, P.A., 2012. Differential regulation of aquaporins, small GTPases and V-ATPases proteins in rice leaves subjected to drought stress and recovery. Proteomic 12, 864877. Murata, K., Mitsuoka, K., Hirai, T., Walz, T., Agre, P., Heymann, J.B., et al., 2000. Structural determinants of water permeation through aquaporin-1. Nature 407, 599605. Negishi, T., Oshima, K., Hattori, M., Kanai, M., Mano, S., Nishimura, M., et al., 2012. Tonoplast- and plasma membrane-localized aquaporin-family transporters in blue hydrangea sepals of aluminum hyperaccumulating plant. PLoS ONE 7, e43189. Nilsson, H.-E., 1995. Remote sensing and image analysis in plant pathology. Ann. Rev. Plant Phytopathol. 15, 489527. Otto, B., Kaldenhoff, R., 2000. Cell-specific expression of the mercury-insensitive plasma-membrane aquaporin NtAQP1 from Nicotiana tabacum. Planta 211, 167172. Pantin, F., Monnet, F., Jannaud, D., Costa, J.M., Renaud, J., Muller, B., et al., 2013. The dual effect of abscisic acid on stomata. New Phytol. 197, 6572. Parent, B., Hachez, C., Redondo, E., Chaumont, F., Tardieu, F., 2008. ABA affects root hydraulic conductance and leaf growth via aquaporin content and activity. Compar. Biochem. Physiol. AMol. Integ. Physiol. 150, S196S197. Patra, M., Sharma, A., 2000. Mercury toxicity in plants. Bot. Rev. 66, 379422. Picaud, S., Becq, F., Dédaldéchamp, F., Ageorges, A., Delrot, S., 2003. Cloning and expression of two plasma membrane aquaporins expressed during the ripening of grape berry. Funct. Plant Biol. 30, 621630. Plaut, Z., Edelstein, M., Ben-Hur, M., 2013. Overcoming salinity barriers to crop production using traditional methods. Crit. Rev. Plant Sci. 32, 250291. Pou, A., Medrano, H., Flexas, J., Tyerman, S., 2013. A putative role for TIP and PIP aquaporins in dynamics of leaf hydraulic and stomatal conductances in grapevine under water stress and re-watering. Plant Cell. Environ. 36, 828843. Prado, K., Maurel, C., 2013. Regulation of leaf hydraulics: from molecular to whole plant levels. Frontiers Plant Sci. 4, 255. Prado, K., Boursiac, Y., Tournaire-Roux, C., Monneuse, J.M., Postaire, O., Da Ines, O., et al., 2013. Regulation of Arabidopsis leaf hydraulics involves light-dependent phosphorylation of aquaporins in veins. Plant Cell. 25, 10291039. Prak, S., Hem, S., Boudet, J., Viennois, G., Sommerer, N., Rossignol, M., et al., 2008. Multiple phosphorylations in the C-terminal tail of plant plasma membrane aquaporins role in subcellular trafficking of AtPIP2;1 in response to salt stress. Mol. Cell. Proteom. 7, 10191030. Preston, G.M., Carroll, T.P., Guggino, W.B., Agre, P., 1992. Appearance of water channels in Xenopus oocytes expressing red-cell chip28 protein. Science 256, 385387. Sade, N., Vinocur, B.J., Diber, A., Shatil, A., Ronen, G., Nissan, H., et al., 2009. Improving plant stress tolerance and yield production: is the tonoplast aquaporin SlTIP2;2 a key to isohydric to anisohydric conversion? New Phytol. 181, 651661.

446


Sade, N., Gebremedhin, A., Moshelion, M., 2012. Risk-taking plants: anisohydric behavior as a stressresistance trait. Plant Signal. Behav. 7, 767770. Sakurai, J., Ishikawa, F., Yamaguchi, T., Uemura, M., Maeshima, M., 2005. Identification of 33 rice aquaporin genes and analysis of their expression and function. Plant Cell. Physiol. 46, 15681577. Sakurai-Ishikawa, J., Murai-Hatano, M., Hayashi, H., Ahamed, A., Fukushi, K., 2011. Transpiration from shoots triggers diurnal changes in root aquaporin expression. Plant Cell. Environ. 34, 11501163. Sarda, X., Tousch, D., Ferrare, K., Legrand, E., Dupuis, J.M., Casse-Delbart, F., et al., 1997. Two TIP-like genes encoding aquaporins are expressed in sunflower guard cells. Plant J. 12, 11031111. Secchi, F., Zwieniecki, M.A., 2010. Patterns of PIP gene expression in Populus trichocarpa during recovery from xylem embolism suggest a major role for the PIP1 aquaporin subfamily as moderators of refilling process. Plant Cell. Environ. 33, 12851297. Secchi, F., Lovisolo, C., Uehlein, N., Kaldenhoff, R., Schubert, A., 2006. Isolation and functional characterization of three aquaporins from olive (Olea europaea L.). Planta 225, 381392. Secchi, F., Lovisolo, C., Schubert, A., 2007. Expression of OePIP2.1 aquaporin gene and water relations of Olea europaea twigs during drought stress and recovery. Ann. Appl. Biol. 150, 163167. Shabala, S., 2013. Learning from halophytes: physiological basis and strategies to improve abiotic stress tolerance in crops. Annal. Bot. 112, 12091221. Shahbaz, M., Ashraf, M., 2013. Improving salinity tolerance in cereals. Crit. Rev. Plant Sci. 32, 237249. Shatil-Cohen, A., Attia, Z., Moshelion, M., 2011. Bundle-sheath cell regulation of xylem-mesophyll water transport via aquaporins under drought stress: a target of xylem-borne ABA? Plant J. 67, 7280. Shavrukov, Y., 2013. Salt stress or salt shock: which genes are we studying? J. Exp. Bot. 64, 119127. Siefritz, F., Tyree, M.T., Lovisolo, C., Schubert, A., Kaldenhoff, R., 2002. PIP1 plasma membrane aquaporins in tobacco: from cellular effects to function in plants. Plant Cell. 14, 869876. Sreedharan, S., Shekhawat, U.K.S., Ganapathi, T.R., 2013. Transgenic banana plants overexpressing a native plasma membrane aquaporin MusaPIP1;2 display high tolerance levels to different abiotic stresses. Plant Biotechnol. J. 11, 942952. Steudle, E., 2000. Water uptake by roots: effects of water deficit. J. Exp. Bot. 51, 15311542. Steudle, E., Peterson, C.A., 1998. How does water get through roots? J. Exp. Bot. 49, 775788. Suga, S., Komatsu, S., Maeshima, M., 2002. Aquaporin isoforms responsive to salt and water stresses and phytohormones in radish seedlings. Plant Cell. Physiol. 43, 12291237. Sui, H.X., Han, B.G., Lee, J.K., Walian, P., Jap, B.K., 2001. Structural basis of water-specific transport through the AQP1 water channel. Nature 414, 872878. ˇ Surbanovski, N., Sargent, D.J., Else, M.A., Simpson, D.W., Zhang, H., Grant, O.M., 2013. Expression of Fragaria vesca PIP aquaporins in response to drought stress: PIP down-regulation correlates with the decline in substrate moisture content. PLoS ONE 8, e74945. Tajkhorshid, E., Nollert, P., Jensen, M., Miercke, L.J.W., O’Connell, J., Stroud, R.M., et al., 2002. Control of the selectivity of the aquaporin water channel family by global orientational tuning. Science 296, 525530. Tyerman, S.D., Niemietz, C.M., Bramley, H., 2002. Plant aquaporins: multifunctional water and solute channels with expanding roles. Plant Cell. Environ. 25, 173194. Uehlein, N., Sperling, H., Heckwolf, M., Kaldenhoff, R., 2012. The Arabidopsis aquaporin PIP1;2 rules cellular CO2 uptake. Plant Cell. Environ. 35, 10771083. Vandeleur, R.K., Mayo, G., Shelden, M.C., Gilliham, M., Kaiser, B.N., Tyerman, S.D., 2009. The role of plasma membrane intrinsic protein aquaporins in water transport through roots: diurnal and drought stress responses reveal different strategies between isohydric and anisohydric cultivars of grapevine. Plant Physiol. 149, 445460.

References

447

Wallace, I.S., Roberts, D.M., 2004. Homology modeling of representative subfamilies of Arabidopsis major intrinsic proteins. Classification based on the aromatic/arginine selectivity filter. Plant Physiol. 135, 10591068. Wallace, I.S., Willis, D.M., Guenther, J.F., Roberts, D.M., 2002. Functional selectivity for glycerol of the nodulin, 26 subfamily of plant membrane intrinsic proteins. FEPBS Lett. 523, 109112. Wan, X., Zwiazek, J.J., 1999. Mercuric chloride effects on root water transport in aspen seedlings. Plant Physiol. 121, 939946. Wang, L.L., Chen, A.P., Zhong, N.Q., Liu, N., Wu, X.M., Wang, F., et al., 2013. The Thellungiella salsuginea tonoplast aquaporin TsTIP1;2 functions in protection against multiple abiotic stresses. Plant Cell. Physiol. 55, 148161. Wang, Y., Tajkhorshid, E., 2007. Molecular mechanisms of conduction and selectivity in aquaporin water channels. J. Nutr. 137, 1509S1515S. Weig, A., Deswarte, C., Chrispeels, M., 1997. The major intrinsic protein family of Arabidopsis has, 23 members that form three distinct groups with functional aquaporins in each group. Plant Physiol. 114, 13471357. Yooyongwech, S., Cha-um, S., Supaibulwatana, K., 2013. Water relation and aquaporin genes (PIP1;2 and PIP2;1) expression at the reproductive stage of rice (Oryza sativa L. spp. indica) mutant subjected to water deficit stress. Plant Omic. 6, 7985. Zardoya, R., Ding, X.D., Kitagawa, Y., Chrispeels, M.J., 2002. Origin of plant glycerol transporters by horizontal gene transfer and functional recruitment. Proc. Natl. Acad. Sci. USA 99, 1489314896.


CHAPTER

Prospects of Field Crops for Phytoremediation of Contaminants

19

Poonam, Renu Bhardwaj, Resham Sharma, Neha Handa, Harpreet Kaur, Ravdeep Kaur, Geetika Sirhindi and A.K. Thukral

19.1 Introduction Soil is being degraded as a result of industrial, agricultural, and civil activities worldwide, and there is no way to avoid exposure of it to toxic chemicals and metals. Soil contamination, whether diffused or localized, causes loss of various soil functions and also leads to contamination of surface and groundwater. Diffusion from the atmosphere, flowing water, and eroded soil itself are the main sources of soil pollution. Other than this, the application of pesticides and fertilizers, sewage sludge, dust from smelters, industrial waste, and inefficient watering practices of agricultural lands causes contamination (Schwartz et al., 2001; Passariello et al., 2002). Brown fields, a term given to contaminated soils (French et al., 2006), are mostly associated with abandoned industrial plants, accidental release of pollutants, and inappropriate municipal and industrial waste disposal sites. Risk of contamination from the mining industry, which is a foremost cause of land degradation, is associated with sulfur and metal-bearing tailing sites and with the use of chemicals required in the refining processes (EEA, 2003). There are various organic contaminants, primarily petroleum hydrocarbons, aromatic hydrocarbons, polynuclear aromatic hydrocarbons (PAHs), nitroaromatic compounds (NACs) and chloroaromatics, and so on, and inorganic pollutants including heavy metals such as cadmium (Cd), copper (Cu), mercury (Hg), nickel (Ni), lead (Pb), zinc (Zn), and arsenic (As). According to a 2003 European Economic Area (EEA) report, metal accounts for more than 37% of the contamination, followed by mineral oil (33.7%), PAHs (13.3%), and others. The term “soil remediation” means returning the soil to a form of ecological stability together with the establishment of the plant communities it supported prior to disturbance (Allen, 1988). Conventional technologies of soil remediation include soil washing with chemicals and addition of lime, phosphate, calcium carbonate, and more as needed (Ebbs et al., 1998; Krebs et al., 1999; Chen et al., 2000); however, most of them are not ecofriendly and sustainable. Phytoremediation is an integrated multidisciplinary approach for the cleaning of contaminated soils (Cunningham and Ow, 1996; Maurice and Lagerkvist, 2000). It is a group of technologies that uses plants to reduce, remove, degrade, or immobilize environmental pollutants, and its aim is to restore polluted sites so that they are usable. In the past, this technique has been applied to various pollutants in small-scale, laboratory studies. The pollutants treated include heavy metals,


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CHAPTER 19 Prospects of Field Crops for Phytoremediation of Contaminants

chlorinated solvents, polychlorinated benzenes (PCBs), PAHs, organophosphate insecticides, radionuclides, explosives, and surfactants (Khan et al., 2004). Some plant species can accumulate higher concentrations of pollutants without showing toxicity (Klassen et al., 2000; Bennet et al., 2003); such plants must possess few properties, excrete a large concentration of pollutants into roots, translocate pollutants into surface biomass, and produce a significant quantity of plant biomass. Thus, plants with these properties give promising results in ecofriendly clean-up strategies. Field crops are economically grown plants and include food crops (e.g., rice, wheat, common bean, maize), oil crops (e.g., sunflower, mustard, rapeseed, groundnut), and bioenergy and fodder crops. Field crops in this context are very valuable as they have a short life cycle and produce a large amount of biomass, thus, compensating for their low uptake with these properties. Therefore, present-day research focuses on identifying plant species with higher potential for phytoremediation as well as developing new methods of phytoremediation.

19.2 Contaminants in soil, water, and plants Heavy metals and metalloids are the major contaminants that accumulate in soil through emissions from industrial areas, disposal of metal wastes, mine tailings, animal manures, pesticides, sewage sludge, coal combustion residues, atmospheric deposition, wastewater irrigation, and spillage of petrochemicals (Khan et al., 2008; Zhang et al., 2010). The heavy metals found mostly at contaminated sites include Zn, Cu, Cr, Pb, As, Cd, Ni, and Hg. Metals unlike organic contaminants do not undergo degradation by microbes and chemicals (Kirpichtchikova et al., 2006). After introduction into soil, their total concentration persists for a long time (Adriano, 2003). Contamination of soil by heavy metals poses a threat to the ecosystem and humans through the food chain, ingestion, or contact with soil, drinking of groundwater, land tenure problems, and food insecurity due to reduction in usable land for agricultural production (McLaughlin et al., 2000a,b; Ling et al., 2007). A variety of approaches can be used for the remediation of contaminated soil. The technologies have been broadly classified by the US Environmental Protection Agency (EPA) into two categories: (1) containment remedies and (2) source control (Maslin and Maier, 2000; McLaughlin et al., 2000a,b). Containment remedies involve the construction of caps, liners, and vertically engineered barriers (VEB) for the prevention of contaminant migration. Source control includes ex situ and in situ treatment technologies. Ex situ treatment technologies involve the removal or excavation of contaminated soil from the site, whereas in in situ treatment technologies there is no need to excavate contaminated soil; it is treated at its original site. The selection of any remediation technology depends on a number of factors, according to Wuana and Okieimen (2011), including: (1) long-term effectiveness, (2) cost, (3) general acceptance, (4) commercial availability, (5) applicability to mixed wastes/organics and heavy metals, (6) applicability to high metal concentrations, (7) volume reduction, (8) toxicity reduction, and (9) mobility reduction. Reliable methods to detect environmental pollutants, their dynamics and fate, are required to evaluate their impact on soil quality and living organisms. Techniques used to monitor volatile and semivolatile pollutants in soil include physicochemical techniques such as solid phase micro-extraction (SPME), followed by analysis by GC-MS, use of bioindicators, and use of sensing technology (e.g., electronic nose) (Cesare and Macagnano, 2013).

19.2 Contaminants in soil, water, and plants

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The increase in human population has raised the quantity of waste and introduced many different types of pollutants into water bodies; these were not considered pollutants earlier but are now seen as harmful to the environment and public health. The pollutants include pharmaceuticals, toxins, hormones, viruses, and endocrine-disrupting chemicals (Xagoraraki and Kuo, 2008). Heavy metals (e.g., Cd, Pb, Mn, Fe, Zn, Cu) are also major contaminants of water (Opaluwa et al., 2012). Human activity is the major source of most of the water pollutants, whereas some amount of them are added by natural activities such as volcanic eruptions. The main anthropogenic activities that cause water pollution include agricultural waste, livestock waste, industrial chemical waste, pesticides, fertilizers, mine drainage, untreated municipal sewage, spillage of petroleum products, spent solvents, and so forth. Once pollutants are discharged into any of the surface water bodies or the groundwater, they enter the water cycle. Pollutants may also undergo physical, biological, and chemical transformations (Xagoraraki and Kuo, 2008). The contaminants in water bodies, such as heavy metals, are also bioaccumulated in the flora and fauna of that region and so enter into the food chain. The contaminated water, whether used for drinking, irrigation, or other purposes, may lead to many health issues. For example, chemical pollutants can damage functional systems (e.g., immune system and nervous system) and major organs (e.g., kidney and liver), and pathogenic microorganisms in the water lead to gastrointestinal problems. Increased cancer risk is also a major threat posed by enhanced concentrations of pollutants in drinking water (Xagoraraki and Kuo, 2008). An atomic absorption spectrophotometer (AAS) is used to assess the presence and amount of heavy metals in polluted water (Opaluwa et al., 2012). Adsorbents, such as activated carbon, can be used to remove heavy metals from contaminated water; however, it is an expensive material. So, instead of using commercial activated carbon, researchers used materials (e.g., sawdust, chitosan, mango leaves, coconut shell) that were inexpensive, had a high-adsorption capacity, and were locally available (Renge et al., 2012). Contaminants enter plants when they are grown in soil that has various types of them, such as heavy metals, or when irrigated with polluted water containing contaminants. The plants show growth reduction, altered metabolism, metal accumulation, and lower biomass production (Nagajyoti et al., 2010). Some metals (e.g., Mn, Cu, Zn, Co, and Cr) are important for plant metabolism in trace amounts. When these metals are present in bioavailable forms and in excess, they become toxic to plants. Few heavy metals are very toxic to metal-sensitive plants, so result in growth inhibition and may also cause death of the organisms. The uptake of heavy metals does not show a linear increase with an increasing metal concentration. A number of factors affect the uptake of heavy metals by plants, which includes the growing environment. Some examples are soil aeration, soil moisture, soil pH, temperature, competition between plant species, type and size of plants, plant root systems, type of leaves, the elements available in the soil, and plant energy supply to roots and leaves (Yamamato and Kozlowski, 1987). Metal contamination affects various biochemical and physiological processes in plants such as carbon dioxide fixation, gaseous exchange, respiration, and nutrient absorption. The toxic effects of six heavy metals—Mn, Cd, Cr, Hg, Co, and Pb—were studied on Zea mays by Ghani (2010). Cd was found to be the most toxic and Cr to be the least toxic metal. The phytotoxicity of the six heavy metals was found in this order: Cd . Co . Hg . Mn . Pb . Cr. Heavy metals in plants lead to production of reactive oxygen species (ROS) such as hydrogen peroxide, superoxide radicals, and hydroxyl radicals. The ROS can oxidize biological molecules, lead to major cellular damages, and ultimately cell death. Hydroxyl radicals produced in the DNA proximity can remove or add hydrogen

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atoms to the DNA backbone or bases, respectively (Pryor, 1988). This resulted in 104105 DNA base modifications in a cell in one day (Ames et al., 1991). Fe21 ions, free in solution or coordinated with ring nitrogens or complexed to a phosphate residue, were involved in these DNA alterations mediated by the hydroxyl radical (Luo et al., 1994). Metal ions also lead to oxidative modification of proteins and free amino acids (Stadtman, 1993). The oxidation in proteins most commonly occurs at arginine, histidine, methionine, proline, cysteine, and lysine residues. Transition metals (e.g., iron) and oxygen lead to lipid peroxidation and damage to biological membranes. Plants cope in a number of ways with metal toxicity. The ROS generated in leaf cells are removed by enzymes of the antioxidant system of plants such as ascorbate peroxidase (APX), superoxide dismutase (SOD), glutathione reductase (GR), and catalase (CAT). Proline is reported to detoxify active oxygen in Cajanus cajan and Brassica juncea under heavy metal stress (Alia et al., 1995).

19.3 Phytoremediation: a green technology A staggering number of anthropogenic activities that involve industrial discharges from electroplating, tanneries, municipalities, smelting, refining, and so on pose a significant threat to the quality of the ever-fragile ecosystem (Gisbert et al., 2003; Liu et al., 2005). These controlled and uncontrolled actions have resulted in the addition of toxic xenobiotic compounds, both organic and inorganic in nature, inclusive of many heavy metals and other toxic elements that have intruded into food chains via soil; they cause innumerable allergies and life-threatening diseases in humans and animals (Zornoza et al., 2002; Liu et al., 2005). Their highly toxic concentration has destroyed soil properties and rendered large tracts of agricultural land unfit for cultivation. There are a number of ex situ soil cleanup techniques based on the physicochemical theory (e.g., volatilization, vitrification, excavation, soil washing, soil incineration, chemical extraction, solidification, and landfills) for contaminant removal; however, these are very costly, inconvenient, and sometimes further damage soil properties (Meagher, 2000; Liu et al., 2013). To address this major quandary, an in situ and novel approach to reach a solution that is natural and safe is phytoremediation, often referred as Green/Clean Technology. In other words, this approach is the use of special plants, known as hyperaccumulators, for the extraction of contaminants from the environment or for lowering their toxicity. These plants possess extraordinary abilities for degradation and removal of many obstinate xenobiotics (both organic and inorganic) and act as a sink for their accumulation, thus are referred to as “green livers” (Ismail, 2013). Subsequently, using it has instigated hope for many environmental enthusiasts and multinational coporations, thus making phytoremediation a very popular field (Salt et al., 1998). For each one of the processes, there are two possible strategies for exercising this green cleanup technique. The first involves decontamination using hyperaccumulator plants that are capable of accumulating 50 to 100 times more contaminants as compared to normal plants via roots (Pulford and Watson, 2003). The second alternative is to use normal plants as pollutant scavengers coupled with changes in soil environment, either by increasing bioavailability and stabilization of contaminants or by using biotechnological approaches. Compared to the methods used earlier, phytoremediation turned out to be inexpensive, environmentally safe, aesthetically pleasing, and apt for decontaminating large tracts of otherwise unusable agricultural soils.

19.4 Field crops as hyperaccumulators and their potential for phytoremediation

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For the preceding reasons, phytoremediation should be viewed as a long-term remediation solution because many cropping cycles may be needed, spanning several months to years, to determine the contaminants. Thus, remediation using plants can be seen as a competitive and far superior approach to existing conventional technologies for decontaminating “spiked” sites. Still, there are several factors that influence the use of phytoremediation as a green technology such as plants’ biomass accumulation, responsiveness of the plants to agricultural practices (e.g., harvesting and cropping), availability of the metal, and so on (Paz-Alberto and Sigua, 2013). Therefore, there is a need to establish effective monitoring and evaluation methods for in situ field remediation (Gerhardt et al., 2009). In addition, it is important to understand the long-term implications of green plant technology in sequestering environmental pollutants. There are many types of phytoremedial processes, among them: (1) rhizofiltration, adsorption and precipitation of contaminants present near the plant root zone; (2) phytoextraction, also known as phytoaccumulation in which the contaminant is translocated by plant roots to aboveground parts; (3) phytostabilization i.e., by using plants, contaminants are transformed into an immobilized form; (4) phytodegradation, also known as phytotransformation, where contaminants are broken down into less toxic forms inside the plants or in the rhizosphere; and (5) phytovolatalization, the uptake of a contaminant and transpiration of it into the atmosphere. Table 19.1 shows the detailed mode of action of these phytoremedial processes and various examples of plants on which studies have been done.

19.4 Field crops as hyperaccumulators and their potential for phytoremediation Field crops are grown on a large scale for consumption purposes. They are usually annual with a life cycle of 3 to 5 months. Crop plants can be used for phytoremediation because they have high biomass production and can easily adapt to the changing environment (Keller et al., 2003; Meers et al., 2005; Ciura et al., 2005). To be regarded as successful, phytoremediative agents of crop plants must be able to tolerate, as well as accumulate, significant amounts of pollutants (Angelova et al., 2011). Such crops can also have a commercial use as fodder if pollutant accumulation does not exceed critical levels for livestock (Murillo et al., 1999). However, certain crops have the capability to accumulate high concentrations of heavy metals thereby making them unfit for consumption. Further, this wasteful biomass can be used for reextracting the accumulated metals by a process called phytomining. Other than food crops, bioenergy crops have a great potential for phytoremediation because they can be used for both energy production and environmental cleanup. To successfully carry out phytoremediation with field crops, it is necessary for the plants to be able to accumulate significant levels of pollutants. Thus, hyperaccumulator field crops can be considered as the most favorable contenders for phytoremediation. Hyperaccumulators have the unique ability to actively take up large amounts of pollutants especially metals, 100-fold higher than nonaccumulator plant species (Yang et al., 2005). All hyperaccumulators are tolerant to toxic substances; however, they are very different from the category of tolerant plants that can exclude pollutants from entering plant systems. Therefore, tolerant species may also include nonaccumulators. Concentration of a pollutant that is taken up by the crop plant system varies according to different species. Hyperaccumulator plants possess a greater potential to absorb pollutants from the soil, faster

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Table 19.1 Key Phytoremediation Processes in Different Plant Species Phytoremediation Mechanism Rhizofiltration

Phytoextraction

Phytostabilization

Phytodegradation

Phytovolatilization

Mode of Action

Plant Species and Interaction

Absorption, precipitation, and concentration of heavy metal ions into the roots from the polluted effluents Metal uptake from soil/water, translocation via xylem, and sequestration in aerial plant parts Absorption, precipitation, complex formation, and metal valence reduction for fixing the metal, stabilizing the soil and preventing toxic leachate formation in a short span of time (immobilization of metal to a less toxic form) Optimum use of metabolic capabilities of plants and rhizoshphere microbes to break down soil contaminants mostly organic in nature via different enzymes (e.g., dehalogenases, oxygenases, and reductases) Uptake and transpiration of contaminants into the atmosphere (evaporates or vaporizes).

Aquatic macrophytes known for metal filtration (Eichhornia crassipes a, Hydrocotyle umbellate b, Lemna minor, c etc.) A total of 400 hyperaccumulator species, 90 belonging to Brassicaceae itself d,e Mercury stabilization to least toxic forms in Brassica juncea L. f

Trinitrotoluene (TNT) breakdown via Nicotiana tabaccum g

Selenium/mercury vaporization via Brassica juncea L. h

a

Kay et al., 1984. Dierberg et al., 1987. c Mo et al., 1989. d Ghosh and Singh, 2005. e Baker and Brooks, 1989. f Shiyab et al., 2009. g Hannink et al., 2007. h US EPA, 2000. b

translocation from roots to shoots, and better mechanisms of sequestration of contaminants as compared to nonaccumulators (Rascio and Navari-Izzo, 2011). Among various types of pollutants, heavy metal pollution has been studied widely, and hyperaccumulation mechanisms in plants have also been established in detail. To absorb metals from the soil, the crop plants either release ligands to bind metals or acidify the rhizosphere with the help of plasma membrane proton pumps (Peer et al., 2006). The soluble metals enter the root system by symplast or apoplast. Further, to enter the vascular system of the plant, metals use pumps and channels of essential elements. The metals via xylem sap are translocated and deposited in the leaves of the plant. After deposition in the leaves, the metals are detoxified by forming complexes to chelates present in the cellular system. Finally, the chelated metal in the cell is sequestered to an organelle where it is unable to interfere with normal cellular mechanisms; usually, they are sequestered in the vacuole. However, these chelated metal complexes can also remain bound to the cell wall or in some cases are volatilized (Peer et al., 2006).

19.5 Facilitated phytoextraction in crops

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More than 500 species of plants belonging to families, such as Brassicaceae, Asteraceae, Fabaceceae, Caryophyllaceae, Poaceae, Euphorbiaceae, and others, have been reported to accumulate metals in large quantities; those that perform maximum hyperaccumulators belong to Brassicaceae and Asteraceae (Ebbs et al., 1997; Sarma, 2011). Table 19.2 contains a list of food crops that have potential for phytoremediation.

19.5 Facilitated phytoextraction in crops Phytoextraction is the uptake of contaminants from the environment into plants and then storage of them in harvestable plant parts. Using various chelating/reducing agents—microbial secretions and soil exudations and increasing contaminant bioavailability, mobility, and uptake into the hyperaccumulator system—has been well documented in the literature for three decades. The soil amendments increase metal diffusion in the soil solution, keeping them in bioavailable form and stabilizing the metal ions. Chelating agents occur naturally in hyperaccumulators in the form of “Natural Chelating Agents,” such as low-molecular-weight organic acids (LMWOAs), amino acids, ferretins, nicotianamine, and so on, released by crop roots into the rhizosphere or secreted and accumulated in cell cytoplasm, which makes the ions of both nutrients and contaminants more mobile and compliable. Sequestration is followed by dissociation of the metalchelator bond because plants take up the metal and release the chelator back into the soil (see Figure 19.1). Hyperaccumulator crop plants have built-in chelator molecules, such as phytochelatins (PC), metallothioneins (MT), root exudations, and others, rich in amino acids, organic acids, ferritins, and phytins that remediate metal in the plant’s proximity. Alternatively, soil amendments, both biodegradable and nonbiodegradable, can be added to the growth medium to facilitate metal and/or contaminant removal, particularly in commercialized phytoremediation practices (Bucheli-Witschel and Egli, 2001; Jiang et al., 2004). Either way, facilitating the contaminant removal process by employing chelatemetal kinetics is one of the most popular phytoremedial practices in use at present.

19.5.1 Chelating agents Chelating agents can be naturally tapped or used as soil modifications to enhance the availability of heavy metals to the field crops. “Chelate” usually refers to a complex between metal and a chelating agent, not the agent itself (Nowack and Van Briesen, 2005). Several examples have been reported across field crops (e.g., Pisum sativum, Brassica juncea, and Zea mays) for metal remediation via chelants/chelators (Bucheli-Witschel and Egli, 2001). Natural chelators are mostly proteins or nonproteins by chemical nature. A number of synthetic chelating agents—for example, aminopolycarboxylic acids, ethylenediamine tetraacetic acid (EDTA), ethelynediaminedisuccinic acid (EDDS), nitriloacetic acid (NTA), ethylene glycol bis (2-aminoethyl ether) tetraacetic acid (GEDTA), and diethylenetriamine pentaacetic acid (DTPA)—have been used frequently to increase the mobility and transport of heavy metals from contaminated soil via field crops. However, these persist in the soil and may also cause toxicity, and so are not reliable. A more environmentally friendly approach is the use of biodegradable amino acids/LMWOA(s) as chelators; this is a promising approach in phytoextraction research.

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Table 19.2 Food Crops with Probable Role in Phytoextraction of Heavy Metals Plant Species

Common Name

Brassica carinata Brassica juncea

Ethiopian mustard Indian mustard

Brassicaceae

Brassica napus Festuca spp. Glycine max

Rapeseed

Brassicaceae

Soybean

Poaceae Fabaceae

Helianthus annus

Sunflower

Asteraceae

Hordeum vulgare Lolium perenne Medicago sativa Oryza sativa Phaseolus vulgaris Pistia stratiotes Pisum sativum Raphanus sativus Sorghum bicolor Triticum secalotriticum Vicia faba

Barley

Poaceae

Perrenial ryegrass Alfalfa

Poaceae

Zea mays

Family

Brassicaceae

Fabaceae

Rice Common bean Water lettuce Sweet pea

Poaceae Fabaceae

Fabaceae

Radish

Brassicaceae

Sorghum

Poaceae

Poaceae

Horse bean Maize

Fabaceae

Araceae

Poaceae

Source: Modified from Vamerali et al. (2010).

Metal Affinity Cd, Cr, Cu, Ni, Pb, Zn Ag, Cr, Cd, Cu, Ni, Pb, Zn, Mn, Se Cr, Hg, Pb, Se, Zn, Cu Cu, Zn As, Cd, Cu, Pb, Zn Cr, Cu, Zn, As, Cd, Co, Pb Al, As, Cu, Zn, Pb Cu, Pb, Zn

Reference(s) Marchiol et al. (2004) McCutcheon and Schnoor (2003); Bennett et al. (2003); Marchiol et al. (2004); Clemente et al. (2005); Haverkamp et al. (2007) McCutcheon and Schnoor (2003); Marchiol et al. (2004) Alvarez et al. (2003) Fellet et al. (2007) McCutcheon and Schnoor (2003); Fellet et al. (2007); Marchiol et al. (2007) McCutcheon and Schnoor (2003); Soriano and Fereres (2003) Alvarenga et al. (2009)

Cr, Pb, Cu, Cd, As Cu, Pb, Zn As, Cu, Pb, Zn Cr, Cd, Hg, Cu Pb

McCutcheon and Schnoor (2003); Pajuelo et al. (2007) Murakami and Ae (2009) Luo et al. (2005, 2008)

Cd, Cr, Cu, Ni, Pb, Zn As, Cd, Co, Cu, Pb, Zn As, Cd, Cu, Pb, Zn Al

Marchiol et al. (2004)

As, Cd, Cu, Pb, Zn

Luo et al. (2005); Fellet et al. (2007)

Sen et al. (1987); McCutcheon and Schnoor (2003) Chen et al. (2004)

Fellet et al. (2007); Marchiol et al. (2007) Soriano and Fereres (2003) McCutcheon and Schnoor (2003)


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Cell wall

Heat shock proteins(HSP)

Cytoplasm

Metellothloneins(MT)

Sequestration and compartmentalization

Vacuole

Glutathione(GSH)

Organic acids

Phytochelatins(PC) Phytins

Amino acids

Stabilization and compartmentalization

Accumulation/ chelation/ contaminant fixation

Nicotinamine

Contaminant-chelator complex Translocation via xylem

Plant uptake

Microbial degradation

Chelation bond dissociation

Rhizosphere interactions LMWOAs/ amino acids/other chelators

Root exudates

Contaminants

FIGURE 19.1 An outline of chelate-assisted contaminant uptake by plants. The process continues with the subsequent intra- and intercellular activation of natural chelating responses and sequestration in cell cytoplasm, followed by chelator replenishment to the rhizosphere. Source: Modified from Bhardwaj et al. (2013).

19.5.1.1 Amino acids Chelation is also mediated by metal-binding peptides or amino acids (Salt et al., 1998). Amino acids (e.g., cysteine, glycine, histidine, proline) are nitrogen-donating ligands that have a high affinity for metal ions (Rauser, 1999). Generally, amino acids are used to enhance nutrient availability to garden crops; therefore this concept was thought to be applicable to metals as well. Due to its ability to act as a trident ligand via carboxylato, amine, and imadazole groups, histidine is considered a versatile ligand and one of the most important free amino acids. Callahan et al. (2006) observed how free histidine increases Ni tolerance and capacity to translocate it to the shoot region by chelation. Kra¨mer et al. (1996) reported that Ni exposure to Alyssum lesbiacum increased total amino acid content; in particular, free histidine content showed an increase of up to 36 times. Extended X-ray absorption fine structure analysis revealed histidinenickel (His-Ni) complexes in vivo. Further, exogenous application of free histidine increased Ni tolerance and translocation from root to shoot in a nonhyperaccumulator (Alyssum montanum). Overexpression of A. lesbiacum ATP-PRT cDNA

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increased the free histidine pool 15-fold in the shoot tissues in transgenic Arabidopsis (Kerkeb and Kramer, 2003). Research evidence also is needed to verify the role of other amino acids (e.g., L-glycine) as metal chelators.

19.5.1.2 Phytins Many ligands are produced by crop plants for binding heavy metal ions such as Cd, Cu, Ni, and Zn. One of them is a phosphorus-rich complex called Zn-phytates. Phytin or phytate is a mixed salt of myoinositol hexaphosphoric acid or phytic acid. It is variably distributed throughout the protein matrix, or confined in condensed masses called globoids. In vitro studies indicated that those phytic acids possess iron-chelating properties (Minihane and Rimbach, 2002). Van Steveninck et al. (1994) conducted electron probe microanalysis of fractured, quenchfrozen root specimens of common crop species. They found that a substantial amount of Zn can be bound as Zn phytate (myo-inositol kis-hexaphosphate) within small vacuoles of cells in the root elongation zone of lucerne, soybean, lupins, tomato, rapeseed, cabbage, radish, maize, and wheat when exposed to high levels of Zn (80300 μM). Lou et al. (2007) conducted greenhouse experiments to study the effects of chelating agents on the growth and metal accumulation of Pteris vittata L., Vetiveria zizanioides L., and Sesbania rostrata L. in soil polluted with As, Cu, Pb, and Zn using five chelating agents—EDTA, HEDTA, NTA, OA, and phytic acid (PA). The results with PAinduced uptake were substantially significant.

19.5.1.3 Organic acids Organic acids are low-molecular-weight (2CHO) containing compounds, which are widely distributed among all organisms. They carry a negative charge, according to the dissociation properties and presence of a number of carboxylic acids, which allows the displacement of anions from the soil matrix and the complexation of metal cations in solution. These are involved in various soil processes such as detoxification of metals by plants, microbial proliferation in the rhizosphere, dissolution of soil minerals, and mobilization and nutrient uptake by microorganisms and plants (Marschner, 1995). Citric, ferulic, fumaric, lactic, malic, oxalic, propionic, succinic, sinapic, and tartaric acids are the most common low-molecular-weight organic acids (LMWOAs) found in the soil (Raskin et al., 1997; Dakora and Phillips, 2002). Under favorable environmental conditions, the concentration of LMWOAs is low in the soil. Primarily, organic acid formation occurs in the soil through metabolism by microbes, degradation of canopy detritus, and so on (Oburger et al., 2009). These are known to be key players of abiotic stress tolerance, nutrient deficiencies, and interaction between plant and microbes that operate at the rootsoil interface. Many recent reports indicate that under environmental stress, the biosynthesis, accumulation, transport, and exudation by roots of plant/ microbial interactions with organic acids is greatly increased (Fernández et al., 2012; Tan et al., 2013). With respect to heavy metal/metalloid/radionuclide uptake via organic acids, some important reports are discussed next. Huang et al. (1998) found organic acid increased uranium extraction in Indian mustard and Chinese cabbage. Similarly, increased chromium accumulation in tomato by organic acids was observed. The authors found that Brassica juncea may accumulate uranium (Ur) in its shoots mediated by citric acid application up to a level of 5000 mg/kg. When considering their application as a soil amendment for phytoextraction purposes, LMWOA(s) have a potential advantage over substances, such as EDTA and DTPA, in that they are more readily degraded in the soil and their


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persistence in soil is pretty short-lived. These function as natural chelating agents and are very efficient in the solubilization of mineral soil components such as heavy metals (Wasay et al., 1998; Hens and Hocking, 2002). Spartina maritima was evaluated for phytoextraction potential for several heavy metals in salt marshes via three different LMWOAs (i.e., citric, malic, and acetic acid). Acetic acid turned out to be the most effective metal-extracting organic acid with many metals (Duarte et al., 2011). The role of LMWOAs (citric acid and succinic acid) from root exudations in the rhizosphere sediments of three mangrove plant species showed that the concentration of them was altered with the varying levels of PAH contamination. Among the mangrove species, Bruguiera gymnorrhiza attained the highest root biomass and concentration of LMWOAs and also was the most efficient in removing PAHs (Wang et al., 2013). Citric, fumaric, malic, and α-cetoglutaric acids were studied for accumulation in Sesuvium portulacastrum and Brassica juncea determined by the HPLC technique in shoots, roots, and xylem saps for exposure to lead. For both species, a positive correlation was observed between lead and citrate concentrations in xylem sap. Accumulation of citric acid in xylem and shoots of S. portulacastrum indicated its high potential to translocate and accumulate this metal in shoots, suggesting their possible use to remediate Pb-polluted soils (Ghanaya et al., 2013). Thus, after taking an overview of low-molecular-weight organic acids, it has been observed that these are feasible chelators in the context to soil remediation through plants (Agnello et al., 2013).

19.5.2 Growth-promoting bacteria and mycorrhizae Plant growth-promoting rhizobacteria and mycorrhizal associations contribute positively in ameliorating the phytoremediation efficiency of contaminated soils. These soil microbes play a pivotal role at the plantrhizosphere interface. Rhizospheric soil microbes enhance the effectiveness of the phytoremedial process in two ways: (1) directly facilitating phytoextraction by enhancing root-toshoot metal translocation or facilitating phytostabilization of the contaminant by lowering its mobility or availability in rhizosphere; and (2) indirectly facilitating phytoremediation by enhancing plant growth and biomass, increasing the survival of plants in the contaminated environment, improving acquisition and recycling of nutrients, and controlling plant pathogens (Rajkumar et al., 2012).

19.5.2.1 Mycorrhizae Mycorrhizae are the mutualistic association between fungi and roots of plants. Almost 80% of terrestrial plants have symbiotic associations with mycorrhizae fungi (Sylvia, 2005). There are many types of mycorrhizal associations: arbuscular mycorrhizas, ectomycorrhizas, orchid mycorrhizas, and ericaceous mycorrhizas. Of these the most widespread is the association between roots of terrestrial plants and arbuscular mycorrhizal fungi (AMF) (Marques et al., 2009). AMF assist phytoremedial efficiency in numerous ways—for example, by improving plant root and shoot growth and biomass, up-regulating nutrient and water uptake by plants, and increasing plant survival under environmental stress (Smith and Read, 2008; Denton, 2007). AMF associations also enhance phytoextraction of metals by increasing root-to-shoot metal translocation. Bhaduri and Fulekar (2012) reported AMF inoculation increased the phytoremediation potential of Ipomoea aquatic by increasing Cd accumulation in plant tissues. AMF protect plants from damage caused by organic pollutants by regulating translocation and distribution in rhizodermis then in

460


shoots (Fester, 2013). Arbuscular mycorrhizal fungi also have a stimulatory effect on organic contaminants, degrading bacteria living in rhizosphere (Alarcon et al., 2008). Yu et al. (2011) and Zhou et al. (2009) found that AMF associations have increased the biodegradation of PAHs by Lolium multiflorum and Medicago sativa plants. Malachowska-Jutsz and Kalka (2010) reported that AMF associations helped in the phytoremediation of petroleum contaminants by Triticum aestivum.

19.5.2.2 Plant growth-promoting rhizobacteria Plant growth-promoting rhizobacteria (PGPRs) are the beneficial rhizosphere inhabiting soil bacteria (Kloepper and Schroth, 1978). Depending on their association with the host plant, there are two categories of PGPRs: intracellular and extracellular. Intracellular PGPRs are like nodule-forming bacteria that inhabit the inside of plant cells. Extracellular PGPRs (e.g., Burkholderia, Pseudomonas, and Bacillus) are free-living bacteria that live outside plant cells (Tak et al., 2013). They are present in bulk in the rhizosphere of hyperaccumulator plants inhabiting metalcontaminated soils (Naees et al., 2011). Inoculation of PGPRs in contaminated sites has been reported to enhance the total phytoremedial efficiency of field crops. Inoculation of Pseudomonas fluorescence improved plant growth and cadmium extraction in inoculated plants in comparison to noninoculated plants (Heshmatpure and Rad, 2012). PGPRs also have been isolated from organic pollutant contaminated soils and found to have rhizodegradation potential. Pseudomonas is one of the prominent groups of rhizobacteria involved in organic contaminant degradation (Glick, 2010). Symbiotic association between Rhizobium and alfalfa is reported to have a stimulatory effect on other soil microflora and polyaromatic hydrocarbon degradation (Teng et al., 2011). PGPRs enhance plant growth and phytoremediation efficiency as follows: 1. by secreting plant growth-promoting substances such as indole-3-acetic acid (IAA), cytokinin, and gibberellins (Glick, 2012); 2. by excreting stress-alleviating metabolites such as 1-aminocyclopropane-1-carboxylic acid deaminase (ACC deaminase) (Glick, 1995; Rajkumar et al., 2006); 3. by altering metal bioavailability by secreting chelators such as siderophores and organic acids, altering soil pH, and through oxidation/reduction reactions to enhance their accumulation (Ma et al., 2011; Rajkumar et al., 2012); and 4. by solubilizing nutrients such as phosphorus and nitrogen fixation (Glick, 2012). Various studies have demonstrated the beneficial interaction of PGPRs and field crops. Sheng and Xia (2006) found that inoculation of cadmium-resistant, rhizosphere-competent bacterial strains in Brassica napus increased root and shoot biomass. Similarly, inoculation of PGPRs in Brassica juncea enhanced the growth and biomass production when grown in Pb-Zn mine tailings and Ni polluted soil (Wu et al., 2006, Zaidi et al., 2006). Ding (2012) found that the interaction of Medicago osativa and soil microbes degraded benzo[a]pyrene in soil and decreased the accumulation of pollutant inside plant tissues.

19.5.3 Plant growth regulatory substances Plant growth regulatory substances (PGRs) are the phytohormones (i.e., auxins, cytokinins, gibberellins, ethylene, and abscisic acid). The new class of phytohormones includes brassinosteroids,


461

salicylic acid, jasmonic acid, and stringolactones. These are essential for normal growth, development, and reproduction of plants. PGRs-mediated phytoremediation is known as phytohormoneassisted phytoremediation (Barbafieri and Tassi, 2011). Phytohormones stimulate plant growth by regulating various intercellular processes (Hadi et al., 2010). Phytohormones serve as one of the effective strategies for improving phytoremediation by boosting plant biomass and root and shoot growth, increasing plant tolerance toward contaminants, and enhancing metal acquisition and accumulation (Ouzounidou and Ilias, 2005; Tassi et al., 2008). Application of both crude and commercially available plant growth regulators increased metal uptake stress tolerance in pearl millet (Firdaus-e-Bareen et al., 2012).

19.5.3.1 Auxins The auxin group is one of the master phytohormones that regulate plant cell division, organ differentiation, growth, and maturation (Trewavas, 2000). Auxins regulate cation uptake and cation fluxes (Vamerali et al., 2011). IAA is the most commonly occurring natural auxin, while other auxins, such as indole-3-butyric acid (IBA), 4-chloro-IAA, and phenylacetic acid, also occur (Machackova et al., 2008). Very few studies have been conducted to check the potential of phytohormones for phytoremediation. IAA treatment increased lead accumulation in Medicago sativa roots (Lo´pez et al., 2005). When administered to Sedum alferdii hyperaccumulating and nonhyperaccumulating ecotypes, IAA treatment increased lead accumulation 2.7-fold more in hyperaccumulating ecotype than in nonhyperaccumulating ecotype (Liu et al., 2007). Du et al. (2011) observed that IAA treatment increased phytoextraction potential of lead by zinc/cadmium hyperaccumulator Picris divaricata. Thus, auxin treatment can be used for the phytoremediation of polymetallic-contaminated sites. Chouychai (2012) found IBA treatment alleviated lindane and alpha endosulfan toxicity in Brassica chinenses by increasing its root and shoot fresh weights. Thus, auxin treatment may alleviate organochlorine phytotoxicity.

19.5.3.2 Cytokinins Cytokinins (Ck) regulate plant growth and development by playing a critical role in cell division and differentiation, shoot initiation, leaf expansion, delay of senescence, bud formation, growth of lateral buds, chlorophyll synthesis, control of shootroot balance, and transduction of nutritional signals. Cks can also stimulate crop productivity and plant resistance to various environmental stresses (Sakakibara, 2006; Tassi et al., 2008). Transpiration rate is one of the key processes regulating the success of phytoremediation efficiency (Rock, 2003). Cytokinin treatment can increase the acquisition of metal by accelerating the transpiration rate (Tassi et al., 2008). Appliction of Cks has been found to increase stomatal aperture in leaves of Tradescantia and Paphiopedilum tonsum (Irving et al., 1992) and the transpirational rate in leaves of Helianthus, Hordeum, Brassica, Triticum, Avena, and Vigna (Pharmavati et al., 1998; Pospı´sˇilová et al., 2000). Tassi et al. (2008) found that Ck treatment can effectively improve phytoextraction of heavy metals by up-regulating metal uptake, increasing biomass production, and improving the plant transpiration rate. Simultaneous application of Ck and ammonium thiosulfate enhances mercury uptake and translocation in Brassica juncea and Helianthus annuus up to 248% and 232% by increasing plant biomass and the evapotranspiration rate (Cassina et al., 2012).

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19.5.3.3 Brassinosteroids Brassinosteroids (BRs) are polyhydroxysteroids that regulate various physiological responses in plants, including germination, seedling photomorphogenesis, root and stem elongation, leaf bending and epinasty, vascular differentiation, male fertility, induction of ethylene biosynthesis, timing of senescense and flowering, activation of photosynthesis, and resistance to biotic and abiotic stresses (Clouse and Sasse, 1998; Krishna, 2003; Bajguz and Hayat, 2009). Brassinosteroids alleviate heavy metal stress in plants (Bajguz, 2011). BR-assisted phytoremediation can improve the phytoremediation potential of inorganics by increasing germination, improving crop yield, increasing stress tolerance, facilitating phytostabilization and phytoextraction, and increasing root apparatus. BRs can assist phytoremediation of organics by increasing their degradation, growth, and biomass under contaminant stress (Barbafieri and Tassi, 2011).

19.5.4 Molecular techniques The molecular techniques applied to plants mainly include genetic engineering to enhance tolerance, accumulation, and metabolism of pollutants. Many genes have been identified from various organisms, especially bacteria and yeasts, that are involved in the acquisition, allocation, and detoxification of pollutants (Ehrlich, 1997). Thus, genetic engineering of plants may help improve the phytoremediation efficiency of plants. A full-length OsCs1 gene encoding for citrate synthase has been isolated; it is induced under Al toxicity in Oryza sativa. Transgenic tobacco lines containing OsCS1 genes showed increased citrate reflux and enhanced aluminum tolerance (Han et al., 2009). Up-regulated expression of γ-glutamylcysteine synthetase or glutathione synthetase in transgenic Brassica juncea resulted in the higher accumulation of and tolerance to some metals (e.g., Cd, Cr, and As) (Reisinger et al., 2008). Chen et al. (2013) used a one gene transgenic approach to enhance arsenic tolerance and accumulation in Arabidopsis thaliana. A key arsenite, As(III), antiporter PvACR3 present in As hyperaccumulator fern, Pteris vittata, was expressed in Arabidopsis thaliana derived by promoter CaMV 35S. Transgenic plants have shown a many-fold increase in As tolerance. Arsenic methylation and volatilization have been induced due to expression of bacterial arsenite S-adenosylmethyltransferase in transgenic plants (Xiang-Yan et al., 2011). Matsui et al. (2013) isolated a transcription factor, AtPHR1, regulator of inorganic phosphate starvation response in Arabidopsis thaliana. This factor was made to overexpress in garden plants (i.e., Torenia, Petunia, and Verbena) and these transgenic plants resulted in the hyperaccumulation of inorganic phosphate in leaves and accelerated phosphate absorption rates from hydropnic solutions. Transgenic plants with the bacterial genes used in polychlorinated biphenyl (PCB) degradation showed effective removal of PCBs from contaminated sites (Novakova et al., 2009). Bacterial mercuric ion reductase (mer A) and organomercurial lyase (mer B) genes are used in genetically engineered plants for the phytoremediation of mercury. Various plant species, such as poplar, rice, tobacco, peanut, Arabidopsis, and Chlorella, have been modified with these genes. These genetically modified plants grow well in organic and inorganic mercury-contaminated soils and accumulate Hg in roots (Ruiz and Daniell, 2009). Transgenic plants that overexpress the bacterial mercury reductase have exhibited a high tolerance to organic mercury (Bizilly et al., 2003) and effectively enhanced the volatilization of ionic mercury (Haque et al., 2010).

References

463

19.6 Conclusion and future prospects The presence of several contaminants limits the use of polluted sites; such contaminants include various organic and inorganic compounds. The remediation of these sites can be achieved through a newly developed, low-cost green technology known as phytoremediation in which plants are used to clean the contaminants. A few plant species with a higher tolerance for contaminants have been identified. The hyperaccumulator species have some limitations such as poor growth rate and difficulty in practical applications. Thus, field crops are seen as a reliable alternative to hyperaccumulators. To elucidate the limitations of field crops for phytoremediation, such as low uptake and translocation of target pollutants and for activation of unavailable pollutants in soil, various improvement methods should be employed. To achieve this, chelators can be used to enhance the bioavailability of pollutants and phytohormones can be applied to increase the growth rate. Use of molecular and biotechnological approaches and advanced agricultural practices may be helpful to the advancement of phytoremediation procedures.

References Adriano, D.C., 2003. Trace Elements in Terrestrial Environments: Biogeochemistry, Bioavailability and Risks of Metals. second ed. Springer, New York. Agnello, A.C., Huguenot, D., van Hullebusch, E.D., Esposito, G., 2013. Enhanced phytoremediation: a review of low molecular weight organic acids and surfactants used as amendments. Crit. Rev. Env. Sci. Available from: http://dx.doi.org/10.1080/10643389.2013.829764. Alarcon, A., Fred, T., Davies Jr., Autenrieth, R.L., Zuberer, D.A., 2008. Arbuscular mycorrhiza and petroleum-degrading microorganisms enhance phytoremediation of petroleum-contaminated soil. Int. J. Phytoremediation 10, 251263. Alia, K.V., Prasad, S.K., Pardha Saradhi, P., 1995. Effect of zinc on free radical and proline in Brasica juncea and Cajanus cajan. Phytochemistry 39, 4547. Allen, E.B., 1988. The Reconstruction of Disturbed Arid Lands: An Ecological Approach. Westview Press, Boulder, Colorado. Alvarenga, P., Goncalves, A.P., Fernandes, R.M., de Varennes, A., Vallini, G., Duarte, E., et al., 2009. Organic residues as immobilizing agents in aided phytostabilization: (I) effects on soil chemical characteristics. Chemosphere 74, 12921300. Alvarez, E., Fernandez Marcos, M.L., Vaamonde, C., Fernandez-Sanjurjo, M.J., 2003. Heavy metals in the dump of an abandoned mine in Galicia (NW Spain) and in the spontaneously occurring vegetation. Sci. Total Environ. 313, 185197. Ames, B.A., Shingenaga, M.K., Park, E.M., 1991. Oxidative damage of macromolecules. In: Davis, K. (Ed.), Oxidation Damage and Repair: Chemical, Biological and Medical Aspects. Pergamon Press, Elmsford, NY, pp. 181187. Angelova, V.R., Ivanova, R.V., Delibaltova, V.A., Ivanov, K.I., 2011. Use of sorghum crops for in situ phytoremediation of polluted soils. J. Agricul. Sci. Technol. A1, 693702. Bajguz, A., 2011. Suppression of Chlorella vulgaris growth by cadmium, lead, and copper stress and its restoration by endogenous brassinolide. Arch. Environ. Contam. Toxicol. 60, 406416. Bajguz, A., Hayat, S., 2009. Effects of brassinosteroids on the plant responses to environmental stresses. Plant Physiol. Biochem. 47, 18.

464


Baker, A.J.M., Brooks, R.R., 1989. Terrestrial higher plants which hyperaccumulate metal elements: a review of their distribution, ecology, and phytochemistry. Biorecovery 1, 81126. Barbafieri, M., Tassi, E., 2011. Brassinosteroids for phytoremediation application. In: Hayat, S., Ahmad, A. (Eds.), Brassinosteroids: A Class of Plant Hormone. Springer, Amsterdam, pp. 403437. Bennett, L.E., Burkhead, J.L., Hale, K.L., Terry, N., Pilon, M., Pilon-Smits, E.A.H., 2003. Analysis of transgenic Indian mustard plants for phytoremediation of metals-contaminated mine tailings. J. Environ. Qual. 32, 432440. Bhaduri, A.M., Fulekar, M.H., 2012. Assessment of arbuscular mycorrhizal fungi on the phytoremediation potential of Ipomoea aquatica on cadmium uptake. Biotechnology 2 (3), 193198. Bhardwaj, R., Sharma, R., Gautam, V., Bali, S., Kaur, R., Thukral, A.K., 2013. Metal uptake and sequestration dynamics in chelate mediated phytoremediation. In: Nehra, S. (Ed.), Festschrift Volume on Prof. P.C. Trivedi. Pointer Publishers, Jaipur, pp. 216231. Bizilly, S.P., Kim, T., Kandasamy, M.K., Meagher, R.B., 2003. Subcellular targeting of methylmercury lyase enhances its specific activity for organic mercury detoxification in plants. Plant Physiol. 131, 463471. Bucheli-Witschel, M., Egli, T., 2001. Environmental fate and microbial degradation of aminopolycarboxylic acids. FEMS Microbiol. Rev. 25, 69106. Callahan, D.L., Baker, A.J.M., Kolev, S.D., Wedd, A.G., 2006. Metal ion ligands in hyperaccumulating plants. J. Biol. Inorg. Chem. 11, 212. Cassina, L., Tassi, E., Pedron, F., Petruzzelli, G., Ambrosini, P., Barbafieri, M., 2012. Using a plant hormone and a thioligand to improve phytoremediation of Hg-contaminated soil from a petrochemical plant. J. Hazard Mater. 231232, 3642. Cesare, F.D., Macagnano, A., 2013. Detection and monitoring of volatile and semivolatile pollutants in soil through different sensing strategies. EGU2013-2074-1, EGU General Assembly. Chen, H.M., Zeng, C.R., Tu, C., Shen, Z.G., 2000. Chemical methods and phytoremediation of soil contaminated with heavy metals. Chemosphere 41, 229234. Chen, Y., Xu, W., Shen, H., Yan, H., Xu, W., He, Z., et al., 2013. Engineering arsenic tolerance and hyperaccumulation in plants for phytoremediation by a PvACR3 transgenic approach. Environ. Sci. Technol. 47, 93559362. Chen, Y.H., Li, X.D., Shen, Z.G., 2004. Leaching and uptake of heavy metals by ten different species of plants during an EDTA assisted phytoextraction process. Chemosphere 57, 187196. Chouychai, W., 2012. Effect of some plant growth regulators on lindane and alpha-endosulfan toxicity to Brassica chinensis. J. Environ. Biol. 33, 811816. Ciura, J., Poniedzialek, M., Sekara, A., Jedrsczyk, A., 2005. The possibility of using crops as metal phytoremediation. Pol. J. Environ. Stud. 14, 1722. Clemente, R., Walker, D.J., Berna, M.P., 2005. Uptake of heavy metals and as by Brassica juncea grown in a contaminated soil in Aznalcollar (Spain): the effect of soil amendments. Environ. Pollut. 138, 4658. Clouse, S.D., Sasse, J.M., 1998. Brassinosteroids: essential regulators of plant growth and development. Annu. Rev. Plant Physiol. Plant Mol. Biol. 49, 427451. Cunningham, S.D., Ow, D.W., 1996. Promises and prospects of root zone of crops. Phytoremediation. Plant Physiol. 110, 715719. Dakora, F.D., Phillips, D.A., 2002. Root exudates as mediators of mineral acquisition in low-nutrient environments. Plant Soil 245, 3547. Denton, B., 2007. Advances in phytoremediation of heavy metals using plant growth promoting bacteria and fungi. MMG 445. Basic Biotechnol. 3, 15. Dierberg, F.E., Debusk, T.A., Goulet, J.R., 1987. Removal of copper and lead using a thin-film technique. In: Reddy, K.R., Smith, W.H. (Eds.), Aquatic Plants for Water Treatment and Resource Recovery. Magnolia Publishing, Orlando, Florida, pp. 497504. Ding, K.Q., 2012. Phytoremediation of benzo[a]pyrene-contaminated soil by alfalfa (Medicago sativa L.). Adv. Mat. Res. 518523, 55595564.

References

465

Du, R.-J., He, E.-K., Tang, Y.-T., Hu, P.-J., Ying, R.-R., Morel, J.-L., et al., 2011. How phytohormone IAA and Chelator EDTA affect lead uptake by ZN/CD hyperaccumulator Picris Divaricata. Int. J. Phytoremediation 13, 10241036. Duarte, B., Freitas, J., Caçador, I., 2011. The role of organic acids in assisted phytoremediation processes of salt marsh sediments. Hydrobiologia 674, 169177. Ebbs, S.D., Lasat, M.M., Brady, D.J., Cornish, J., Gordon, R., Kochian, L.V., 1997. Heavy metals in the environment: phytoextraction of cadmium and zinc from a contaminated soil. J. Environ. Qual. 26, 14241430. Ebbs, S.D., Brady, D.J., Kochian, L.V., 1998. Role of uranium speciation in the uptake and translocation by plants. J. Exp. Bot. 49, 11831190. EEA, 2003. Soil degradation. In: Europe’s Environment: The Third Assessment. Environmental Assessment Report No. 10. EEA, Copenhagen, pp. 198212. Ehrlich, H.L., 1997. Microbes and metals. Appl. Microbiol. Biotechnol. 48, 687692. Fellet, G., Marchiol, L., Perosa, D., Zerbi, G., 2007. The application of phytoremediation technology in a soil contaminated by pyrite cinders. Ecol. Eng. 31, 207214. Fernández, D.A., Roldán, A., Azcoń, R., Caravaca, F., Ba˚a˚th, E., 2012. Effects of water stress, organic amendment and mycorrhizal inoculation on soil microbial community structure and activity during the establishment of two heavy metal-tolerant native plant species. Microb. Ecol. 63, 794803. Fester, T., 2013. Arbuscular mycorrhizal fungi in a wetland constructed for benzene-, methyl tert-butyl etherand ammonia-contaminated groundwater bioremediation. Microb. Biotechnol. 6, 8084. Firdaus-e-Bareen, Shafiq, M., Jamil, S., 2012. Role of plant growth regulators and a saprobic fungus in enhancement of metal phytoextraction potential and stress alleviation in pearl millet. J. Hazard. Mater. 237238, 186193. French, C.J., Dickinson, N.M., Putwain, P.D., 2006. Woody biomass phytoremediation of contaminated brownfield land. Environ. Pollut. 141, 387395. Gerhardt, K.E., Huang, X.D., Glick, B.R., Greenberg, B.M., 2009. Phytoremediation and rhizoremediation of organic soil contaminants: potential and challenges. Plant Sci. 176, 2030. Ghanaya, T., Hanen, Z., Raoudha, B., Souhir, S., Giorgio, L., Gian, A.S., et al., 2013. Implication of organic acids in the long-distance transport and the accumulation of lead in Sesuvium portulacastrum and Brassica juncea. Chemosphere 90, 14491454. Ghani, A., 2010. Toxic effects of heavy metals on plant growth and metal accumulation in maize (Zea mays L.). Iran. J. Toxicol. 3, 325334. Ghosh, M., Singh, S.P., 2005. A review on phytoremediation of heavy metals and utilization of its byproducts. Appl. Ecol. Environ. Res. 3, 118. Gisbert, C., Ros, R., Haro, A.D., Walker, D.J., Bernal, M.P., Serrano, R., et al., 2003. A plant genetically modified that accumulates Pb is especially promising for phytoremediation. Biochem. Biophys. Res. Commun. 303, 440445. Glick, B.R., 1995. The enhancement of plant growth by free-living bacteria. Can. J. Biochem. 41, 109117. Glick, B.R., 2010. Using soil bacteria to facilitate phytoremediation. Biotechnol. Adv. 28, 367374. Glick, B.R., 2012. Plant growth-promoting bacteria: mechanisms and applications. Scientifica 2012, 115. Hadi, F., Bano, A., Fuller, M.P., 2010. The improved phytoextraction of lead (Pb) and the growth of maize (Zea mays L.): the role of plant growth regulators (GA3 and IAA) and EDTA alone and in combinations. Chemosphere 80, 457462. Han, Y.Y., Zhang, W.Z., Zhang, B.L., Zhang, S.S., Wang, W., Ming, F., 2009. One novel mitochondrial citrate synthase from Oryza sativa L. can enhance aluminum tolerance in transgenic tobacco. Mol. Biotechnol. 42, 299305.

466


Hannink, N.K., Subramanian, M., Rosser, S.J., Basran, A., Murray, J.A., Shanks, J.V., et al., 2007. Enhanced transformation of tnt by tobacco plants expressing a bacterial nitroreductase. Int. J. Phytoremediation 9, 385401. Haque, S., Zeyaullh, M., Nabi, G., Srivastava, P.S., Ali, A., 2010. Transgenic tobacco plant expressing environmental E. coli merA gene for enhanced volatilization of ionic mercury. J. Microbiol. Biotechnol. 20, 917924. Haverkamp, R.G., Marshall, A.T., van Agterveld, D., 2007. Pick your carats: nanoparticles of gold-silvercopper alloy produced in vivo. J. Nanopart. Res. 9, 697700. Hens, M., Hocking, P., 2002. Phosphorus mobilization by organic-acid exudation: processes governing benefits in rotational cropping. In: Proceedings of the Seventeenth WCSS World Congress of Soil Science. Bangkok, Thailand, Symposium 6 Paper no. 1092. Heshmatpure, N., Rad, M.Y., 2012. The effect of PGPR (Plant-Growth-Promoting Rhizobacteria) on phytoremediation of cadmiums by canola (Brassica napus L.) cultivars of Hyola 401. Ann. Biol. Res. 3, 56245630. Huang, J.W., Blaylock, M.J., Kapulnik, Y., Ensley, B.D., 1998. Phytoremediation of uranium-contaminated soils: role of organic acids in triggering uranium hyperaccumulation in plants. Env. Sci. Tech. 32, 20042008. Irving, H.R., Gehring, C.A., Parish, R.W., 1992. Changes in cytosolic pH and calcium of guard cells precede stomatal movements. Proc. Natl. Acad. Sci. USA 89, 17901794. Ismail, S., 2013. Phytoremediation: a green technology. Iran. J. Plant Physiol. 3, 567568. Jiang, X.J., Luo, Y.M., Liu, Q., Liu, S.L., Zhao, Q.G., 2004. Effects of cadmium on nutrient uptake and translocation by Indian mustard. Environ. Geochem. Health 26, 319324. Kay, S.H., Haller, W.T., Garrard, L.A., 1984. Effect of heavy metals on water hyacinths [Eichhornia crassipes (Mart.) Solms]. Aquat. Toxicol. 5, 117128. Keller, C., Hammer, D., Kayser, A., Richner, W., Brodbeck, M., Sennhauser, M., 2003. Root development and heavy metal phytoextraction efficiency: comparison of different plant species in the field. Plant Soil 249, 6781. Kerkeb, L., Kramer, U., 2003. The role of free histidine in xylem loading of nickel in Alyssum lesbiacum and Brassica juncea. Plant Physiol. 131, 716724. Khan, F.I., Hussain, T., Hejazi, R., 2004. An overview and analysis of site remediation technologies. J. Environ. Manage. 71, 95122. Khan, S., Cao, Q., Zheng, Y.M., Huang, Y.Z., Zhu, Y.G., 2008. Health risks of heavy metals in contaminated soils and food crops irrigated with wastewater in Beijing, China. Environ. Pollut. 152, 686692. Kirpichtchikova, T.A., Manceau, A., Spadini, L., Panfili, F., Marcus, M.A., Jacquet, T., 2006. Speciation and solubility of heavy metals in contaminated soil using X-ray microfluorescence, EXAFS spectroscopy, chemical extraction, and thermodynamic modelling. Geochim. Cosmochim. Acta 70, 21632190. Klassen, S.P., McLean, J.E., Grossel, P.R., Sims, R.C., 2000. Fate and behavior of lead in soils planted with metal-resistant species (River birch and smallwing sedge). J. Environ. Qual. 29, 18261834. Kloepper, J.W., Schroth, M.N., 1978. Plant growth promoting rhizobacteria on radishes. Fourth International Conference on Plant Pathogen Bacteria, vol. 2. Angers, France, pp. 879882. Kra¨mer, U., Cotter-Howells, J.D., Charnock, J.M., Baker, A.J.M., Smith, J.A.C., 1996. Free histidine as a metal chelator in plants that accumulate nickel. Nature 379, 635638. Krebs, R., Gupta, S.K., Furrer, G., Schulin, R., 1999. Gravel sludge as an immobilizing agent in soils contaminated by heavy metals—a field study. Water Air Soil Pollut. 115, 465479. Krishna, P., 2003. Brassinosteroid-mediated stress responses. J. Plant Growth Regul. 22, 289297. Ling, W., Shen, Q., Gao, Y., Gu, X., Yang, Z., 2007. Use of bentonite to control the release of copper from contaminated soils. Aust. J. Soil Res. 45, 618623.

References

467

Liu, D., Li, T., Yang, X., Islam, E., Jin, X., Mahmood, Q., 2007. Enhancement of lead uptake by hyperaccumulator plant species Sedum alfredii using EDTA and IAA. Bull. Environ. Contam. Toxicol. 78, 280283. Liu, W.H., Zhao, J.Z., Ouyang, Z.Y., Soderlund, L., Liu, G.H., 2005. Impacts of sewage irrigation on heavy metals distribution and contamination. Environ. Int. 31, 805812. Liu, X., Li, X., Chermaine Ong, S.M., Chu, Z., 2013. Progress of phytoremediation: focus on new plant and molecular mechanism. J. Plant Biol. Soil Health 1, 15. Lo´pez, M.L., Peralta-Videa, J.R., Benitez, T., Gardea-Torresdey, J.L., 2005. Enhancement of lead uptake by alfalfa (Medicago sativa) using EDTA and a plant growth promoter. Chemosphere 61, 595598. Lou, L.Q., Ye, Z.H., Wong, M.H., 2007. Solubility and accumulation of metals in Chinese brake fern, vetiver and rostrate sesbania using chelating agents. Int. J. Phytoremediation 9, 325343. Luo, C.L., Shen, Z.G., Li, X.D., 2005. Enhanced phytoextraction of Cu, Pb, Zn and Cd with EDTA and EDDS. Chemosphere 59, 111. Luo, C.L., Shen, Z.G., Li, X.D., 2008. Hot NTA application enhanced metal phytoextraction from contaminated soil. Water Air Soil Pollut. 188, 127137. Luo, Y., Han, Z., Chin, S.M., Linn, S., 1994. Three chemically distinct types of oxidants formed by iron mediated Fenton reactions in the presence of DNA. Proc. Natl. Acad. Sci. USA 91, 1243812442. Ma, Y., Prasad, M.N., Rajkumar, M., Freitas, H., 2011. Plant growth promoting rhizobacteria and endophytes accelerate phytoremediation of metalliferous soils. Biotechnol. Adv. 29, 248258. Machakova, I., Zazimalova, E., George, E.F., 2008. Plant growth regulators I: introduction; auxins, their analogues and inhibitors. In: George, E.F., Hall, M.A., De Klerk, G.-J. (Eds.), Plant Propagation by Tissue Culture, third ed. The Background, Springer, Dordrecht, The Netherlands, pp. 175204. Malachowska-Jutsz, A., Kalka, J., 2010. Influence of mycorrhizal fungi on remediation of soil contaminated by petroleum hydrocarbons. Environ. Bull. 19, 32173223. Marchiol, L., Sacco, P., Assolari, S., Zerbi, G., 2004. Reclamation of polluted soil: phytoremediation potential of crop-related Brassica species. Water Air Soil Pollut. 158, 345356. Marchiol, L., Fellet, G., Perosa, D., Zerbi, G., 2007. Removal of trace metals by Sorghum bicolor and Helianthus annuus in a site polluted by industrial wastes: a field experience. Plant Physiol. Biochem. 45, 379387. Marques, A.P.G.C., Rangel, A.O.S.S., Castro, P.M.L., 2009. Remediation of heavy metal contaminated soils: phytoremediation as a potentially promising clean-up technology. Crit. Rev. Env. Sci. Technol. 39, 622654. Marschner, H., 1995. Mineral Nutrition of Higher Plants. second ed. Academic Press, London. Maslin, P., Maier, R.M., 2000. Rhamnolipid-enhanced mineralization of phenanthrene in organic-metal co-contaminated soil. Bioremediat. J. 4, 295308. Maurice, C., Lagerkvist, A., 2000. Using Betula pendula and Telephora caryophyllea for soil pollution assessment. J. Soil Contam. 9, 3150. Matsui, K., Togami, J., Mason, J.G., Chandler, S.F., Tanaka, Y., 2013. Enhancement of phosphate absorption by garden plants by genetic engineering: a new tool for phytoremediation. BioMed. Res. Int. Available from: http://dx.doi.org/10.1155/2013/182032. McCutcheon, S.C., Schnoor, J.L., 2003. Phytoremediation: Transformation and Control of Contaminants. John Wiley & Sons, New York. McLaughlin, M.J., Zarcinas, B.A., Stevens, D.P., Cook, N., 2000a. Soil testing for heavy metals. Commun. Soil Sci. Plant Anal. 31, 16611700. McLaughlin, M.J., Hamon, R.E., McLaren, R.G., Speir, T.W., Rogers, S.L., 2000b. Review: a bioavailabilitybased rationale for controlling metal and metalloid contamination of agricultural land in Australia and New Zealand. Aust. J. Soil Res. 38, 10371086. Meagher, R.B., 2000. Phytoremediation of toxic elemental and organic pollutants. Curr. Opin. Plant Biol. 3, 153162.

468


Meers, E., Ruttens, A., Hopgood, M., Lesage, E., Tack, F.M.G., 2005. Potential of Brassica rapa, Canabis sativa, Helianthus annus and Zea mays for phytoextraction of heavy metals from calcareous dredged sediments derived soils. Chemosphere 61, 561572. Minihane, A.M., Rimbach, G., 2002. Iron absorption and the iron binding and anti-oxidant properties of phytic acid. Int. J. Food Sci. Tech. 37, 741748. Mo, S.C., Choi, D.S., Robinson, J.W., 1989. Uptake of mercury from aqueous solution by duckweed: the effect of pH, copper, and humic acid. J. Environ. Health 24, 135146. Murakami, M., Ae, N., 2009. Potential for phytoextraction of copper, lead, and zinc by rice (Oryza sativa L.), soybean (Glycine max [L.] Merr.), and maize (Zea mays L.). J. Hazard. Mater. 162, 11851192. Murillo, J.M., Maranon, T., Cabrera, F., Lo´pez, R., 1999. Accumulation of heavy metals in sunflower and sorghum plants affected by the Guadiamar spill. Sci. Total Environ. 242, 281292. Naees, M., Ali, Q., Shahbaz, M., Ali, F., 2011. Role of rhizobacteria in phytoremediation of heavy metals: an overview. Int. J. Plant Sci. 2, 220232. Nagajyoti, P.C., Lee, K.D., Sreekanth, T.V.M., 2010. Heavy metals, occurrence and toxicity for plants: a review. Environ. Chem. Lett. 8, 199216. Novakova, M., Mackova, M., Chrastilova, Z., Viktorova, J., Szekeres, M., Demnerova, K., et al., 2009. Cloning the bacterial bphC gene into Nicotiana tabacum to improve the efficiency of PCB phytoremediation. Biotechnol. Bioeng. 102, 2937. Nowack, B., VanBriesen, J.M., 2005. Chelating agents in the environment. In: Nowack, B., VanBriesen, J.M. (Eds.), Biogeochemistry of Chelating Agents; ACS Symposium Series. American Chemical Society, Washington DC, pp. 118. Oburger, E., Kirk, G.D.J., Wenzel, W.W., Puschenreiter, M., Jones, D.L., 2009. Interactive effects of organic acids in the rhizosphere. Soil Biol. Biochem. 41, 449457. Opaluwa, O.D., Aremu, M.O., Ogbo, L.O., Magaji, J.I., Odiba, I.E., Ekpo, E.R., 2012. Assessment of heavy metals in water, fish and sediments. Curr. World Environ. 7, 213220. Ouzounidou, G., Ilias, I., 2005. Hormone-induced protection of sunflower photosynthetic apparatus against Cu toxicity. Biol. Plant 49, 223228. Pajuelo, E., Carrasco, J.A., Romero, L.C., Chamber, M.A., Gotor, C., 2007. Evaluation of the metal phytoextraction potential of crop legumes. Regulation of the expression of O-acetylserine (thiol) lyase under metal stress. Plant Biol. 9, 672681. Passariello, B., Giuliano, V., Quaresima, S., Barbaro, M., Caroli, S., Forte, G., et al., 2002. Evaluation of the environmental contamination at an abandoned mining site. Microchem. J. 73, 245250. Paz-Alberto, A.M., Sigua, G.C., 2013. Phytoremediation: a green technology to remove environmental pollutants. Am. J. Clim. Change 2, 7186. Peer, W.A., Baxter, I.R., Richards, E.L., Freeman, J.L., Murphy, A.S., 2006. Phytoremediation and hyperaccumulator plants. In: Tamas, M.J., Martinoia, E. (Eds.), Molecular Biology of Metal Homeostasis and Detoxification. Topics in Current Genetics. Springer-Verlag, Berlin/Heidelberg, pp. 299340. Pharmawati, M., Billington, T., Gehring, C.A., 1998. Stomatal guard cell responses to kinetin and natriuretic peptides are cGMP-dependent. Cell Mol. Life Sci. 54, 272276. Pospı´sˇilová, J., Synková, H., Rulcová, J., 2000. Cytokinins and water stress. Biol. Plant 43, 321328. Pryor, W.A., 1988. Why is the hydroxyl radical the only radical that commonly adds to DNA? Hypothesis: it is a rare combination of high electrophilicity, high thermo chemical reactivity, and a mode of production that occurs near DNA. Free Radic. Biol. Med. 4, 219223. Pulford, I.D., Waston, C., 2003. Phytoremediation of heavy metal—contaminated land by tree a review. Environ. Int. 29, 592540. Rajkumar, M., Nagendran, R., Lee, K.J., Lee, W.H., Kim, S.Z., 2006. Influence of plant growth promoting bacteria and Cr61 on the growth of Indian mustard. Chemosphere 62, 741748.

References

469

Rajkumar, M., Sandhya, S., Prasad, M.N., Freitas, H., 2012. Perspectives of plant-associated microbes in heavy metal phytoremediation. Biotechnol. Adv. 30, 15621574. Rascio, N., Navari-Izzo, F., 2011. Heavy metal hyperaccumulating plants: how and why do they do it? And what makes them so interesting? Plant Sci. 180, 169181. Raskin, I., Smith, R.D., Salt, D.E., 1997. Phytoremediation of metals: using plants to remove pollutants from the environment. Curr. Opin. Biotechnol. 8, 221226. Rauser, W.E., 1999. Structure and function of metal chelators produced by plants: the case for organic acids, amino acids, phytin and metallothioneins. Cell Biochem. Biophys. 31, 1948. Reisinger, S., Schiavon, M., Terry, N., Pilon-Smits, E.A.H., 2008. Heavy metal tolerance and accumulation in Indian mustard (Brassica juncea L.) expressing bacterial gamma glutamylcysteine synthetase or glutathione synthetase. Int. J. Phytoremediation 10, 440454. Renge, V.C., Khedkar, S.V., Pande, S.V., 2012. Removal of heavy metals from wastewater using low cost adsorbents: a review. Sci. Revs. Chem. Commun. 2, 580584. Rock, S.A., 2003. Vegetative covers for waste containment. In: Tsao, D.T. (Ed.), Advances in Biochemical Engineering/Biotechnology. Springer, Berlin/Heidelberg, pp. 157170. Ruiz, O.N., Daniell, H., 2009. Genetic engineering to enhance mercury phytoremediation. Curr. Opin. Biotechnol. 20, 213219. Sakakibara, H., 2006. Cytokinins: activity, biosynthesis, and translocation. Annu. Rev. Plant Biol. 57, 431449. Salt, D.E., Smith, R.D., Raskin, I., 1998. Phytoremediation. Annu. Rev. Plant Physiol. Plant Mol. Biol. 49, 643668. Sarma, H., 2011. Metal hyperaccumulation in plants: a review focusing on phytoremediation technology. J. Environ. Sci. Technol. 4, 118138. Schwartz, C., Gerard, E., Perronnet, K., Morel, J.L., 2001. Measurement of in situ phytoextraction of zinc by spontaneous metallophytes growing on a former smelter site. Sci. Total Environ. 279, 215221. Sen, A.K., Mondal, N.G., Mandal, S., 1987. Studies of uptake and toxic effects of Cr (VI) on Pistia stratiotes. Water Sci. Technol. 19, 119127. Sheng, X.-F., Xia, J.-J., 2006. Improvement of rape (Brassica napus) plant growth and cadmium uptake by cadmium resistant bacteria. Chemosphere 64, 10361042. Shiyab, S.M., Han, F., Yi, S., 2009. Phytotoxicity of mercury in Indian mustard (Brassica Juncea L.). Ecotoxicol. Environ. Saf. 72, 619625. Smith, S.E., Read, D.J., 2008. Mycorrhizal Symbiosis. third ed. Academic Press, San Diego. Soriano, A.M., Fereres, E., 2003. Use of crops for in situ phytoremediation of polluted soils following a toxic flood from a mine spill. Plant Soil 256, 253264. Stadtman, E.R., 1993. Oxidation of free amino acids and amino acid residues in proteins by radiolysis and by metal-catalysed reactions. Annu. Rev. Biochem. 62, 797821. Sylvia, D.M., 2005. Mycorrhizal symbiosis. In: Sylvia, D.M., Fuhrmann, J.J., Hartel, P.G., Zuberer, D.A. (Eds.), Principles and Applications of Soil Microbiology. Pearson/Prentice Hall, Upper Saddle River, NJ, pp. 263282. Tak, H.I., Ahmad, F., Babalola, O.O., 2013. Advances in the application of plant growth-promoting rhizobacteria in phytoremediation of heavy metals. Rev. Environ. Contam. Toxicol. 223, 3352. Tan, S., Yang, C., Mei, X., Shen, S., Raza, W., Shen, Q., et al., 2013. The effect of organic acids from tomato root exudates on rhizosphere colonization of Bacillus amyloliquefaciens T-5. Appl. Soil Ecol. 64, 1522. Tassi, E., Pouget, J., Petruzzelli, G., Barbafieri, M., 2008. The effects of exogenous plant growth regulators in the phytoextraction of heavy metals. Chemosphere 71, 6673. Teng, Y., Shen, Y., Luo, Y., Sun, X., Sun, M., Fu, D., et al., 2011. Influence of Rhizobium meliloti on phytoremediation of polycyclic aromatic hydrocarbons by alfalfa in an aged contaminated soil. J. Hazard. Mater. 186, 12711276.

470


Trewavas, A., 2000. Signal perception and transduction In: Buchanan, B., Gruissem, W., Jones, R., (Eds.), Biochemistry and Molecular Biology of Plants. American Society of Plant Physiologists, pp. 930988. U.S. Environmental Protection Agency (EPA), 2000. Introduction to phytoremediation, EPA 600-R-99-107. February, Washington, DC. Vamerali, T., Bandiera, M., Mosca, G., 2010. Field crops for phytoremediation of metal-contaminated land. A review. Environ. Chem. Lett. 8, 117. Vamerali, T., Bandiera, M., Hartley, W., Carletti, P., Mosca, G., 2011. Assisted phytoremediation of mixed metal(loid)-polluted pyrite waste: effects of foliar and substrate IBA application on fodder radish. Chemosphere 84, 213219. Van Steveninck, R.F.M., Babare, A., Fernando, D.R., Van Steveninck, M.E., 1994. The binding of zinc, but not cadmium, by phytic acid in roots of crop plants. Plant Soil 167, 157164. Wang, Y., Fang, Y., Lin, L., Luan, T., Tam, N.F.Y., 2013. Effects of low molecular-weight organic acids and dehydrogenase activity in rhizosphere sediments of mangrove plants on phytoremediation of polycyclic aromatic hydrocarbons. Chemosphere doi: 10.1016/j. Wasay, S.A., Barrington, S.F., Tokunaga, S., 1998. Remediation of soils polluted by heavy metal using salts of organic acid sand chelating agents. Environ. Technol. 19, 369380. Wu, S.C., Cheung, K.C., Luo, Y.M., Wong, M.H., 2006. Effects of inoculation of plant growth-promoting rhizobacteria on metal uptake by Brassica juncea. Environ. Pollut. 140, 124135. Wuana, R.A., Okieimen, F.E., 2011. Heavy metals in contaminated soils: a review of sources, chemistry, risks and best available strategies for remediation. ISRN Ecol. 2011, Article ID 402647. Xagoraraki, I., Kuo, D., 2008. Water pollution: emerging contaminants associated with drinking water. In: Heggenhougen, K., Quah, S. (Eds.), International Encyclopedia of Public Health. Academic Press, San Diego, pp. 539550. Xiang-Yan, M., Jie, Q., Li-Hong, W., Gui-Lan, D., Guo-Xin, S., Hui-Lan, W., et al., 2011. Arsenic biotransformation and volatilization in transgenic rice. New Phytol. 191, 4956. Yamamoto, F., Kozlowski, T.T., 1987. Effect of flooding, tilting of stem, and ethrel application on growth, stem anatomy, and ethylene production of Acer platanoides seedlings. Scand J. For. Res. 2, 141156. Yang, X., Feng, Y., He, Z., Stoffella, P.J., 2005. Molecular mechanisms of heavy metal hyperaccumulation and phytoremediation. J. Trace Elem. Med. Biol. 18, 339353. Yu, X.Z., Wu, S.C., Wu, F.Y., Wong, M.H., 2011. Enhanced dissipation of PAHs from soil using mycorrhizal ryegrass and PAH-degrading bacteria. J. Hazard Mater. 186, 12061217. Zaidi, S., Usmani, S., Singh, B.R., Musarrat, J., 2006. Significance of Bacillus subtilis strain SJ-101 as a bioinoculant for concurrent plant growth promotion and nickel accumulation in Brassica juncea. Chemosphere 64, 991997. Zhang, M.K., Liu, Z.Y., Wang, H., 2010. Use of single extraction methods to predict bioavailability of heavy metals in polluted soils to rice. Commun. Soil Sci. Plant Anal. 41, 820831. Zhou, X.B., Cébron, A., Béguiristain, T., Leyval, C., 2009. Water and phosphorus content affect PAH dissipation in spiked soil planted with mycorrhizal alfalfa and tall fescue. Chemosphere 77, 709713. Zornoza, P., Vázquez, S., Esteban, E., Fernández-Pascual, M., Carpena, R., 2002. Cadmium-stress in nodulated white lupin: strategies to avoid toxicity. Plant Physiol. Biochem. 40, 10031009.

CHAPTER

Sustainable Soil Management in Olive Orchards: Effects on Telluric Microorganisms

20

Adriano Sofo, Assunta Maria Palese, Teresa Casacchia and Cristos Xiloyannis

20.1 Introduction Obtaining top yields of high quality and preservation of environmental sustainability is possible by maintaining microbiological soil fertility using innovative, sustainable agricultural techniques (Kushwaha et al., 2000; Ding et al., 2013). In particular, the first layers of the pedosphere are the habitat for a high number of bacterial and fungal communities that play a key role in the pedogenetic processes and in soil fertility improvement (Brady and Weil, 2008; Jagadamma et al., 2008). On this basis, changes in the structure and dynamics of soil bacterial and fungal communities, as a response to different soil management in agricultural systems, represent an interesting assessment index of soil status with respect to its quality and complexity (Visser and Parkinson, 1992; Anderson, 2003). The use of microbiological techniques has allowed the isolation of important physiological groups of bacteria related to soil fertility, such as the microorganisms involved in important steps of the carbon cycle (e.g., actinomycetes, Pseudomonas spp., and Bacillus spp.), the major decomposers of complex polymers (e.g., lignocelluloses and chitin), and the nitrogen cycle (i.e., nitrogen fixer, proteolytic, ammonifying, nitrifying, and denitrifying bacteria) (Zaitlin et al., 2004; Ding et al., 2013). Nitrogen-fixer microorganisms are able to reduce NRN to NH3 for the biosynthesis of organic nitrogen compounds (Brady and Weil, 2008). Proteolytic bacteria are responsible for soil protein degradation in peptons, peptic acids, and in aminoacids, whereas ammonifying bacteria release ammonium ions (NH41) from nitrogen-containing organic compounds (Brady and Weil, 2008; Ding et al., 2013). Moreover, fungi and actinomycetes are able to colonize rhizosphere and use root exudates as a carbon source, supply roots with easily assimilable nitrates, and play a key role in the biological control of root pathogens and in the maintenance of soil health (Govaerts et al., 2008). The olive is the emblematic tree of the Mediterranean Basin where it is an integral and significant part of the landscape and culture (Loumou and Giourga, 2003; Castillo-Llanque and Rapoport, 2011; Ehrenberger et al., 2012; Go´mez-del-Campo and Garcıá, 2012; Rodrigues et al., 2012; Sanzani et al., 2012; Cuevas et al., 2013); however, its ecological importance has only recently been acknowledged. Olive oil was and is the major source of nutritional fats for the residents of the Mediterranean area and the most valuable export product from this region. Olive trees have been cultivated for centuries mainly in the hilly and marginal parts of the Basin, becoming one of the P. Ahmad (Ed): Emerging Technologies and Management of Crop Stress Tolerance, Volume 2. DOI: http://dx.doi.org/10.1016/B978-0-12-800875-1.00020-X © 2014 Elsevier Inc. All rights reserved.

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most representative and stable fruit crops in the world occupying around 9.5 Mha in 2010 (Barlett et al., 2012; FAOSTAT, 2012). In such areas soil degradation processes (e.g., erosion, soil organic impoverishment, groundwater contamination, soil salinization, biodiversity losses) are very intense because of a lack of conservative soil management practices (tillage, no organic matter input) and the abandonment of nonproductive olive groves and/or their overgrazing (Ben-Gal, 2011; Hammami et al., 2011; Perez-Martin et al., 2011; Fernández-Escobar et al., 2012; Carr, 2013; Caruso et al., 2013; Go´mez-del-Campo, 2013; Morales-Sillero et al., 2013; Palese et al., 2013). Therefore, in the semiarid Mediterranean olive orchards, the loss of soil fertility needs to be avoided by using innovative and optimized agricultural techniques with low environmental impact (Dag et al., 2011; Rewald et al., 2011a,b; Diaz-Espejo et al., 2012; Gracia et al., 2012; Gucci et al., 2012a,b). On this basis, the chapter’s aim is to present some results about the effects of sustainable management systems on soil microbial, genetic, functional, and metabolic diversity in Mediterranean olive orchards. We place particular attention on the most important groups of microorganisms. Among the agronomic sustainable practices, the input of soil organic matter as compost is an important factor that affects soil fertility. For this reason, the system of in situ compost production in olive groves is thoroughly discussed.

20.2 Sustainable management systems Suitable management practices for fruit growing—that is, conservation tillage, cover crops, compost amendments, incorporation of cover crops (green manure), pruning residues into the soil, and adequate irrigation and fertilization—are recommended to save conventional water, restore soil organic matter, and reduce environmental pollution (Lal, 2004; Fernández et al., 2011a,b; Gomiero et al., 2011; Rapoport et al., 2012; Rodriguez-Dominguez et al., 2012; Sánchez-Alcalá et al., 2012; Fernández et al., 2013). As a matter of fact, sustainable soil management can determine optimal plant nutrition equilibrium, avoid nutrient accumulation in soils and leaching risks, improve irrigation efficiency, and prevent soil erosion and root asphyxia. Further, these sustainable practices can have positive effects on the activities and complexity of soil microbial communities (Govaerts et al., 2008; Gomiero et al., 2011). The optimization and innovative use of agricultural techniques with a low negative environmental impact have positive effects on both soil, yield, and quality because they increase microbial biomass activity and complexity (Gruhn et al., 2000; Kushwaha et al., 2000; Widmer et al., 2006). In the semiarid Mediterranean agricultural lands, a new approach in fruit orchard management has been imposed by environmental emergencies such as soil degradation and water shortage (Lal, 2004; Hochstrat et al., 2006; Graniti et al., 2011; Larbi et al., 2011; Rosati et al., 2011; Searles et al., 2011; Moriana et al., 2012; Prieto et al., 2012; Proietti et al., 2012; Diaz-Espejo et al., 2013; Lobet et al., 2013). Therefore, the use of agronomical techniques that may be able to improve or preserve soil quality, health, and fertility is particularly recommended (Kushwaha and Singh, 2005; Govaerts et al., 2008; Machado et al., 2013; Pierantozzi et al., 2013). Especially in olive orchards, a positive influence of sustainable orchard management systems on soil biochemical characteristics and soil microbial genetic diversity has been observed (Hernández et al., 2005; Benitez et al., 2006; Moreno et al., 2009; Sofo et al., 2010, 2013).

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Metabolic microbial community diversity in the structure of soil bacterial and fungal communities can be estimated by different methods and techniques. One of the most reliable and interesting is the Biologs metabolic assay based on the ability of microbial isolates to oxidize different carbon and nitrogen sources (Zak et al., 1994; Insam, 1997). The community-level physiological profiles (CLPPs) obtained by the Biolog method are used to differentiate microbial populations from various soil environments or from soils subjected to different treatments (Calbrix et al., 2005; Gelsomino et al., 2006; Singh et al., 2006). It is also true that these important data should be interpreted and accompanied by the use of culture-dependent methods in order to obtain the correct characterization of the microorganisms tested, and by the determination of the activities of some soil enzymes that are important markers of soil fertility status (e.g., glucosidase, dehydrogenase, protease, and fluorescein diacetate hydrolase). As in other agroecosystems, the response of telluric microorganisms to sustainable soil practices in olive orchards depends on the duration of the treatments. In the rest of this section, we describe three examples (short-, medium-, and long-term) based on recent field research. Sofo et al. (2010) studied the effects of two soil management systems, known as “sustainable” (ST) and “conventional” (CT), on the composition and on the genetic, functional, and metabolic diversity of soil microbial communities in an olive orchard. The research was carried out during a seven-year period (short-term) in a mature olive orchard located in southern Italy under semiarid conditions (Figure 20.1). The ST system included no-tillage, integrated chemical fertilization, and organic matter input from drip irrigation, spontaneous cover crops, and pruning material shredding. In the experiment, microbial analyses were done using an integrated approach of culture-dependent (microbial cultures and Biolog) and culture-independent methods (i.e., denaturing gradient gel electrophoresis, DGGE). After seven years of treatments, the average olive yield was 8.4 and 3.1 t ha21 yr21 for ST and CT systems, respectively. CT had a significantly higher number of total culturable bacteria and actinomycetes when compared to ST, whereas fungi were significantly lower. With ST, the number of ammonifying bacteria, proteolytic bacteria, and Azotobacter in the wetted areas under the drippers (ST-WET) was much higher than along inter-rows (ST-INTER). The DGGEs of microbial 16S/18S rDNA showed differences between ST and CT, whereas 16S/18S rRNA DGGEs of

FIGURE 20.1 Comparison of sustainable (left) and conventional (right) management of a mature olive orchard (cv. Maiatica) located in southern Italy.

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ST-WET clustered in a different way from those of CT and ST-INTER. Some Biolog metabolic indexes were significantly different between ST and CT. The results of this work revealed qualitative and quantitative changes of soil microbial communities in response to sustainable agricultural practices that stimulate soil microorganism activity. The aim of another Sofo et al. (2013) study was to investigate the medium-term (12 years) effects of ST and CT on the soil microbial composition and metabolic diversity of a rain-fed mature olive orchard located in southern Italy. Although the ST system included no-till, spontaneous cover crops, and mulch derived from the pruning material, CT was managed by frequent tillage and included heavy pruning with residues removed from the orchard. Microbial analyses were carried out by culture-dependent methods (i.e., microbial cultures and Biolog). Molecular methods by light and electronic microscope were used to confirm the identification of the isolates of fungi and Streptomyces (Figure 20.2). A significantly higher number of total culturable fungi and bacteria

FIGURE 20.2 Examples of Aspergillus spp. identification in soils from an olive orchard located in southern Italy (cv. Maiatica). The orchard was subjected to a sustainable management system for 12 years. The identification was carried out by means of cultural, molecular, and light microscopy techniques (a, top) and electronic microscopy (b, bottom). Source: Thanks to Professor Ippolito Camele for some of these images.

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were found using ST. The number of fungal groups found in ST was also much higher than when the CT system was used. Generally, overall and substrate-specific Biolog metabolic diversity indices of microbial communities and soil enzyme activities were greater with ST. The results of the study of Sofo et al. (2013) demonstrated that soil microorganisms responded positively to a sustainable orchard management characterized by periodic applications of endogenous sources of organic matter. This confirmed the necessity to guide olive orchard farmers toward soil management based on organic matter inputs associated with zero tillage to ameliorate soil functionality. The abandonment of olive orchards is a phenomenon of great importance triggered mainly by economic and social causes. In such orchards, trees assume their original bushy form, canopies become dense and closed, and pioneer vegetation recolonizes free spaces according to ecological successions that tend to return, after a long time, to a natural formation (“climax”) where soil and vegetation components are in equilibrium (Loumou and Giourga, 2003). During the transition of an olive grove from a “disturbed” (cultivated) condition to a climax phase, soil properties progressively change, as found in similar agricultural systems (Zornoza et al., 2009). For this reason, the aim of a recent study by Palese et al. (2013) was to investigate some chemical, biochemical, and microbiological properties in soil of an olive grove located in southern Italy. To define the effect of long-term land abandonment (25 years) on soil properties, an adjacent olive grove, managed according to extensive practices, was taken as a reference (essentially minimum tillage and no fertilization) (Figure 20.3). Soil organic matter, total nitrogen, and pH were significantly higher in the abandoned olive grove due to the absence of tillage and the natural input of organic matter at a high CN ratio that, inter alia, increased the number of cellulolytic bacteria and stimulated the activity of β-glucosidase—an indicator of a more advanced stage of soil evolution. The soil of the abandoned olive orchard showed a lower number of total bacteria and fungi and lower microbial diversity, measured by means of the Biolog method, as a result of a sort of specialization trend toward low-quality organic substrates. From this point of view, Palese et al. (2013) concluded that extensive cultivation management did not seem to induce a disturbance to microbiological communities.

FIGURE 20.3 Comparison of a cultivated (left) and an abandoned (right) olive orchard located in southern Italy. The trees (cv. Perenzana) were planted in 1970; in 1985, three-quarters of the orchard was completely abandoned, and its appearance has taken on the form of a Mediterranean coppice with shrubs, herbs, and weeds colonizing the space between the original trees and rows (left).

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20.3 Using in situ compost production Among the agronomic sustainable practices, the input of soil organic matter as compost in olive orchards is one of the most important factors affecting soil fertility in terms of enhancement of soil permeability and water retention, better endowment and availability of nutrients for plants, higher CO2 uptake and carbon fixation, and reduction of soil erosion (Toscano et al., 2008; Toscano et al., 2009; Diacono and Montemurro, 2010; Boughalleb and Hajlaoui, 2011; MartıńVertedor et al., 2011a,b; Nadezhdina et al., 2012; Tunaho˘glu and Durdu, 2012; Garcıá et al., 2013; Rossi et al., 2013; Tomás et al., 2013; Torres-Ruiz et al., 2013a,b). The olive pomace (OP), also called “sansa vergine” in Italian or “orujo” in Spanish, is defined as the residue that remains after the first oil extraction from olives (crude olive cake). The OP is a dry material that is 8 to 10% moisture. It is composed of ground olive stones and pulp with a high lignin, cellulose, and hemicelluloses content and a 3 to 5% oil content, depending on the olive mill typology (pressure or centrifugation) (Niaounakis and Halvadakis, 2006). This by-product is generally used for residual oil extraction using solvents, heating, animal feed supplements, or as an organic amendant for olive grove or other crop soils (Alburquerque et al., 2004). In terms of its agronomic value, the OP watered with olive mill wastewater (OMWW), another product of olive milling, or with another organic material, leads to a product that supplies nutrients to plants and is an efficient method for the disposal of olive mill residuals (Hachicha et al., 2008; Sellami et al., 2008). According to the Italian law 574/1996, it is possible to use not-composted OMWW and OP for agronomic purposes, as they are considered simple plant amendants with no limitation on the amount of OP to be applied to the soil; however, CEE Regulation 91/156 indicates that composting is one of the methods to recycle and recover organic wastes. Olive mill wastewater is composed by the olives’ own water (vegetation water) and the water used in the different stages of oil elaboration (Niaounakis and Halvadakis, 2006). From an environmental point of view, OMWW is a hazard because it has a considerable organic polluting load, with a maximum biological and chemical oxygen demand of about 100 and 220 kg m23, respectively, and an average concentration of volatile solids and inorganic matter of 15% and 2%, respectively; it has an organic matter fraction that includes sugars, tannins, polyphenols, polyalcohols, pectins, and lipids (Benitez et al., 1997). Therefore, a series of studies focused on the degradation of OMWW and its chemical components (Benitez et al., 1997; Vitolo et al., 1999; Beccari et al., 2002; Amaral et al., 2008), and many authors used specific microorganisms for OMWW treatment (Robles et al., 2000; Tsioulpas et al., 2002; D’Annibale et al., 2004; Dias et al., 2004; Lanciotti et al., 2005). Microbiological and physicochemical parameters were used as indicators to study the kinetics of OMWW biodegradation such as chemical oxygen demand (COD), dissolved organic carbon, counts of heterotrophs, filamentous fungi and yeasts, and the K, P, and N content (Fadil et al., 2003; Amaral et al., 2008). Because OMWW does not generally contain sufficient N and P for an adequate aerobic purification process, its degradation may be performed by cocomposting, anaerobic digestion or enzymatic treatment (Paredes et al., 2002; Amaral et al., 2008). Some authors obtained satisfactory results, in terms of OMWW degradation and amelioration of soil physicochemical properties, by adding this liquid waste to agroindustrial and urban wastes and monitoring the physicochemical parameters during the composting process of the matrices (Paredes et al., 2000, 2001, 2005). Angelidaki and Ahring (1997) studied a combined anaerobic digestion of OMWW together with manure, household waste, or sewage sludge; with this method, they managed to degrade OMWW


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without previous dilution, without addition of external alkalinity, and without addition of an external nitrogen source. Over four months, Hachicha et al. (2008) efficiently monitored a compost made of OP, OMWW, and poultry manure by following temperature, pH, humidity, and CaN ratio to ascertain its maturity; after that, the authors tested its effectiveness in increasing potato agronomic production. Further, the cocomposting of exhausted olive cake with poultry manure and sesame shells was investigated by Sellami et al. (2008), who followed the process by studying some physicochemical parameters. Generally, the study of the composting process of olive mill by-products was focused on their physicochemical aspects. In the near future, studies need to be performed to evaluate whether mixtures of olive mill pomace, olive mill wastewater, and olive pruning residues (OPR), without adding any other additives external to olive groves, can be efficiently composted under “in farm,” nonindustrial conditions—that is, based on spontaneous aerobic degradation by autochthonous microorganisms. This method of compost production needs limited resources, low energetic inputs, and uses machinery and equipment often already present at the farm. Indeed, to be really sustainable, the composting process should be carried out using the by-products available in situ. In a study done by Casacchia et al. (2011), different mixtures of OP, OMWW, and OPR were aerobically cocomposted under natural conditions in an olive orchard located in southern Italy. During the experiment, compost temperature showed a sharp increase for the first 40 to 60 d, followed by stabilization at 60 C and a decline after 150 d; in contrast, compost water content ranged from 50 to 55% to 25 to 30%. The authors observed that Pseudomonas spp., anaerobic bacteria, actinomycetes, and fungi reached levels of 8, 7, 5, and 6 log CFU g21 compost, respectively, with a slight depression after 30 to 80 d. Total and fecal coliforms decreased significantly during composting, suggesting the lack of microbiological risk due to pathogenic microorganisms during this process. Considering that information on selective media for the microorganisms responsible for the spontaneous aerobic degradation of compost deriving from different olive materials and, in particular, from OP is lacking, Casacchia et al. (2011) also tested an innovative microbiological technique; it is based on microorganism cultivation using a broth extracted from the matrix to be composted in order to monitor the biomass degradation process during OP cocomposting. In another recent work, Casacchia et al. (2012) performed a two-year experiment with two different soils from an Italian olive orchard—one managed traditionally and the other amended with in situ produced compost. The authors observed increases in total organic matter and total nitrogen and pH in the amended soil compared to that managed traditionally. Further, significant increases in total and specific microbial counts (Pseudomonas, Bacillus, and Azotobacter) were noted in the amended soil with a clear amelioration of microbiological soil quality. The results of this 2012 study demonstrated that soil amendant using composts derived from olive mill by-products (i.e., OP, OMWW, and OPR) can be an important agricultural practice for supporting and stimulating soil microorganisms and, at the same time, for reusing the by-products, thus avoiding their negative environmental impact.

20.4 Conclusion and future prospects This chapter highlights the correct utilization of “innovative,” suitable agricultural techniques and soil management, which are important for fruit production and quality; they can also improve

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orchards’ soil quality and fertility. On the other hand, soil conservation is becoming a priority for sustainable soil management in rural areas due to the awareness of the deterioration of this natural resource and of the difficulty of efficiently recovering it (i.e., the cross-compliance concept of the European Union). As a result of different traditions, climate conditions, soils, topography, water availability, and so on, there is substantial diversity regarding olive orchard management among the Mediterranean countries. Therefore, an essential objective in the near future may be to determine a set of standards and common operating principles based on scientific knowledge. Such standards and practical procedures need to be widely and effectively disseminated to growers in every olive producing country; they need to be adopted to design and adjust the local soil management practices in order to increase microbiological diversity. This is likely to lead to improvement in olive yield and product quality. The additional benefit may be to control environmental impact, while minimizing groundand surface-water use and soil contamination through implementation of up-to-date soil management techniques.

References Alburquerque, J.A., Gonzálvez, J., Garcıá, D., Cegarra, J., 2004. Agrochemical characterisation of “alperujo”, a solid by-product of the two-phase centrifugation method for olive oil extraction. Bioresour. Technol. 91, 195200. Amaral, C., Lucas, M.S., Coutinho, J., Crespı´, A.L., do Rosário Anjos, M., Pais, C., 2008. Microbiological and physicochemical characterization of olive mill wastewaters from a continuous olive mill in Northeastern Portugal. Bioresour. Technol. 99, 72157223. Anderson, T.H., 2003. Microbial eco-physiological indicators to assess soil quality. Agric. Ecosyst. Environ. 98, 285293. Angelidaki, I., Ahring, B.K., 1997. Codigestion of olive oil mill wastewaters with manure, household waste or sewage sludge. Biodegradation 8, 221226. Barlett, M.K., Scoffoni, C., Sack, L., 2012. The determinants of leaf turgor loss point and predition of drought tolerance of species and biomes: a global meta-analysis. Ecol. Lett. 15, 393405. Beccari, M., Carucci, G., Lanz, A.M., Majone, M., Petrangeli, P.M., 2002. Removal of molecular weight fractions of COD and phenolic compounds in an integrated treatment of olive oil mill effluents. Biodegradation 13, 401410. Ben-Gal, A., 2011. Salinity and olive: from physiological responses to orchard management. Isr. J. Plant Sci. 59, 1528. Benitez, E., Nogales, R., Campos, M., Ruano, F., 2006. Biochemical variability of olive-orchard soils under different management systems. Appl. Soil Ecol. 32, 221231. Benitez, J., Beltran-Heredia, J., Torregrosa, J., Acero, J.L., Cercas, V., 1997. Aerobic degradation of olive mill wastewaters. Appl. Microbiol. Biotechnol. 47, 185188. Boughalleb, F., Hajlaoui, H., 2011. Physiological and anatomical changes induced by drought in two olive cultivars (cv Zalmati and Chemlali). Acta Physiol. Plant 33, 5365. Brady, N.C., Weil, R.R., 2008. Elements of the Nature and Properties of Soils. fourteenth ed. Pearson/Prentice Hall, Upper Saddle River, NJ, pp. 230248. Calbrix, R., Laval, K., Barray, S., 2005. Analysis of the potential functional diversity of the bacterial community in soil: a reproducible procedure using sole-carbon-source utilization profiles. Eur. J. Soil Biol. 41, 1120.

References

479

Carr, M.K.V., 2013. The water relations and irrigation requirements of olive (Olea europaea L.): a review. Exp. Agric. 49, 597639. Caruso, G., Rapoport, H.F., Gucci, R., 2013. Long-term evaluation of yield components of young olive trees during the onset of fruit production under different irrigation regimes. Irrigation Sci. 31, 3747. Casacchia, T., Toscano, P., Sofo, A., Perri, E., 2011. Assessment of microbial pool by an innovative microbiological technique in olive mill by-products co-composted under natural conditions. Agric. Sci. 2, 104110. Casacchia, T., Sofo, A., Zelasco, S., Perri, E., Toscano, P., 2012. In situ olive mill residual co-composting for soil organic fertility restoration and by-product sustainable reuse. Ital. J. Agron. 7 (e23), 3538. Castillo-Llanque, F., Rapoport, H.F., 2011. Relationship between reproductive behaviour and new shoot development in 5-year-old branches of olive trees (Olea europaea L.). Trees 25, 823832. Cuevas, M.V., Martıń-Palomo, M.J., Diaz-Espejo, A., Torres-Ruiz, J.M., Rodriguez-Dominguez, C.M., PerezMartin, A., et al., 2013. Assessing water stress in a hedgerow olive orchard from sap flow and trunk diameter measurements. Irrigation Sci. 31, 729746. Dag, A., Kerem, Z., Yogev, N., Zipori, I., Lavee, S., Ben-David, E., 2011. Influence of time of harvest and maturity index on olive oil yield and quality. Sci. Hort. 127, 358366. Diacono, M., Montemurro, F., 2010. Long-term effects of organic amendments on soil fertility. A review. Agron. Sustain. Dev. 30, 401422. Dias, A.A., Bezerra, R.M., Nazaré Pereira, A., 2004. Activity and elution profile of laccase during biological decolorization and dephenolization of olive mill wastewater. Bioresour. Technol. 92, 713. Diaz-Espejo, A., Buckley, T.N., Sperry, J.S., Cuevas, M.V., de Cires, A., Elsayed-Farag, S., et al., 2012. Steps toward an improvement in process-based models of water use by fruit trees: a case study in olive. Agric. Water Manage. 114, 3749. Diaz-Espejo, A., Nicolás, E., Nortes, P., Rodriguez-Dominguez, C.M., Cuevas, M.V., Perez-Martin, A., et al., 2013. Xylem functioning and water relations of the elastic living tissue of the bark: new insights about their coordination. Acta Hortic. 991, 163169. Ding, G.C., Piceno, Y.M., Heuer, H., Weinert, N., Dohrmann, A.B., Carrillo, A., et al., 2013. Changes of soil bacterial diversity as a consequence of agricultural land use in a semi-arid ecosystem. PLoS One 8, e59497. D’Annibale, A., Ricci, M., Quaratino, D., Federici, F., Fenice, M., 2004. Panus tigrinus efficiently removes phenols, color and organic load from olive-mill wastewater. Res. Microbiol. 155, 596603. Ehrenberger, W., Ru¨ger, S., Rodrı´guez-Domıńguez, C.M., Dıáz-Espejo, A., Fernández, J.E., Moreno, J., et al., 2012. Leaf patch clamp pressure probe measurements on olive leaves in a nearly turgorless state. Plant Biol. 14, 666674. Fadil, K., Chahlaoui, A., Ouahbi, A., Zaid, A., Borja, R., 2003. Aerobic biodegradation and detoxification of wastewaters from the olive oil industry. Int. Biodeter. Biodegr. 51, 3741. FAOSTAT, 2012. FAO Statistics. Available from: ,http://faostat.fao.org. (accessed 15.12.13). Fernández, J.E., Moreno, F., Martıń-Palomo, M.J., Cuevas, M.V., Torres-Ruiz, J.M., Moriana, A., 2011a. Combining sap flow and trunk diameter measurements to assess water needs in mature olive orchards. Environ. Exp. Bot. 72, 330338. Fernández, J.E., Rodriguez-Dominguez, C.M., Perez-Martin, A., Zimmermann, U., Ru¨ger, S., Martıń-Palomo, M.J., et al., 2011b. Online-monitoring of tree water stress in a hedgerow olive orchard using the leaf patch clamp pressure probe. Agric. Water Manage. 100, 2535. Fernández, J.E., Perez-Martin, A., Torres-Ruiz, J.M., Cuevas, M.V., Rodriguez-Dominguez, C.M., ElsayedFarag, S., et al., 2013. A regulated deficit irrigation strategy for hedgerow olive orchards with high plant density. Plant Soil 372, 279295. Fernández-Escobar, R., Garcıá-Novelo, J.M., Molina-Spria, C., Parra, M.A., 2012. An approach to nitrogen balance in olive orchards. Sci. Hortic. 135, 219226. Garcıá, J.M., Cuevas, M.V., Fernández, J.E., 2013. Production and oil quality in “Arbequina” olive (Olea eurpoaea, L.) trees under two deficit irrigation strategies. Irrigation Sci. 31, 359370.

480


Gelsomino, A., Badalucco, L., Ambrosoli, R., Crecchio, C., Puglisi, E., Meli, S.M., 2006. Changes in chemical and biological soil properties as induced by anthropogenic disturbance: a case study of an agricultural soil under recurrent flooding by wastewaters. Soil Biol. Biochem. 38, 20692080. Go´mez-del-Campo, M., 2013. Summer deficit-irrigation strategies in a hedgerow olive orchard cv. “Arbequina”: effect on fruit characteristics and yield. Irrigation Sci. 31, 259269. Go´mez-del-Campo, M., Garcıá, J.M., 2012. Canopy fruit location can affect olive oil quality in “Arbequina” hedgerow orchards. J. Am. Oil Chem. Soc. 89, 123133. Gomiero, T., Pimentel, D., Paoletti, M.G., 2011. Environmental impact of different agricultural management practices: conventional vs. organic agriculture. Crit. Rev. Plant Sci. 30, 95124. Govaerts, B., Mezzalama, M., Sayre, K.D., Crossa, J., Lichter, K., Troch, V., et al., 2008. Long-term consequences of tillage, residue management, and crop rotation on selected soil micro-flora groups in the subtropical highlands. Appl. Soil Ecol. 38, 197210. Gracia, P., Sánchez-Gimeno, A.C., Benito, M., Oria, R., Lasa, J.M., 2012. Harvest time in hedgerow “Arbequina” olive orchards in areas with early frosts. Span. J. Agric. Res. 10, 179182. Graniti, A., Faedda, R., Cacciola, S.O., Magnano di San Lio, G., 2011. Olive diseases in a changing ecosystem. In: Schena, L., Agosteo, G.E., Cacciola, S.O. (Eds.), Olive Diseases and Disorders. Transworld Research Network, Kerala, India, pp. 403433. Gruhn, P., Goletti, F., Yudelman, M., 2000. Integrated nutrient management, soil fertility, and sustainable agriculture: current issues and future challenges. Food, Agriculture, and the Environment, Discussion Paper 32. International Food Policy Research Institute, Washington DC, pp. 1518. Gucci, R., Goldhamer, D.A., Fereres, E., 2012a. Olive. In: Steduto, P., Hsiao, T.C., Fereres, E., Raes, D. (Eds.), Crop Yield Response to Water. Irrigation & Drainage Paper No. 66. FAO, Rome, Italy, pp. 298313. Gucci, R., Caruso, G., Bertolla, C., Urbani, S., Taticchi, A., Esposto, S., et al., 2012b. Changes of soil properties and tree performance induced by soil management in a high-density olive orchard. Eur. J. Agron. 41, 1827. Hachicha, S., Sallemi, F., Medhioub, K., Hachicha, R., Ammar, E., 2008. Quality assessment of composts prepared with olive mill wastewater and agricultural wastes. Waste Manage. 28, 25932603. Hammami, S.B.M., Manrique, T., Rapoport, H.F., 2011. Cultivar-based fruit size in olive depends on different tissue and cellular processes throughout growth. Sci. Hortic. 130, 445451. Hernández, A.J., Lacasta, C., Pastor, J., 2005. Effects of different management practices on soil conservation and soil water in a rainfed olive orchard. Agric. Water Manage. 77, 232248. Hochstrat, R., Wintgens, T., Melin, T., Jeffrey, P., 2006. Assessing the European wastewater reclamation and reuse potential—a scenario analysis. Desalination 188, 18. Insam, H., 1997. A new set of substrates proposed for community characterization in environmental samples. In: Insam, H., Rangger, A. (Eds.), Microbial Communities. Functional Versus Structural Approaches. Springer, New York, pp. 260261. Jagadamma, S., Lal, R., Hoeft, R.G., Nafziger, E.D., Adee, E.A., 2008. Nitrogen fertilization and cropping system impacts on soil properties and their relationship to crop yield in the central Corn Belt, USA. Soil Till Res. 98, 120129. Kushwaha, C.P., Singh, K.P., 2005. Crop productivity and soil fertility in a tropical dryland agro-ecosystem: impact of residue and tillage management. Exp. Agric. 41, 3950. Kushwaha, C.P., Tripathi, S.K., Singh, K., 2000. Variations in soil microbial biomass and N availability due to residue and tillage management in a dryland rice agroecosystem. Soil Till Res. 56, 153166. Lal, R., 2004. Soil carbon sequestration to mitigate climate change. Geoderma 123, 122. Lanciotti, R., Gianotti, A., Baldi, D., Angrisani, R., Suzzi, G., Mastrocola, D., et al., 2005. Use of Yarrowia lipolytica strains for the treatment of olive mill wastewater. Bioresour. Technol. 96, 317322.

References

481

Larbi, A., Gargouri, K., Ayadi, M., Dhiab, A.B., Msallem, M., 2011. Effect of foliar boron application on growth, reproduction, and oil quality of olive trees conducted under a high density planting system. J. Plant Nutr. 34, 20832094. Lobet, G., Page`s, L., Draye, X., 2013. First steps towards an explicit modelling of ABA production and translocation in relation with the water uptake dynamics. Acta Hortic. 991, 373381. Loumou, A., Giourga, C.H.R., 2003. Olive groves: the life and identity of the Mediterranean. Agric. Hum. Val. 20, 8795. Machado, M., Felizardo, C., Fernandes-Silva, A.A., Nunes, F.M., Barros, A., 2013. Polyphenolic compounds, antioxidant activity and L-phenylalanine ammonia-lyase activity during ripening of olive cv. “Cobrançosa” under different irrigation regimes. Food Res. Intern. 51, 412421. Martıń-Vertedor, A.I., Pérez-Rodrı´guez, J.M., Prieto-Losada, E., Fereres-Castiel, E., 2011a. Interactive responses to water deficits and crop load in olive (Olea europaea L, cv. Morisca). II: Water use, fruit and oil yield. Agric. Water Manage. 98, 950958. Martıń-Vertedor, A.I., Pérez-Rodrı´guez, J.M., Prieto-Losada, E., Fereres-Castiel, E., 2011b. Interactive responses to water deficits and crop load in olive (Olea europaea L., cv. Morisca). I: Growth and water relations. Agric. Water Manage. 98, 941949. Morales-Sillero, A., Garcıá, J.M., Torres-Ruiz, J.M., Montero, A., Sánchez-Ortiz, A., 2013. Is the productive performace of olive trees under localized irrigation affected by leaving some roots in drying soil? Agric. Water Manage. 123, 7992. Moreno, B., Garcia-Rodriguez, S., Can˜izares, R., Castro, J., Benı´tez, E., 2009. Rainfed olive farming in southeastern Spain: long-term effect of soil management on biological indicators of soil quality. Agric. Ecosyst. Environ. 131, 333339. Moriana, A., Pérez-Lo´pez, D., Prieto, M.H., Ramı´rez-Santa-Pau, M., Pérez-Rodrı´guez, J.M., 2012. Midday stem water potential as a useful tool for estimating irrigation requirements in olive trees. Agric. Water Manage. 112, 4354. Nadezhdina, N., David, T.S., David, J.S., Nadezhdin, V., Cermak, J., Gebauer, R., et al., 2012. Root function: in situ studies through sap flow research. In: Manusco, S. (Ed.), Measuring Roots, an Updated Approach. Springer, Heidelberg/Dordrecht/London/NewYork, pp. 267290. Niaounakis, M., Halvadakis, C.P., 2006. Olive Processing Waste Management: Literature Review and Patent Survey. second ed. Elsevier Ltd., Oxford, UK, pp. 340395. Palese, A.M., Magno, R., Casacchia, T., Curci, M., Baronti, S., Miglietta, F., et al., 2013. Chemical, biochemical and microbiological properties of soils from abandoned and extensively cultivated olive orchards. Sci. World J. Article ID 496278. Paredes, C., Roig, A., Bernal, M.P., Sánchez-Monedero, M.A., Cegarra, J., 2000. Evolution of organic matter and nitrogen during co-composting of olive mill wastewater with solid organic wastes. Biol. Fertil. Soils 32, 222227. Paredes, C., Bernal, M.P., Roig, A., Cegarra, J., 2001. Effects of olive mill wastewater addition in composting of agroindustrial and urban wastes. Biodegradation 12, 225234. Paredes, C., Bernal, M.P., Cegarra, J., Roig, A., 2002. Bio-degradation of olive mill wastewater sludge by its co-composting with agricultural wastes. Bioresour. Technol. 85, 18. Paredes, C., Cegarra, J., Bernal, M.P., Roig, A., 2005. Influence of olive mill wastewater in composting and impact of the compost on a Swiss chard crop and soil properties. Environ. Int. 31, 305312. Perez-Martin, A., Michelazzo, C., Torres-Ruiz, J.M., Flexas, J., Fernández, J.E., Sebastiani, L., et al., 2011. Physiological and genetic response of olive leaves to water stress and recovery: implications of mesophyll conductance and genetic expression of aquaporins and carbonic anhidrase. Acta Hortic. 922, 99106.

482


Pierantozzi, P., Torres, M., Bodoira, R., Maestri, D., 2013. Water relations, biochemical physiological and yield responses of olive trees (Olea europaea L. cvs. Arbequina and Manzanilla) under drought stress during the pre-flowering and flowering period. Agric. Water Manage. 125, 1325. Prieto, I., Armas, C., Pugnaire, F.I., 2012. Water release through plant roots: new insights into its consequences at the plant and ecosystem level. New Phytol. 193, 830841. Proietti, P., Nasini, L., Ilarioni, L., 2012. Photosynthetic behavior of Spanish Arbequina and Italian Maurino olive (Olea europaea L.) cultivars under super-intensive grove conditions. Photosynthetica 50, 239246. Rapoport, H.F., Hammami, S.B.M., Martins, P., Pérez-Priego, O., Orgaz, F., 2012. Influence of water deficits at different times during olive tree inflorescence and flower development. Environ. Exp. Bot. 77, 227233. Rewald, B., Leuschner, C., Wiesman, Z., Ephrath, J.E., 2011a. Influence of salinity on root hydraulic properties of three olive varieties. Plant Biosys. 145, 1222. Rewald, B., Rachmilevitch, S., McCue, M.D., Ephrath, J.E., 2011b. Influence of saline drip-irrigation on fine root and sap-flow densities of two mature olive varieties. Environ. Exp. Bot. 72, 107114. Robles, A., Lucas, R., Alvarez de Cienfuegos, G., Gálvez, A., 2000. Biomass production and detoxification of wastewaters from the olive oil industry by strains of Penicillium isolated from wastewater disposal ponds. Bioresour. Technol. 74, 217221. Rodrigues, M.A., Ferreira, I.Q., Claro, M.A., Arrobas, M., 2012. Fertilizer recommendations for olive based upon nutrients removed in crop and pruning. Sci. Hortic. 142, 205211. Rodriguez-Dominguez, C.M., Ehrenberger, W., Sann, C., Ru¨ger, S., Sukhorukov, V., Martıń-Palomo, M.J., et al., 2012. Concomitant measurements of stem sap flow and leaf turgor pressure 2173 in olive trees using the leaf patch pressure probe. Agric. Water Manage. 114, 5058. Rosati, A., Caporali, S., Paoletti, A., Famiani, F., 2011. Pistil abortion is related to ovary mass in olive (Olea europaea L.). Sci. Hortic. 127, 515519. Rossi, L., Sebastiani, L., Tognetti, R., d’Andria, R., Morelli, G., Cherubini, P., 2013. Tree ring wood anatomy and stable isotopes show structural and functional adjustments in olive trees under different water availability. Plant Soil 372, 567579. Sánchez-Alcalá, I., Belloń, F., del Campillo, M.C., Barroń, V., Torrent, J., 2012. Application of synthetic siderite (FeCO3) to the soil is capable of alleviating iron chlorosis in olive trees. Sci. Hortic. 138, 1723. Sanzani, S.M., Schena, L., Nigro, F., Sergeeva, V., Ippolito, A., Salerno, M.G., 2012. Abiotic diseases of olive. J. Plant Pathol. 94, 469491. Searles, P.S., Aguëro-Alcarás, M., Rousseaux, M.C., 2011. El consumo del agua por el cultivo de olivo (Olea europaea L.) en el noroeste 2207 de Argentina: una comparacioń con la Cuenca Mediterránea. Ecol. Aust. 21, 1528. Sellami, F., Jarboui, R., Hachicha, S., Medhioub, K., Ammar, E., 2008. Co-composting of oil exhausted olivecake, poultry manure and industrial residues of agro-food activity for soil amendment. Bioresour. Technol. 99, 11771188. Singh, B.K., Munro, S., Reid, E., Ord, B., Potts, J.M., Paterson, E., et al., 2006. Investigating microbial community structure in soils by physiological, biochemical and molecular fingerprinting methods. Eur. J. Soil Sci. 57, 7282. Sofo, A., Palese, A.M., Casacchia, T., Celano, G., Ricciuti, P., Curci, M., et al., 2010. Genetic, functional, and metabolic responses of soil microbiota in a sustainable olive orchard. Soil Sci. 175, 8188. Sofo, A., Ciarfaglia, A., Scopa, A., Camele, I., Curci, M., Xiloyannis, C., et al., 2013. Soil microbial diversity and activity in a Mediterranean olive orchard managed by a set of sustainable agricultural practices. Soil Use Manage. Available from: http://dx.doi.org/10.1111/sum.12097. Tomás, M., Flexas, J., Copolovici, L., Galmes, J., Hallik, L., Medrano, H., et al., 2013. Importance of leaf anatomy in determining mesophyll diffusion conductance to CO2 across species: quantitative limitations and scaling up by models. J. Exp. Bot. 64, 22692281.

References

483

Torres-Ruiz, J.M., Dıàz-Espejo, A., Morales-Sillero, A., Martıń-Palomo, M.J., Mayr, S., Beikircher, B., et al., 2013a. Shoot hydraulic characteristics, plant water status and stomatal response in olive trees under different soil water conditions. Plant Soil 373, 7787. Torres-Ruiz, J.M., Dıàz-Espejo, A., Perez-Martin, A., Hernandez-Santana, V., 2013b. Loss of hydraulic functioning at leaf, stem and root level and its role in the stomatal behaviour during drought in olive trees. Acta Hortic. 991, 333339. Toscano, P., Casacchia, T., Zaffina, F., 2008. Recuperare i reflui oleari per ri-fertilizzare i suoli. Olivo e Olio 4, 4953. Toscano, P., Casacchia, T., Zaffina, F., 2009. The “in farm” olive mill residual composting for by-products sustainable reuse in the soils organic fertility restoration. In: Proceedings of the Eighteenth Symposium of the International Scientific Centre of Fertilizers—More Sustainability in Agriculture: New Fertilizers and Fertilization Management. Rome, pp. 116121. Tsioulpas, A., Dimou, D., Iconomou, D., Aggelis, G., 2002. Phenolic removal in olive oil mill wastewater by strains of Pleurotus spp. in respect to their phenol oxidase (laccase) activity. Bioresour. Technol. 84, 251257. ¨ .F., 2012. Assessment of future olive crop yield by a comparative evaluation of Tunaho˘glu, R., Durdu, O drought indices: a case study in western Turkey. Theor. Appl. Climatol. 108, 397410. Visser, S., Parkinson, D., 1992. Soil biological criteria as indicators of soil quality: soil microorganisms. Am. J. Altern. Agric. 7, 3337. Vitolo, S., Petrarca, L., Bresci, B., 1999. Treatment of olive oil industry wastes. Bioresour. Technol. 67, 129137. Widmer, F., Rasche, F., Hartmann, M., Fliessbach, A., 2006. Community structures and substrate utilization of bacteria in soils from organic and conventional farming systems of the DOK long-term field experiment. Appl. Soil Ecol. 33, 294307. Zaitlin, B., Turkington, K., Parkinson, D., Clayton, G., 2004. Effects of tillage and inorganic fertilizers on culturable soil actinomycete communities and inhibition of fungi by specific actinomycetes. Appl. Soil Ecol. 26, 5362. Zak, J.C., Willig, M.R., Moorhead, D.L., Wildman, H.G., 1994. Functional diversity of microbial communities: a quantitative approach. Soil Biol. Biochem. 26, 11011108. Zornoza, R., Mataix-Solera, J., Guerrero, C., Arcenegui, V., Mataix-Beneyto, J., 2009. Comparison of soil physical, chemical, and biochemical properties among native forest, maintained and abandoned almond orchards in mountainous areas of Eastern Spain. Arid Land Res. Manage. 23, 267282.


CHAPTER

The Vulnerability of Tunisian Agriculture to Climate Change

21

Mohsen Mansour and Mohamed Hachicha

21.1 Introduction Climate change constitutes a real environmental problem, which is of concern for all the countries of the planet. Worldwide rapid changes in the weather are already happening and multiple consequences are expected but the degree of impact depends on which part of the world we are talking about (IPCC, 2007, 2013). According to the 2007 Intergovernmental Panel on Climate Change Fourth Assessment Report and the World Bank (2004), the Middle East and North African (MENA) regions are the most vulnerable to climate change, and this is an urgent issue (OsmanElasha, 2010; Sowers et al., 2011). However, in addition to climate changes, the MENA region already suffers from weather variability; the region experiences increasingly frequent droughts and a looming water supply shortage. It is predicted that environmental stresses will increase due to climate change (Mutin, 2009; Drine, 2011). In Tunisia, besides the North African countries, the population, life, and activities are significantly linked with the climate and its fluctuation (Agoumi, 2003). The sectors on which the economy of the country is based were identified as the most vulnerable to climate change: water, agriculture, coastal, and tourism (GTZ-MARH, 2007). Two-thirds of the country is arid to semiarid, making agriculture and water supply vulnerable to the predicted climate changes. The multiyear and recurrent episodes of drought generally affect most of the country and can lead to serious problems caused by water scarcity (Iglesias et al., 2011). The spatial and temporal changes in climatic variables relating to change have resulted in much debate and several studies are ongoing worldwide (Chattopadhyay and Hulme, 1977; Georgiadi et al., 1991; Muhs and Maat, 1993; Iglesias et al., 2004; McNulty et al., 1997; Goyal, 2004; Lindner et al., 2010; Segnalini et al., 2011). This chapter presents a summary of some local studies used to assess the impact of climate change on the agricultural sector mainly in the semiarid region of Tunisia. It is a case study, not representative for all Tunisian microclimates and also is not applicable to every agricultural system. The aim here is to call attention to the specific vulnerabilities of a sensitive, threatened region and to contribute to a better understanding of the risks and the possible impacts of climate change on agriculture.


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CHAPTER 21 The Vulnerability of Tunisian Agriculture to Climate Change

21.2 Tunisia’s agricultural constraints Tunisia is situated in North Africa at the connection of the western and oriental Mediterranean Sea between longitudes 7 and 12 East and latitudes 32 and 38 North. Covering an area of 164.000 km2, it is characterized by a pronounced climatic gradient from north to south as result of the general orientation of the main reliefs and its geographic position. Indeed, it is influenced in the north by the Mediterranean Sea, in the south by the Sahara, and in the center the combined effect of these two.

21.2.1 Climate The northern area, profitting from the Mediterranean climate, is characterized by warm and dry summers and mild and relatively rainy winters, with an average rainfallB600 mm/year. The center is semiarid to arid and is characterized by relatively hot temperatures and modest precipitation, between 200 and 400 mm/year. The rest of the country has a dry desert climate, characterized by hot temperatures as well as a large volume of irregular precipitation rarely exceeding 100 mm (Figure 21.1). Annual evaporation varies from 1300 mm to even more than 2500 mm, respectively, from the north to the south (Kallel et al., 2012). In addition, Tunisia experiences drought periods that can be generalized for the whole country or restricted to one or some regions. The drought duration and its intensity are variable in space and in time (Louati et al., 2007; Louati and Bucknall, 2010).

21.2.2 Water resources and distribution Tunisia is a water-stressed country because most of it is semiarid to arid, in addition to episodic droughts; this makes water resources scarce. The World Bank warned in 2004 that Tunisia is one of 17 countries where water resources will be an “absolute rarity” by 2025. From ancient times, Tunisia’s water and soil were considered valuable and received special attention to ensure their sustainability. Ancient civilizations that succeeded in the country developed various soil and water conservation techniques and the successful ones so far continue to be used. It is mainly water collection systems and soil conservation through various methods that are adapted to the environmental conditions. The mean yearly precipitation in Tunisia is estimated to be 36 billion m3. The available water resources of 4.8 billion m3 are divided into 2.7 billion m3 surface and 2.1 billion m3 groundwater. Being aware of the water scarcity problem, Tunisians have focused considerable effort on developing all resources; actually, more than 85% of the water resources have been mobilized using several means: dams (29), hill dams (223), check dams (812), deep wells (5000), and shallow wells (95,000) (Hamdan, 2007; Horchani, 2007; Mekki, 2009). The geographical distribution of rainfall often involves major imbalances between the north, sometimes relatively well watered, and the highly arid south. Precipitation is highly variable in space and time at monthly or yearly levels. The mean average rainfall ranges from less than 100 mm in the extreme south to more than 1500 mm in the extreme northwest (Thabet et al., 1994). Water resources are unevenly distributed across the country. Indeed, the northern region ranks first with 60%, followed by the south (22%), and finally the center (18%). Although, the northern regions occupy only 17% of the total area of Tunisia, 81.2% of surface water resources are localated in the north. On the contrary, the south has the most groundwater, particularly in deep-lying aquifers. The center is the poorest region for water resources, both in terms of quantity and in its

21.2 Tunisia’s agricultural constraints

FIGURE 21.1 Tunisia rainfall distribution.

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FIGURE 21.2 Water mobilization and transfer in Tunisia.

quality (Hamdan, 2007). The inequalities between regions make water management more difficult and explain the need to transfer surface water from the north to the center and south in order to improve the drinking water supply and ensure equity between regions (Figure 21.2). The problem of inequality of water distribution is as old as the history of the country. Indeed, by 130 AD and through the ingenuity of the emperor Hardian, the Roman (who occupied Tunisia for nearly five centuries) tried to solve the problem of water supply in the region of Carthage by constructing a huge 132 km aqueduct linking the city to the sources of Djebel Zaghouan, a real water tower (Figure 21.3). With the ancient aqueducts restored in 1860, until 1905 Zaghouan remained the main source of drinking water for the city of Tunis. Likewise, in the early eighth century, the aghlabides supplied the town of Kairouan (center of Tunisia); they transferred the groundwater and stored it in big basins (Figure 21.4). The concern about water persists because it is required for development in all social and economic sectors (Ben Abdallah, 2007).

21.2 Tunisia’s agricultural constraints

489

FIGURE 21.3 The Roman aqueduct that transferred water over the Zaghouan to the city of Carthage.

FIGURE 21.4 Aghlabid Basin in Kairouan.

Besides water scarcity, its quality constitutes an additional problem because the salinity of most water resources exceeds the international threshold for health and agricultural uses (30% with a salinity of more than 4 g/L). In fact, due to the high salinity level, only a modest proportion of the available water meets the standards for drinking water. The problem of salinity is not as pronounced for surface water, where its salt content is low to moderate (except for some tributaries of the Medjerda River), as for groundwater, which is significantly affected. Indeed, 26% of surface resources, 91.6% of shallow aquifers, and 80% of deep aquifers exceed the salinity standard of 1.5 g/L (Mamou and Kassah, 2000). What is disquieting is that salinity continues to increase as a result of overexploitation of groundwater and intrusion of the seawater. In addition, it is thought that climate change may make the situation worse through increasing evaporation and the rising sea level.

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21.2.3 Agricultural characteristics In Tunisia, the agricultural sector occupies a first-rate place in the national economy and plays an important role in regional and social development. However, it consumes the most water (83% of total available resources). As noted by Horchani (2007), 2100 million m3 of water are used for irrigation with an average consumption per ha of approximately 5500 m3/year. Water deficit and drought represent a permanent risk for Tunisian agriculture and makes production variable and highly correlated with rainy events. Indeed, the smallest part of the irrigated area (,10% of total cultivated land) constitutes an important pillar of the agricultural economy because it provides 35% of the production, 20% of the exports (of the sector), and 27% of the workforce. In addition, it plays a social role by decreasing exodus, as it provides a regular income that can be twice or may even be three times that of the rain-fed farming area (Horchani, 2007). Agricultural production in Tunisia is extensive and the main products are olive oil, citrus fruit, cereals, dates, and several horticultural products. The division of cultivated land by major crops shows the importance of cereals, mainly wheat and barley, followed by tree crops, which together cover B87% of the total cultivated area—43% cereals, 44% tree crops (mainly olives); the remaining 13% is divided between forage crops (7%), vegetable crops (3%), legumes (2.5%), and others (0.5%) (Thabet et al., 1994). Cereals followed by olive trees are the most important crops grown under rain-fed conditions. As they are the main source of food calories and the common basis of all diets, both urban and rural areas and for different income strata, cereals are considered one of the most important agricultural sectors of Tunisia’s economy. Thus, cereals, mainly wheat, are considered a vital product. On the other hand, 97% of the cereals are cultivated under rain-fed conditions. (Mougou and Ben Salem, 2003); therefore production is very variable because essentially it depends on rainfall (Mougou et al., 2008). The olive tree, widely present in the Tunisian landscape, constitutes one of the most important and traditional agricultural activities. This sector, which marks the history of Tunisia’s rural population, covers more than 1.6 million ha, representing 79% of total surface area of fruit trees and close to 35% of arable land. These trees, which are spread out all over the country under different bioclimatic conditions from the north to the south, constitute an important part of the Tunisian agriculture and play a leading socioeconomic role. In addition, the olive tree and its products make up an integral part of the daily life of Tunisians, as material as spiritual. It needs to be emphasized that olive oil contributes more than 60% to total food exports.The number of olive trees in Tunisia is estimated to be 60 million (29.5% in the north, 45.3% in the center, and 25.2% in the south). Known for its hardiness, the trees also can be found in poor marginal lands, even those threatened by erosion and desertification. The planting density of olive trees varies between regions and is generally adjusted according to mean annual rainfall. The tree is present mostly in monocultures and is rarely integrated with other fruit species. However, olive trees can be located near some vegetables or cereals especially in the center and south where the trees are often widely spaced. The status of this crop as a sacred tree, revered by generations, makes its production contribute to the income of more than 200,000 farmers and constitutes a main activity for 30% of them. In addition, approximately a million families are employed in the various functions of the oliveoil pathway (e.g., mechanization, size, crop, transport, stocking, marketing). The social attachment of farmers to olive trees has its origins in the durability of the crop, marked by its history as being the

21.3 The impact of climate change on wheat production

491

main agricultural activity of the rural population for several generations. Because of the significant attachment of the population to it, Tunisia is ranked as one the largest producers and exporters of olive oil, providing more than a fifth of world exports. The olive tree has a great capacity to adapt to different climates and may also valorize dry regions. Nevertheless, it remains sensitive to water deficit. This Mediterranean tree is able to withstand drought by the strong osmotic pressure of its root system; it is able to profit from low humidity through its capacity to close stomata to decrease evapotranspiration when the air pressure evaporation increases. However, prolonged drought is damaging to this crop. The olive tree can support about 50% of yearly water deficit; if the deficit is experienced for a second year, the tree endures the drought only in marginal zones. According to the national strategy of adaptation (GTZ-MARH, 2007), climate modifications in Tunisia may have serious consequences on water resources, ecosystems, and agrosystems, mainly on the olive and cereal sectors. With the aim of assessing the sustainability of this important crop under future climate change conditions, the studies have been carried relative to the vulnerability of this sector.

21.3 The impact of climate change on wheat production in Tunisia’s semiarid region The central region of Tunisia contains the most important area for olive cultivation and rain-fed cereals. Unfortunately, it is the most vulnerable region because of excessive climatic variability and its mainly rain-fed agriculture. In this region, water deficit and drought constitute an ongoing risk for agriculture. Rainfall is characterized by an important yearly variability and by its scarcity; consequently, production varies widely (Bergaoui, 2010). In severely dry years (deficit .50%), drought persists more frequently in the south and the center than in the north. The temperatures are moderate; however, very hot conditions are frequent and may occur from May to September. The average temperature in August is B30 C and the maximum temperature can reach 45 C. The high temperatures may affect crop production, especially when they occur at a critical stage of the growing. In addition, water resources are limited and a majority of it is of bad quality (.4 dS/m). This region is very representive of a vulnerable agricultural system and facilitates an understanding of how Tunisia’s crops may be affected by climate change. This is why the majority of the studies concerning climate change’s impact on agriculture have been done in this region; two were done with the aim of assessing the effect of future climate change on wheat production (Figure 21.5). Lhomme et al. (2009) simulated durum wheat production under climate change conditions for two regions: Jendouba and Kairouan, respectively situated in the north and the center of Tunisia; they are characterized by a typical Mediterranean climate. Although they are not very far apart, a significant rainfall gradient exists between the two regions, essentially due to the ridge of mountains that separates them (Sakiss et al., 1991). A simple crop model was used for the simulation of the 20712100 climate projection. The ARPEGE atmospheric model, developed by Mété-France (Déqué, 2007), has been used for the A1B scenario (IPCC scenario). Mougou et al. (2011) assessed the impact of projected climate change on wheat yield and the wheat growing season duration using the IPCC, 2001 scenarios of temperature increase: IS92c (11.3 C), IS92a (12 C), IS92e (12.5 C), and (14 C).

492


FIGURE 21.5 The two regions considered in the studies of Lhomme et al. (2009) and Mougou et al. (2011).

The IS92a and IS92c scenarios were used as input for MAGICC/SCENGEN simulations (Santer et al., 1990; Wigley and Raper, 1992; IPCC, 1996; Raper et al., 1996; Hulme et al., 2000). The impact of climate change on wheat production has been evaluated with the Decision Support System for Agrotechnology Transfer (DSSAT) crop model using previous simulation findings. The results showed a disparity in production according to the study region and kind of scenarios used. Lhomme et al. (2009) showed probable decreases in crop productivity in Jendouba (northern region with semiarid climate) but an increase in Kairouan (the center region with arid climate). However, Mougou et al. (2011) showed that in the Kairouan region, when applying the scenario of combined effect of temperature increase (11.5 C) and rainfall decrease (210%), wheat production can fall by 248%.

21.4 Climatic change parameters that influence evapotranspiration

493

It has been noticed also that the wheat growing season varies in relation to the increase in temperature. Mougou et al. (2011) predicted that by 2100 in the Kairounan region, the wheat growing season may be shortened by 10, 16, 20, and 30 d, respectively, for 1.3 C, 2 C, 2.5 C, and 4 C temperature conditions. Lhomme et al. (2009) found similar results, as the wheat crop cycle mean duration was reduced by approximately 25 d in the Kairouan region. The impact of growth cycle shortening can affect yield quantitatively as well as qualitatively as a consequence of damages sustained during flowering and grain filling. Therefore, in the future it may be better to sow earlier (one month before the current planting date) because of more favorable water conditions during early autumn (Lhomme et al., 2009). According to Mougou et al. (2011), wheat yield is significantly correlated with yearly total rainfall especially during the farming season, September to April, with March rainfall being of particular importance. Previous analysis of rainfall data showed that during the last century there was a highly correlated relationship between autumn rainfall quantities and the yearly precipitation amount. This can be used as a pertinent index to determine whether the year is drought prone or likely to be rainy. In fact, by a mean of 70%, drought years have started with a dry autumn. At the regional scale, this percentage is 78% and 90%, respectively, for the north and both the center and the south. Louati et al. (2005) noted that precipitation during the autumn represented 40% of the mean yearly quantity.

21.4 Climatic change parameters that influence evapotranspiration in central Tunisia’s coastal region As quoted in the World Bank report in 2004, Tunisia is expected to experience water scarcity by 2025. Due to population growth, rapid urbanization, and agricultural and industrial development, the country may face a complex situation because of the increase in water demand by the several users, and the conflicts between them may be more acute then. Under such a situation, any supplemental increase in water demand as a result of global warming probably will put tremendous pressure on existing water resources. The warming of the climate may modify water availability by changing precipitation and evaporative demand, and any changes in the climatic parameters due to rising temperatures are expected to affect evapotranspiration and crop water requirements. Many studies have shown a decrease in the evapotranspiration trend over the past decade in many places (Gao et al., 2007; Han et al., 2012). Others have reported the opposite phenomenon: an increase in the evapotranspiration trend (Gao et al., 2007; Chang-yu et al., 2006). Mougou et al. (2011) studied the Kairouan region for the impact of temperature increases on reference evapotranspiration (ETo). The results showed, respectively, an increase in ETo by 3.1%, 4.5%, and 9.4% by a temperature increase of 1.3 C, 2 C, and 4 C compared to actual values. However, the studies of Xu et al. (2006a,b) and Ohmura and Wild (2002) indicated that the ETo trend was not determined by temperature alone. That is why researchers try to study the impact of climate change on temporal trends of evapotranspiration and the climatic parameters influencing it (Mansour et al., 2010) (see Box 21.1). The PenmanMontheith methodology described in the FAO Irrigation and Drainage Paper N 56 (Allen et al., 1998) has been used for the calculation of ETo. The study evaluated a coastal

494


BOX 21.1 CALCULATION OF CROP WATER REQUIREMENTS USING FAO METHODOLOGY

Mean daily actual sunshine hours

Mean daily max. sunshine hours

n

Average monthly temp. C°

Root-square of saturated vapor pressure

Ta

√e2

Rs = (0.25 + 0.5 n/N) Ra

Rn = (0.75 R2 – 2.0(10)–9 (Ta + 273.16)4 (0.34 – 0.044 √e2)(–0.35 + 1.8Rs/Ra))/0.408

Air pressure, Kpa Psychrometric constant, a–1 KpaC

Pa = (1013 – 0.1152(h) + 5.44(10)–6h2)/10

Soil head flux, month i MJm–2 d–1 Wind speed m s–1

U2

ET e =

Crop evapotranspiration mm d–1

Source: Adapted from Hokam (2002).

h

Height above sea level, m

γ = 1615 Pa /2.49(10)6 – 2.13 (10)3Ta

Mean temp. in month i–1 C°

Potential evapotranspiration mm d–1

Ra

N

Observed solar radiation, mm d –1 Netradiation MJ m–2 d –1

Extraterrestrial radiation mm d –1

Ti+1

Tt–1

G month.t = 0.07 (Tt+1 – Tt–1) Relative humidity, % Actual vapor pressure Kpa

RH

Mean temp. in month i+1 C°

Saturated vapor pressure Kpa

es

ea= (RH/100)es

Slop of vapor pressure curve KpaCa–1 Δ

900 U2 (e2 – ea) T + 273 Δ + γ (1 + 0.34 U2)

0.408 Δ (Ra – G) + γ

ETc = ET0 * Kcadj

Kcadj

Adjusted crop coefficient

21.4 Climatic change parameters that influence evapotranspiration

495

region in the center of Tunisia (ChottMeriem: 35 55N lat, 10 34E long, 15 m alt). Daily meteorological parameters (temperature, humidity, wind speed, and sunshine hours) for 33 years (19732005) were used (Figure 21.6). The temporal trend of the climatic parameters were analyzed using the MannKendall trend test (Mann, 1945; Kendall and Gibbons, 1990; Gocic and Trajkovic, 2013). The sensitivity of ETo has been studied in terms of the change of most of the climatic parameters involved. The Kendall test used to determine the annual statistics showed that there is no statistically significant ETo trend because we obtained an unexpected clear trend evolution for the reference of

FIGURE 21.6 Study region (ChottMeriem).

496


ETo, like those shown in several previous studies sited by Gao et al. (2007) and Chang-yu et al. (2006). We tried to understand more about the cause of this result by analyzing the trend of all climatic data on which reference evapotranspiration depends. The reference evapotranspiration equation (i.e., Eq. 21.1 in Box 21.2) is the sum of two terms, known as radiation and aerodynamics, as shown in Eq. 21.2. The temporal study of each part alone shows a significant, respectively, increasing and decreasing trend of ETrad and ETaero. This opposite finding relevant to the two terms explains why a significant trend of the reference ETo was not detected. To understand more about the cause of this result, the trend of all climatic data on which the reference evapotranspiration depends was analyzed. The study showed a significant trend of temperature; however, maximum and minimum temperature does not evolve in the same way. A significant temperature trend was detected during spring and summer periods (hot season), especially for maximum temperatures. A highly significant trend for the air vapor deficit, which appears especially from May to June, was detected. The wind speed showed a significant decreasing trend during the year. Even if a similar trend was found (Chang-yu et al., 2006; Jin-liang et al., 2012), relating this decreasing trend of the wind speed to the climate change phenomenon must be considered more carefully.

BOX 21.2 THE REFERENCE EVAPOTRANSPIRATION EQUATION The ETo can be expressed, according to Allen et al. (1998), as: ETo 5

900 0:408ΔðRn 2 GÞ 1 γ T 1 273 U2 ðes 2 ea Þ Δ 1 γð1 1 0:34U2 Þ

(21.1)

where ETo 5 the reference evapotranspiration (mm day21) ETo was defined as the evaporation of an extension surface of green grass of uniform height (0.12 m) that was actively growing and adequately watered, having a surface resistance of 70 s m21 and albedo of 0.23: Rn 5 net radiation at the crop surface (MJm22 day21) G 5 soil heat flux density (MJm22 day21); T 5 mean daily temperature at 2 m height [ C] U2 5 wind speed at 2 m height [m s21] es 5 saturation vapor pressure [kPa] ea 5 actual vapor pressure [kPa] es 2 ea 5 saturation vapor pressure deficit [kPa] Δ 5 slope of vapor pressure curve [kPa C21] γ 5 psychrometric constant [kPa C21] 5 0.665 3 1023 P Equation (21.1) can be divided into two terms, as follows: ETo 5 ETrad 1 ETaero

(21.2)

With ETrad 5

0:408ΔðRn 2 GÞ Δ 1 γð1 1 0:34U2 Þ

(21.3)

ETaero 5

900 γT1 273 U2 ðes 2 ea Þ Δ 1 γð1 1 0:34U2 Þ

(21.4)


497

Because such a change in wind speed also can be the result of environmental changes around the climatic station, such as buildings rising and or tree growth, we think that this is the most realistic hypothesis. If it is the case, this may induce an error and give an incorrect idea about the ETo as consequence on the effect of future climate change on water resources. This remark is also valid for the other climatic parameters because, for climate change studies, a long series of data is needed; should the environment around the old climatic station have changed, this can influence the credibility of the measured data. The sensitivity analysis test showed that the most influential parameters on ETo are, respectively, net shortwave and longwave radiation, with the actual vapor pressure and the maximum temperature.

21.5 Conclusion and future prospects In a country poor in natural resources, such as Tunisia, agriculture plays a vital role in its economy. However, agriculture in Tunisia is vulnerable as a result of several interconnected causes. The climate variability (in time and space) combined with the aridity of most of the country means that water resources are scarce, with a deteriorated quality in most regions. Not to forget the soil resources problem, because only 47.3% of the land’s soils are fertile to moderately so, and annual soil loss represents 1%. In addition, 55% of the total area is potentially agricultural land (9 million ha); however, 50% of the irrigated land is affected by salinity (10% significantly affected). Tunisia’s agriculture produces mainly rain-fed crops and the agricultural population is made up of small farmers. Climate change, as predicted, may affect the sector and lead to important modifications of practices, mainly to enhance water availability, seeing that a water conflict is likely to occur between the different users in the future. With regard to regional specificity whether at a continental scale or for the country itself, further study is necessary in order to develop future climatic scenarios and prepare a sustainable adaptation plan for the country. As reported by Smit et al. (2000), the extent to which the several sectors related to climate (e.g., ecosystems, agriculture, health, sustainable development) are at risk due to anticipated change; this depends both on the magnitude of the phenomenon and the adaptation capacity of the impacted system. Planning for a sustainable agriculture can be undertaken using the statistical trend of climatic factors. Thus, more research programs to facilitate understanding should be done to determine what is really happening (regional climate). This needs to be followed by evaluating what kind of potential there is, and what the available adaptation possibilities are. Researchers have to know, by an objective analysis of the actual situation, the untapped potential and discover how bad things are in order to get the best value out of existing environmental conditions; this is necessary before improvements can be more efficient and actions can be taken to implement interventions. Thus, before proposing new solutions that may be costly, further studies must highlight a better way to utilize existing resources, mainly the underexploited or inappropriately exploited, to face the climate change. It is also important to take into account the farmer’s strategies and encourage the participative approach in the aim of improving traditional methods and facilitating adaptation of new technologies.

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References Agoumi, A., 2003. Vulnérabilité des pays du Maghreb face aux changements climatiques. Besoin réel et urgent d’une stratégie d’adaptation et de moyens pour sa mise en œuvre. IISD/Climate Change Knowledge Network. Available at: ,www.cckn.net//pdf/north_africa.pdf.. Allen, R.G., Pereira, S., Raes, D., Smith, M., 1998. Crop Evapotranspiration: Guidelines for Computing Crop Water Requirements, FAO Irrig. Drain. Paper 56. Food and Agriculture Organization, Rome. Ben Abdallah, S., 2007. The water resources and water management regimes in Tunisia. Agricultural Water Management: Proceedings of a Workshop in Tunisia (Series: Strengthening Science-Based Decision Making in Developing Countries), pp. 81–87. Bergaoui, M., 2010. The drought impact on agricultural crop production in Tunisia. Opt. Méditerr. Série A. Sémin. Méditerr. 95, 7174. Chang-yu, X., Gong, L., Tong, J., Chen, D., 2006. Decreasing reference evapotranspiration in warming climateA case of changjiang (Yangtze) river catchment during 19702000. Adv. Atmos. Sci. 23, 513520. Chattopadhyay, N., Hulme, M., 1997. Evaporation and potential evapotranspiration in India under conditions of recent and future climate change. Agric. For. Meteorol. 87, 5573. Déqué, M., 2007. Frequency of precipitation and temperature extremes over France in an anthropogenic scenario: model results and statistical correction according to observed values. Glob. Planet Change 57 (12), 1626. Drine, I., 2011. Climate Variability and Agricultural Productivity in MENA region. UNU-WIDER Working paper N.2011/96. Available at: www.wider.unu.edu/stc/repec/pdfs/wp2011/wp2011-096.pdf. Gao, G., Chen, D., Xu, C.Y., Simelton, E., 2007. Trend of estimated actual evapotranspiration over China during 19602002. J. Geophys. Res. 112, D11120. Georgiadi, A.G., Ven, F.H.M., van de Gutknecht, D., Loucks, D.P., Salewicz, K.A., 1991. The change of the hydrological cycle under the influence of global warming. Hydrology for the water management of large river basins, IAHS Publication No. 201, pp. 119128. Gocic, M., Trajkovic, S., 2013. Analysis of changes in meteorological variables using Mann-Kendall and Sen’s slope estimator statistical tests in Serbia. Glob. Planet Change 100, 172182. Goyal, R.K., 2004. Sensitivity evapotranspiration to global warming: a case study of arid zone of Rajasthan (India). Agric. Water Manage. 69, 111. GTZ-MARH, 2007. Stratégie nationale d’adaptation de l’agriculture tunisienne et des e´ cosyste`mes aux changements climatiques. GTZ-MARH. Hamdan, A., 2007. Suivi des progre`s dans le domaine de l’eau et promotion de politiques de gestion de la demande. Raopport National de Tunisie. Available at: ,www.planbleu.org/publications/atelier_eau_ saragosse/Tunisie_rapport_final_FR.pdf.. Han, S., Xu, D., Wang, S., 2012. Decreasing potential evaporation trends in China from 1956 to 2005: Accelerated in regions with significant agricultural influence? Agric. Forest Meteorol. 154155, 4456. Hokam, E.M., 2002. Computer-based expert system to optimize the water supply for modern irrigation systems in selected regions in Egypt. Thesis-Justus-Liebig-Universita¨t Giessen. Horchani, A., 2007. Agriculture Water Management. Proceeding of a Workshop in Tunisia. Laura Holliday, editior. National Academies Press, pp. 8896. Available at: ,www.nap.edu/catalog/11880.html.. Hulme, M., Wigley, T.M.L., Barrow, E.M., Raper, S.C.B., Centella, A., Smith, S.J., et al., Using a Climate Scenario Generator for Vulnerability and Adaptation Assessments: MAGICC and SCENGEN, vol. 2.4. Climatic Research Unit, University of East Anglia, Norwich. IPCC, 2001. Climate change 2001: the scientific basis. In: Houghton, J.T., Ding, Y., Griggs, D.J., Noguer, M., van der Linden, P.J., Dai, X., Maskell, K., Johnson, C.A. (Eds.), Contribution of Working Group I to the Third Assessment Report. Cambridge University Press, Cambridge.

References

499

IPCC, 2007. Summary for Policymaker. Contribution of Working Group I to the Fourth Assessment Report. ,http://ipcc-wg1.ucar.edu/wg1/wg1-report.html.. IPCC, 2013. Climate change 2013: the physical science basis. In: Stocker, T.F., Qin, D., Plattner, G.-K., Tignor, M., Allen, S.K., Boschung, J., et al. (Eds.), Contribution of Working Group I to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge University Press, Cambridge, United Kingdom and New York, NY, USA. Iglesias, A., Tsiourtis, N.X., Wilhite, D.A., Garrido, A., Garrote, L., Moneo, M., et al., 2004. Terms of reference for drought risk management: drought identification studies, drought risk analysis, and best practices. Medroplan Working Paper. Iglesias, A., Mougou, R., Moneo, M., Quiroga, S., 2011. Towards adaptation of agriculture to climate change in the Mediterranean. Reg. Environ. Change 11 (1), 159166. Intergovernmental Panel on Climate Change (IPCC), 1996. Climate change 1995: the science of climate change. In: Houghton, J.T., Meiro Filho, L.G., Callander, B.A., Harris, N., Kattenberg, A., Maskell, K. (Eds.), Contribution of Working Group I to the Second Assessment Report. Cambridge University Press, New York. Jin-liang, R.E.N., Qiong-fang, L., Mei-xiu, Y., Hao-yang, L., 2012. Variation trends of meteorological variables and their impacts on potential evaporation in Hailar region. Water Sci. Eng. 5, 137144. Kallel, M., Belaid, N., Ayoub, T., Ayadi, A., Ksibi, M., 2012. Effects of treated wastewater irrigation on soil salinity and sodicity at El Hajeb region (Sfax-Tunisia). J. Arid Land Stud. 22, 6568. Kendall, M.G., Gibbons, J.D., 1990. Rank Correlation Methods, fifth ed. Griffin, London. Lhomme, J.P., Mougou, R., Mansour, M., 2009. Potential impact of climate change on durum wheat cropping in Tunisia. Clim. Change 96, 549564. Lindner, M., Maroschek, M., Netherer, S., Kremer, A., Garcia-Gonzalo, J., Seidl, R., et al., 2010. Climate change impacts, adaptive capacity, and vulnerability of European forest ecosystems. For. Ecol. Manage. 259, 698709. Louati, M.H., Bucknall, J., 2010. Tunisia’s experience in water resource mobilization and management. In: Jaganathan, V.J., Mohamed, A.S., Kremer, A. (Eds.), Water in the Arab World: Management Perspectives and Innovations. The World Bank, Middle East and North Africa Region, Washington, DC, pp. 157180. Louati, M.H., Mellouli, H., El-Elchi, M.L., 2005. Tunisia. In: Iglesias, A., Moneo, M. (Eds.), Drought Preparedness and Mitigation in the Mediterranean: Analysis of the Organizations and Institutions. CIHEAM-IAMZ, Zaragoza, pp. 155190. Louati, M.H., Bergaoui, M., Lebdi, F., Methlouthi, M., El Euchi, L., Mellouli, H.J., 2007. Application of the drought management guidelines in Tunisia—part 2. Examples of application. In: Iglesias, A., Moneo, M., Lo´pez-Francos, A. (Eds.), Drought Management Guidelines Technical Annex. CIHEAM/EC MEDA, Zaragoza, pp. 417467. Mamou, A., Kassah, A., 2000. Ećonomie et valorisation de l’eau en Tunisie. Sci. Changements Planétaires/ Sécheresse 11 (4), 249256. Mann, H.B., 1945. Nonparametric tests against trend. Econometrica 13, 245259. Mansour, M., Hachicha, M., Mougou, A., 2010. Climate change and temporal trend of climatic parameters influencing the evapotranspiration: case of chatt-meriem region. In: Rhodri Thomas, F.A.O. (Ed.), Proceedings of the Global Forum on Salinization and Climate Change (GFSC2010), Valencia, Spain. McNulty, S.G., Vose, J.M., Swank, W.T., 1997. Regional hydrologic response of loblolly pine to air temperature and precipitation changes. J. Am. Water Resour. Assoc. 33, 10111022. Mekki, H., 2009. La politique de l’eau en Tunisie. Conférence régionale sur la gouvernance de l’eau, e´ change d’expériences entre l’OCDE et les pays arabes. CITET Tunis, 89 Juillet 2009.

500


Mougou, R., Ben Salem, M., 2003. Meteorological conditions in arid regions and effects of climate change in dryland crops. Proceedings of the Training on Agricultural Techniques for Rain-Fed Agriculture and Communication to Farmers. Arab Center for Studies in Dry Land Agriculture, Tunis, Tunisia. Mougou, R., Abou-Hadid, A., Iglesias, A., Medany, M., Nafti, A., Chetali, R., et al., 2008. Adapting dryland and irrigated cereal farming to climate change in Tunisia and Egypt. In: Leary, N., Adejuwon, J., Barros, V., Burton, I., Kulkarni, J., Lasco, R. (Eds.), Climate Change and Adaptation. Earthscan, London, UK, pp. 181195. Mougou, R., Mansour, M., Iglesias, Zitouna, Battaglini, A., 2011. Climate change and agricultural vulnerability: a case study of rain-fed wheat in Kairouan, central Tunisia. Reg. Environ. Change 11 (1), 137142. Muhs, D.R., Maat, P.B., 1993. The potential response of eolian sands to greenhouse warming and precipitation reduction on the Great Plains of the USA. J. Arid Environ. 25, 351361. Mutin, G., 2009. Le Monde arabe face au défi de l’eau. Enjeux et Conflits. Groupe de recherches et d’études sur la méditerranée et le moyen orient—GREMMO. Available at: ,http://hal.archives-ouvertes.fr/ hal-00352860/fr/.. Ohmura, A., Wild, M., 2002. Is the hydrological cycle accelerating? Science 298, 13451346. Osman-Elasha, B., 2010. Mapping of climate change threats and human development impacts in the Arab region. Arab Human Development Report. Research Paper Series. UNDP, New York. Available at: ,http://www.arab-hdr.org/publications/other/ahdrps/paper02-en.pdf.. Raper, S.C.B., Wigley, T.M.L., Warrick, R.A., 1996. Global sea level rise: past and future. In: Milliman, J., Haq, B.U. (Eds.), Sea-Level Rise and Coastal Subsidence: Causes Consequences and Strategies. Kluwer, Dordrecht, pp. 1145. Sakiss, N., Ennabli, N., Slimani, M.S., 1991. La pluviométrie en Tunisie. Institut National Agronomique de Tunisie et Institut National de la Météorologie, Tunis. Santer, B.D., Wigley, T.M.L., Schlesinger, M.E., Mitchell, J.F.B., 1996. Developing climate scenarios from equilibrium GCM results. Report No. 47, Max-Plank Institute for Meteorology, Hamburg. Segnalini, M., Nardone, A., Bernabucci, U., Vitali, A., Ronchi, B., Lacetera, N., 2011. Dynamics of the temperature-humidity index in the Mediterranean basin. Int. J. Biometeorol. 55, 253263. Smit, B., Burton, I., Klein, R., Wandel, J., 2000. An anatomy of adaptation to climate change and variability. Climate Variability and Change, Book Edition. Kluwer Academic Publishers, 45(1): 223251. Sowers, J., Vengosh, A., Weinthal, E., 2011. Climate change, water resources, and the politics of adaptation in the middle east and north Africa. Clim. Change 104, 599627. Thabet, B., Boughzala, M., Ben Ammar, B., 1994. Agriculture and Food Policy in Tunisia. CIHEAM, pp. 181220. Available at: ,http://om.ciheam.org/article.php?IDPDF594400058.. Wigley, T.M.L., Raper, S.C.B., 1992. Implications for climate and sea level of revised IPCC emissions scenarios. Nature 357, 293300. World Bank, 2004. Tunisia - Country Environmental Analysis (19922003) Final Report. Washington, DC: World Bank. Available at: ,http://documents.worldbank.org/curated/en/2004/04/5757452/tunisia-countryenvironmental-analysis-1992-2003-final-report.. Xu, C.Y., Gong, L.B., Jiang, T., Chen, D., 2006a. Decreasing reference evapotranspiration in a warming climate: a case of Changing (Yangtze River) catchment during 19702000. Adv. Atmos. Sci. 23, 513520. Xu, C.Y., Gong, L.B., Jiang, T., Chen, D., Singh, V.P., 2006b. Analysis of spatial distribution and temporal trend of reference evapotranspiration in Changing catchments. J. Hydrol. 327, 8193.

Index Note: Page numbers followed by “f ” and “t ” refers to figures and tables respectively.

A Abiotic stress, 23, 320, 323324, 405 aquaporins’ response to, 436439 chilling, 439 drought, 436438 nutrient deficiency, 438439 salinity, 438 habitat-imposed, 100102 in legumes, 810 drought, 910 salinity, 10 temperature, 10 nitric oxide’s role in, 249 air pollutants, 257 drought stress, 250251 heavy metal stress, 254257 high light conditions, exposure to, 257258 high temperature stress, 252253 low temperature stress, 253 salinity stress, 254 UV-B radiation, 258259 waterlogging stress, 251252 plant responses to, 2425, 25f proteomic analysis of responses to, 2555 heavy metal stress, 4145 imbalances in mineral nutrition, 3741 salt stress, 4547 temperature stress, 4755 water stress, 2637 Abiotic stress tolerance aquaporins for, 439440 in legumes, 1016 tocopherol and, 274279 drought, 276277 extreme temperature, 277278 metal toxicity, 278 ozone, 279 salinity, 275276 UV radiation, 279 Abscisic acid (ABA), 101, 251, 437438 Acacia albida, 295296 Acacia auriculiformis, 82 Acacia nilotica, 80 Acaulospora laevis, 78 ACC deaminase (ACC-D) activity, 118 Acetobacter diazotrophicus, 99

Achromobacter piechaudii, 101 Acinetobacter, 99100 Acremonium, 99 Actinomadura, 99 Acyrthosiphon kondoi, 4 Agriculture under waterlogging conditions of hydromorfic soils, case study, 302 Agrobacterium tumefacien, 8 Agrocin 84, 116t Agroecosystem (AES), 97, 309 Agroforestry, 295296 Agrostis scabra, 52 Agrostis stolonifera, 52, 235 Agrostis tenuis, 44 Air pollutants, 257 Alcohol dehydrogenase (ADH), 35 Alectra vogelii, 5 Alfalfa, 78 anthracnose, resistance to, 78 Medicago truncatula, 8 Allium porrum L., 8082 Alternaria, 99 Alternaria solani, 177, 181 Aluminum (Al), 42 Alyssum lesbiacum, 457458 Amelioration drainage practice, 300 Amino acids, 409410, 457458 1-Aminocyclopropane-1-carboxylate (ACC), 115 1-Aminocyclopropane-1-carboxylate synthase (ACCS), 101 Anabaena variabilis, 419420 Anthoxanthum odoratum L., 81 Anthracnose, 7 resistance to, 78 Anthracnose stalk rot (ASR), 201 Antibiotics, 115 Aphids, 45 Aphis glycine, 45 Apiom godmani, 45 Apple tree (Malus pumila), 40 AQP1, 432 Aquaporins, 431440 future prospects, 440441 plant, 433434 in plantwater relationship, 434436 response to abiotic stress, 436439 chilling, 439

501

502

Index

Aquaporins (Continued) drought, 436438 nutrient deficiency, 438439 salinity, 438 structure and water-conducting properties of, 432433 for tolerance of abiotic stress, 439440 Arabidopsis, 16, 40, 51, 54, 111, 114115, 233 aquaporin expression, 435 Arabidopsis ascorbate peroxidase gene (APX3), 225 Arabidopsis ascorbate-deficient (vtc1), 229 Arabidopsis guard cells, 251 Arabidopsis mutant, 115, 231 Arabidopsis thaliana, 25, 27t, 39, 4142, 46, 49t, 53, 101, 217218, 221, 227228, 232, 255, 258, 274275, 278, 462 transgenic, 281282 Arachis hypogea, 27t Arbuscular mycorrhizal (AM) fungi, 135, 140, 145 metal binding, 141142 -mycorrhizosphere, 139140 symbiosis, 69, 141 Arbuscular mycorrhizal fungi (AMF), 69, 459460 diversity of, 7172 and environmental stresses in plants, 7379 herbicides and pesticides, 7879 pathogen attack, 7778 salinity stress, 7577 water stress, 7475 ion transport in plants under stress and role of, 79 and mineral nutrition, 7982 calcium, 82 magnesium, 82 nitrogen, 8081 phosphorus, 80 potassium and K1/Na1 ratio, 81 and plant stress tolerance, 136144 enhanced metal/nutrient uptake, 138140 metal/nutrient biosorption and precipitation, 141142 soil particulate microaggregation, 143144 on soil fertility, 7273 Arbuscular mycorrhizal plants adoption into metal phytoremediation, 145152 burden of metal stress and dilemma of resource allocation, 150152 plantsoil experimental perspectives, 146150 ARPEGE atmospheric model, 491 Arsenic (As), 44, 219, 256257 sources of, 217t Ascochyta blight, 56 resistance to, 67 Ascochyta rabie, 3

Ascochyta rabiei, 6 Ascorbate (AsA), 228229 Ascorbate peroxidase (APX), 224, 321 Ascorbateglutathione cycle, 226 Aspergillus, 99 Aspergillus spp. identification in soils, 474f Association mapping (AM), 327 Aster tripolium, 7576 AtMYB44, 14 Atomic absorption spectrophotometer (AAS), 451 AtP5CR gene, 14 Atriplex nummularia, 417418 Atriplex semibaccata, 417418 Auxins, 461 under stress, 230231 Avr gene, 173 Azospirillum brasilense, 101, 112t Azospirillum spp., 99

B Bacillomycin, 116t Bacillomycin D, 116t Bacillus, 99100 Bacillus amyloliquefaciens, 112t, 116117 Bacillus cereus, 112t, 115 Bacillus licheniformis, 112t Bacillus pumilus, 99100, 112t Bacillus species, 99, 112t Bacillus subtilis, 112t, 116117 Bacterial artificial chromosome (BAC) libraries, 6 Bacterial leaf blight and leaf streak, 202203 Bacterial leaf streak (BLS), 202 Barley (Hordeum vulgare), 51 land conservation strategies for, 295f prevention of potential diseases of, 203205 leaf rust, 204205 net blotch, 203 powdery mildew disease, 204 scald, 203204 spot blotch, 205 Barley net form net blotch (NFNB), 203 “Baula” drainage system, 308 Bean golden mosaic virus (BGMV), 4 Bean leafroll virus (BLRV), 4 Bermuda grass, 3132 Beta vulgaris L, 27t Biogas, sustainable production of, 335f Biologs metabolic assay, 473 Biotic stresses for legumes, 25 biotechnological interventions for, 58 alfalfa, 78 chickpea, 67

Index

foliar diseases, 3 fungi, 2 insects and pests, 45 parasitic weeds, 5 plant viruses, 34 Biotrophic fungi, 77 Blister beetle (Mylabris pustulata Thunberg), 4 Blumeria graminis, 194 Blumeria graminis f. sp. hordei (Bgh), 204 Boron, 38t Botrytis cinerea, 3, 114115 Botrytis gray mold, 3 Brachypodium distachyon, 197 Brassica, 392 Brassica campestris, 14 Brassica juncea, 42, 224, 227228, 230, 458461 Brassica napus, 27t, 39, 358 Brassinosteroids (BRs), 462 Breeding programs physiological attributes (PAs) for, 323324 Breeding salinity-tolerant plants, manipulating osmolytes for, 385 Brown fields, 449 Brown spot, 202 Bruguiera gymnorrhiza, 223, 459 Bulbine natalensis, 234 Burkholderia phytofirmans, 101102 Bypass channels, 304

C Ca21, 390 Cadmium (Cd), 42, 220221, 358359 sources of, 217t Cadmium stress, nitric oxide production under, 255256 CaETR-1 sequence, 7 Cakile maritime, 275 Calcineurin B-like proteins (CBL), 386387 Calcium, 82 deficiency, 363 Calendula officinalis L. plants, 272273 Calreticulin, 54 Canopy spectral reflectance (CSR), 325 Carbohydrates and salinity tolerance, 393395 Carduus, 7071 Carissa spinaram, 27t, 49t, 52 Carnation (Dianthus caryophillus), 110111 Casuarina equisetifolia, 415 Catalase (CAT), 223224, 321 Catharanthus roseus, 276277 Cell wall proteins (CWP), 35 Cell-to-cell transport, 431 Cercosporazeae-maydis, 200201

503

Chelating agents, 455459, 457f amino acids, 457458 growth-promoting bacteria, 459460 mycorrhizae, 459460 plant growth-promoting rhizobacteria (PGPRs), 460 organic acids, 458459 phytins, 458 ChiB gene, 113 Chickpea (Cicer arietinum), 67, 32 Ascochyta blight, resistance to, 67 Chicory, 49t Chilling, 439 Chlamydomonas reinhardtii, 256 Chlorella vulgaris, 233234 Chlorophyll fluorescence (ChlF) kinetics, 347348 analysis of, 350351 applications of drought, 351355 heavy metals, 358359 herbicides, 370 nutrient deficiency, 359363 ozone, 369370 photosynthetically active radiation, 363367 salinity, 356357 temperature, 367369 future prospects, 370 and heterogeneity of PSII, 349350 Choline monooxygenase (CMO), 392393 Chromium, sources of, 217t Cicer arientinum L., 27t Cicer arietinum, 67, 32, 419 Citrus tangerine, 76, 415 Citrus taxa, 7475 Citrus variegated chlorosis (CVC), 99100 Clean technology. See Phytoremediation Climate change, 485 impact on wheat production in Tunisia’s semiarid region, 491492 Cochliobolus miyabeanus, 202 Cochliobolus sativus, 205 Cold stress, 5355. See also Low temperature stress Cold temperature (CT) stress, 412414 Coldheat stress, 414 Collectotrichum crown rot disease, 78 Colletotrichum, 98 Colletotrichum destructivum, 3 Colletotrichum gloeosporioides, 177 Colletotrichum trifolii, 3, 7 Comamonas, 99100 Common beans (Phaseolus vulgaris), 16 Compatible osmolytes, 388

504

Index

“Compatible solutes”, 388389 Conservation agriculture, 294295 Constructed wetlands (CWs), 333 Contaminants, phytoremediation of, 449450 Contaminants in soil, water, and plants, 450452 remediation technology, 450 Conventional breeding, 1112 “Conventional” (CT) soil management system, 473475 Copper, 220221, 256 sources of, 217t Copper transporter (CTR), 218 Cotton, prevention of potential diseases of, 205206 cotton leaf curl virus, 206 fusarium wilt, 206 root-knot nematode (RKN) disease, 205206 verticillium wilt, 206 Cotton leaf curl virus, 206 Cowpea, 4, 1516 heat stress, 1516 biotechnological interventions for, 16 responses to, 15 Crop plants, effects of salinity on, 174176 Cryphonectria parasitica, 178 Cucumber (Cucumis sativus), 40, 110111 Cucumis melo, 417 Cucumis sativus, 40, 80, 110111, 417 Curtobacterium flaccumfaciens, 99100 Cyanobacteria, 419420 Cyanodon dactylon (L.) Pers X Cyanodon transvaalensis Burtt Davy, 27t Cyanodon dactylon, 27t Cystiene, 409 Cytokinins (CKs), 14, 461 under stress, 233235

D DCMU poisoning method, 349 Decision Support System for Agrotechnology Transfer (DSSAT) crop model, 491 Deep vertical soil aeration, 309 Dehydration-responsive element-binding (DREB), 13 Dehydroascorbate reductase (DHAR), 225226 Denaturing gradient gel electrophoresis (DGGE), 99100 Desalination, 299 Detention ponds, 333 2,4-Diacetylphloroglucinol (DAPG), 115, 116t Dianthus caryophillus, 110111 Digital imaging platforms, 326 Dike, 304 2,3-Dimethyl-6-phytyl-1,4-benzoquinone (DMPBQ), 272

Diseases, prevention of, 193 of barley, 203205 leaf rust, 204205 net blotch, 203 powdery mildew disease, 204 scald, 203204 spot blotch, 205 of cotton, 205206 cotton leaf curl virus, 206 fusarium wilt, 206 root-knot nematode (RKN) disease, 205206 verticillium wilt, 206 of maize, 199201 anthracnose stalk rot (ASR), 201 gray leaf spot (GLS), 200201 head smut, 200 maize streak virus (MSV) disease, 199 northern leaf blight (NLB), 199200 Stewart’s disease, 200 of rice, 201203 bacterial leaf blight and leaf streak, 202203 blast, 201 brown spot, 202 sheath blight, 202 of wheat, 194199 fusarium head blight, 198 Karnal bunt, 198 powdery mildew, 194195 Stagonospora nodorum blotch, 198199 wheat rust disease, 195197 Drainage coefficient, 305 DREB proteins, 331 Drip irrigation, 334335 Drought, 351355 and legume production, 910 tocopherol and, 276277 Drought factor index (DFI), 354 Drought stress, 2634, 118, 119t, 250251, 436438 in changing environments, 319320 proteomic analysis of plant responses to, 27t Drought tolerance, 315319 breeding approaches, 331332 genome-wide selection (GWS), 331332 marker-assisted selection (MAS), 331 candidate genes associated with, 328330 crop growth and response to water deficits, 320321 drought-related genes, identification and characterization of, 326330 drought stress in changing environments, 319320 future prospects, 332336 osmotic adjustment, 322 precise phenotyping for, 325326

Index

canopy spectral reflectance, 325 digital imaging platforms, 326 magnetic resonance imaging and nuclear magnetic resonance, 325326 near-infrared spectroscopy, 325 proteomic studies, 330331 quantitative trait loci (QTL) and association mapping for, 327328 screening genotypes, methodologies for, 322323 targeted breeding programs, physiological attributes for, 323324 water deficit, 320 Drought-tolerance attributes, precise phenotyping for, 325326

E Economic water scarcity, 315 Economic yield, 320 Ectomycorrhiza, 6970 Effector-triggered immunity (ETI), 110 Electron transport activity (ETS), 234 Eleusine coracana, 99 Endomycorrhiza, 69 Endophytes, sustainable use of, 100102 Endophytic bacterium, 99 Endophytic microbes, 97 endophyte diversity, 98100 sustainable use of endophytes and habitat-imposed abiotic stress, 100102 5-Enolpyruvylshikimate 3-phosphate (EPSP) synthase, 270 Enterobacter, 100 Enterobacter cloacae, 99100 Enterobacter sp, 112t Environmental stress, 268, 405, 407408 Enzymatic antioxidants, 222227 ascorbate peroxidase (APX), 224 catalase, 223224 dehydroascorbate reductase (DHAR), 225226 glutathione reductase, 226227 superoxide dismutase (SOD), 222223 Erwinia carotovora, 114115 Erwinia carotovora subsp. carotovora bacteria, 179180 Erysiphe pisi, 3 Erythrina variegata, 415 Escherichia coli, 116117 Ethylene (ET), 110, 113 Ethylene-insensitive root-1 (eir1) gene, 115 Eucalyptus spp, 27t Eucalyptus urophylla, 114115 Evapotranspiration (ETo), 492 Evapotranspiration, 492496 Exopolysaccharides (EPS), 101, 118

505

Expressed sequence tags (ESTs), 328 Extreme temperature, 277278

F Fagus sylvatica, 279 Faidherbia albida, 295296 Fatty-acid methyl ester (FAME) analysis, 99100 Fengycin, 116t Ferricchelate reductase (FCR) activity, 231 Festuca arundinacea, 258 Festuca pratensis, 49t, 5355 Field crops, 450, 463 as hyperaccumulators, 453455 Flooding stress, 3437 Flood-relief channel. See Bypass channels Fluorescein, 114 Foliar diseases, 3 Fructans, 407, 407f Fructosyl transferases (FTs), 407 Fungal foliar diseases, 5 Fungal growth, salinity on, 176182 negative effects of, 176179 negative effects on plant growth of salinity in combination with fungi, 180182 positive effects of, 179180 Fungal stress, 58 alfalfa, 78 anthracnose, resistance to, 78 Medicago truncatula, 8 chickpea, 67 Ascochyta blight, resistance to, 67 Fungi, 2 Fusarium, 9899 Fusarium culmorum, 176177 Fusarium head blight, 198 Fusarium oxysporum, 78, 176, 179 Fusarium oxysporum f.sp. radicis-lycopersici (Forl), 164, 181 Fusarium oxysporum f.sp. vasinfectum, 179180 Fusarium oxysporum lycopersici, 167 Fusarium sambucinum, 177 Fusarium solani, 162, 163f, 165f, 167, 182 Fusarium vasinfectum, 164166 Fusarium wilt, 206 Fussarium sp., 110111

G Gaeumannomyces graminis var. tritici, 115 γ-aminobutyric acid (GABA), 409 γ-glutamylcysteine synthetase (γ-ECS), 228 γ-Toc methyltransferase (γ-TMT), 272, 275 Genome-wide association study (GWAS), 200

506

Index

Genotype-by-sequencing (GBS) approach, 202203, 331 Geranylgeranyl diphosphate (GGDP), 271272 Gibberellic acids under stress, 231233 Gibberellins (GAs), 231 Gigaspora margarita, 78 Girdle beetle (Obereopsis brevis), 4 Gliotoxin, 116t Globoids, 458 Glomalin-related soil protein (GRSP), 73 Glomus estunicatum, 81 Glomus fasciculatum, 78 Glomus intraradices, 75, 101102 Glomus mosseae, 7576 Glomus sp., 71, 78 Gluconacetobacter, 99100 Glutamine biosynthetic pathway, 410f Glutamine synthetase (GS), 4243 Glutathione (GSH) biosynthesis pathway, 42, 227228 Glutathione peroxidase (GPX), 321 Glutathione reductase, 226227 Glutathione synthetase (GS), 228 Glutathione-S-transferase (GST), 321 Glycerol, 409 Glycine betaine (GB), 411, 414415, 417418 in salinity tolerance, 392393 Glycine max, 1116, 27t, 39, 49t, 53 Glycophytes, 4546 GmCKX gene, 14 GmDREB3 gene, 14 GmIPT gene, 14 Gray leaf spot (GLS), 200201 Green bug (Nezara viridula L.), 4 Green technology. See Phytoremediation Green/clean technology, 452 Greenhouse gases (GHG) emissions, 294295 Growth-promoting bacteria, 459460 GSNO reductase (GSNOR), 250 GTP-binding protein, 42 Guignardia, 98

H Habitat-imposed abiotic stress, 100102 Hazardous stress, preventing. See Diseases, prevention of Hb/NO cycle, 252 Head smut, 200 Heat absorbers, 351 Heat stress, 4852, 367, 369 Heavy metal pollution, sources of, 216 Heavy metal stress, 4145, 254257, 418419 arsenic, 256257 cadmium, 255256

copper, 256 zinc, 257 Heavy metal toxicity in plants, 218221 direct effects, 218220 indirect effects, 220221 Heavy metals, 215, 358359, 451452 cadmium, 358359 lead, 358 Hedylapta indicator, 4 Hel gene, 113 Helianthus annuus, 461 Helianthus tuberosus L., 417 Helicoverpa armigera, 45 Helicoverpa punctigera, 45 Herbaspirillum spp., 99 Herbicides, 370 Herbicolin, 116t Hibiscus annus plants, 274 Hibiscus rosa-sineses, 274 High light conditions, exposure to, 257258 High temperature (HT) stress, 252253, 412414 High-efficiency irrigation systems (HEIS), 316317, 334335 High-throughput phenotyping (HTP), 325 Histidine, 409 Homogentisate phytyltransferase (HPT), 272 Hordeum vulgare, 27t, 49t, 51 Host plant resistance, 205 Hyaloperonospora arabidopsidis, 115 2-Hydroxy phenazines, 115 Hyperaccumulators, 452 field crops as, 453455 Hypoxia, 251252 Hypoxic stress, 252

I Idriella licualae, 98 In situ compost production, 476477 Inbred mapping (IBM) population, 199200 Indole-3-acetic acid (IAA), 100, 230231 Induced systemic tolerance (IST), 101, 109 Inorganic osmolytes, 388 in salinity tolerance, 389390 Insects and pests, 45 International Commission on Irrigation and Drainage (ICID), 296 International Triticeae Mapping Initiative (ITMI), 196 International Water Management Institute (IWMI), 318 Inter-specific-sequence-repeat (ISSR) markers, 6 Ionic stress, salinity-induced, 386388 Ipomoea aquatic, 459460 Iron, 38t, 114 deficiency, 362

Index

Irrigated agriculture, improvement of crop production in, 296299 Isopentenyl diphosphate (IPP), 271 Iturin A, 116t

J Jasmonate (JA), 110, 112114 JIP-test, 348, 350351

K

K1 ion, for salinity tolerance, 390 Kandelia candel, 223 Karnal bunt, 198 Kendall test, 494495 Kokuria, 99100

L Land and water management strategies for crop production improvement, 291292 future prospects, 309310 in irrigated agriculture, 296299 in rain-fed agriculture, 292296 in (transiently) waterlogged agroecosystems, 299309 in water-deficient agroecosystems, 292299 Lead, 358 sources of, 217t Leaf blight, 199200 Leaf damage index (LDI), 162 Leaf folder (Hedylapta indicator), 4 Leaf rust, 204205 Leaf rust resistance genes, 195 Legume, 1 abiotic stresses in, 810 drought, 910 salinity, 10 temperature, 10 biotechnological interventions for abiotic stress tolerance in, 1016 cowpea, 1516 soybean, 1115 biotechnological interventions for biotic stress tolerance in, 58 alfalfa, 78 chickpea, 67 biotic stresses for, 25 foliar diseases, 3 fungi, 2 insects and pests, 45 parasitic weeds, 5 plant viruses, 34 productivity of, 1 stresses affecting production of, 2

507

Licualaramasaui, 98 Lipid peroxidation, 280 Lipid peroxyl radicals (LOO•), 273274, 280281 L-myoinositol-1-phosphate synthase (MIPS), 416 Lolium multiflorum, 459460 Lolium perenne, 418 Low temperature stress, 253 Low-molecular-weight organic acids (LMWOAs), 458459 Lupinus albus, 41, 4445 Lycopersicum esculentum, 43, 275

M Macrophomina phaseolina, 78, 114115, 162, 176 Magnaporthe oryzae, 201 Magnesium, 82 deficiency, 362 Magnetic resonance imaging (MRI), 325326 Maize, prevention of potential diseases of, 199201 anthracnose stalk rot (ASR), 201 gray leaf spot (GLS), 200201 head smut, 200 maize streak virus (MSV) disease, 199 northern leaf blight (NLB), 199200 Stewart’s disease, 200 Maize streak virus (MSV) disease, 199 Malus hupehensis roots, 252 Malus pumila, 40 Manganese (Mn), 44 Mannitol, 408 Marker-assisted backcrossing (MAB), 6 Marker-assisted selection (MAS), 6, 197, 327 Mechanism-induced systemic resistance (ISR), 110112, 113f Medicago osativa, 460 Medicago sativa, 78, 418, 459460 Medicago sp., 3 Medicago truncatula, 1, 78, 1617, 40, 230 Meloidogyne incognita, 205 Meloidogyne javanica, 115 Mercury, sources of, 217t Mercury inhibition, 435 Metal contamination, 450452 Metal phytoremediation, 134135 adopting arbuscular mycorrhizal plants into, 145152 burden of metal stress and dilemma of resource allocation, 150152 plantsoil experimental perspectives, 146150 Metal pollution, 133134 Metal stress, burden of, 150152 Metal stress, plant responses to, 215 enzymatic antioxidants, 222227 ascorbate peroxidase (APX), 224 catalase, 223224

508

Index

Metal stress, plant responses to (Continued) dehydroascorbate reductase (DHAR), 225226 glutathione reductase, 226227 superoxide dismutase (SOD), 222223 heavy metal pollution, sources of, 216 heavy metal toxicity, 218221 direct effects, 218220 indirect effects, 220221 nonenzymatic antioxidants, 227229 ascorbate (AsA), 228229 glutathione, 227228 plant defense systems, 221229 plant growth hormones, 229235 auxins under stress, 230231 cytokinins under stress, 233235 gibberellic acids under stress, 231233 transport and distribution of metal in plants, 216218 Metal toxicity, tocopherol and, 278 Metal/nutrient biosorption and precipitation, 141142 Metal/nutrient uptake, 138140 Metalloids, 450 Metallothioneins (MTs), 41, 4344 2-Methyl-6-phytyl-1,4-benzoquinone (MPBQ), 272 Methyl jasmonate (MeJA), 113 Methylerythrotol phosphate (MEP) pathway, 270 Methylobacterium spp., 99100 Microarray, 13 Microbacterium, 99100 Microbial endophytes. See Endophytic microbes Micrococcus, 99100 Micromonospora, 99 Middle East and North African (MENA) regions, 485 Mineral nutrition, imbalances in, 3741 deficient concentrations, 3741, 38t Mole drainage, 308 Molecular techniques, 462 Moling. See Mole drainage Molybdenum, sources of, 217t Monodehydroascorbate (MDHA), 224226 Mucna pruriens, 114115 Multiparent advanced generation inter-cross population (MAGIC), 202203 Mung beans (Vigna radiata), 16 Musa spp, 27t Mycorrhiza, 82, 459460 Mycorrhizal fungi, 69, 134135 Mycorrhizal inoculation, 75 Mycorrhizal symbioses, 70 Mycorrhizosphere, 143144, 149150 Mycosubtilin, 116t Mylabris pustulata Thunberg, 4 Myo-inositol, 408

N N deficiency-responsive proteins, 40 Na1, 390 NaCl stress, 254, 416 NahG, 111 Natural chelating agents, 455, 458459 Near-infrared spectroscopy, 325 Nerol, 177 Net blotch, 203 Nezara viridula L., 4 Nickel, 220 sources of, 217t Nicotiana tabacum, 234235 Nitration, 249250 Nitric oxide (NO), 274, 418 in abiotic stress, 249 air pollutants, 257 drought stress, 250251 heavy metal stress, 254257 high light conditions, exposure to, 257258 high temperature stress, 252253 low temperature stress, 253 salinity stress, 254 UV-B radiation, 258259 waterlogging stress, 251252 Nitric oxide synthase (NOS), 251, 253, 258 Nitrogen, 38t, 8081 deficiency, 360 Nitrogen-fixer microorganisms, 471 Nitrosothiols, 250 Nocardia, 99 Nocardia sp., 99100 Nocardiopsis, 99 Nodulin26-like intrinsic proteins (NIP), 434 Nonenzymatic antioxidants, 227229 ascorbate (AsA), 228229 glutathione, 227228 Nonhalophytes, 4546 Northern leaf blight (NLB), 199200 NPR-1 protein, 112113 Nramp aluminum transporter 1 (Nrat1) transporter, 217218 NTR1 gene, 14 Nuclear magnetic resonance, 325326 Nutrient deficiency, 119t, 120, 359363, 438439 calcium, 363 iron, 362 magnesium, 362 nitrogen, 360 phosphorus, 360 potassium, 360362 sulfur, 363

Index

O Obereopsis brevis, 4 Ochrobactrum sp., 99 Ocimum basilicum L., 75 Oidium sp., 3 Olive mill wastewater (OMWW), 476477 Olive orchards, sustainable soil management in, 471475 future prospects, 477478 using in situ compost production, 476477 Olive pomace (OP), 476 Olive pruning residues (OPR), 477 Open drainage-channel network, 305306 Organelle proteomic approaches, 36 Organic acids, 458459 Organic contaminants, 449 Organic osmolytes, 389 in salinity tolerance, 391395 carbohydrates, 393395 glycinebetaine, 392393 proline, 391392 Ornithopus sp., 3 Orobanche crenata, 5 Orobanche foetida, 5 Oryza sativa, 27t, 39, 46, 49t, 53, 462 OsGH-2 gene, 231 Osmolyte dynamics, 405406 future prospects, 420421 osmoprotectants, 406411 amino acids, peptides, and amines, 409410 metabolic expression and exogenous application of, 412420 quaternary ammonium compounds, 411 sugars and polyols, 406409 Osmolytes, 389 general description of, 385, 388389 inorganic, 389390 organic, 391395 Osmoprotectants in plants, 406411 amino acids, peptides, and amines, 409410 metabolic expression and exogenous application of, 412420 heavy metal stress, 418419 pesticide toxicity, 419420 salinity stress, 416418 temperature stress, 412414 water deficit, 414416 quaternary ammonium compounds, 411 sugars and polyols, 406409 fructans, 407 glycerol, 409 mannitol, 408 myo-inositol, 408

509

raffinose family oligosaccharides (RFOs), 407408 sorbitol, 409 trehalose, 408 Osmoregulation adjustment during drought stress, 322 Osmotic stress, 119t salinity-induced, 386388 Oxidative stress, 267, 274276, 278, 280 metal toxicity and, 278 UV-B-induced, 279 Oxygen deprivation, 34 Oxygen-evolving enhancer protein 1 OEE1 (OEC), 5455 Ozone, 369370 Ozone stress, tocopherol and, 279

P P deficiency-responsive proteins, 3940 P5CS gene, 75 Paenibacillus polymyxa, 101, 112t Pakistan, rain-fed agriculture in, 315, 316f, 318, 319t Pal1 gene, 113 PAMP-triggered immunity (PTI), 110 Panax ginseng, 256 Panicum sphaerocarpon, 81 Pantoea, 99100 Pantoea agglomerans, 99100 Pantoea sp., 99 Paraglomus occultum, 76 Parasitic fungi, 2 Parasitic weeds, 5 Partial root-zone drying (PRD) irrigation strategy, 297298 Paspalum vaginatum, 417 Pathogenesis-related (PR) gene, 111 Pathogenesis-related (PR) proteins, 110 Pdf1.2 gene, 113 Pea (Pisum sativum), 40 Peanut Stem Necrosis Disease, 4 Pectate lyase (PL), 179180 PenmanMontheith methodology, 492494 Performance index (PI), 354 Periurban cropping, 298299 Peronospora viciae, 3 Pestalotiopsis, 98 Pesticide toxicity, 419420 Phaseolus coccineus, 274 Phaseolus vulgaris, 16, 27t, 99, 101 Phelipanche aegyptiaca, 5 Phenazine-1-carboxamide (PCN), 115 Phenazine-1-carboxyclic acid (PCA), 115 Phenazines, 116t 2-Phenyl-4,4,5,5,-tetramethylimidazoline-1-oxyl 3-oxide (PTIO), 257 Phenylalanine ammonia-lyase (PAL), 113

510

Index

Phillyrea angustifolia, 272 Phoma, 9899 Phomopsis, 98 Phosphorus, 38t, 80 deficiency, 360 Photoinhibition, 365 Photosynthetically active radiation (PAR), 325, 363367 Photosystem II (PSII), 347 chlorophyll a fluorescence and, 349350 Phragmites communis, 254 P-hydroxyphenylpyruvate (HPP), 270271 Phyllosticta, 9899 Physical water scarcity, 315 Physiological attributes (PAs) for targeted breeding programs, 323324 Phytins, 458 Phytocentric mechanism, 134 Phytochelatins (PCs), 41 Phytochrome B protein, 42 Phytodegradation, 454t Phytoextraction, 333334, 454t, 455462 chelating agents, 455459 amino acids, 457458 growth-promoting bacteria and mycorrhizae, 459460 mycorrhizae, 459460 organic acids, 458459 phytins, 458 plant growth-promoting rhizobacteria (PGPRs), 460 future prospects, 463 molecular techniques, 462 plant growth regulatory substances (PGRs), 460462 auxins, 461 brassinosteroids, 462 cytokinins, 461 Phytohormone assisted phytoremediation, 460461 Phytohormones, 405, 418. See also Plant growth hormones Phytomining, 453 Phytopathogenic fungi, 2 Phytophthora, 162 Phytophthora capsici, 162, 177 Phytophthora citrophthora, 183 Phytophthora parasitica, 181182 Phytophthora spp., 78 Phytoremediation, 134, 449, 452453 field crops as hyperaccumulators, 453455 Phytostabilization, 454t Phytotransformation, 453 Phytovolatalization, 333334, 454t Phytyldiphosphate (PDP), 271 Picea abies, 52 Pin gene, 113114 Piriformospora indica, 31

Pistacia versa L., 80 Pisum sativum, 27t, 40, 49t, 5355, 223, 233234 Plant aquaporins, 433434 Plant disease, 193 Plant growth hormones, 229230 under stress, 230235 auxins, 230231 cytokinins, 233235 gibberellic acids, 231233 Plant growth regulators, 229 Plant growth regulatory substances, 460462 auxins, 461 brassinosteroids, 462 cytokinins, 461 Plant growth-promoting bacteria (PGPB), 109 -elicited plant response against abiotic stress, 117120 -elicited response of plants against biotic stress, 110114 -mediated induced systemic tolerance, 117f -produced elicitors of ISR against biotic stress, 114117 antibiotics, 115 siderophore, 114115 volatiles, 115117 Plant growth-promoting rhizobacteria (PGPR), 163164, 460 mechanisms of action of, 166167 “Plant remedy”, 134 Plant viruses, 34 Plantago lanceolata L., 8082 Plantsoil experimental perspectives, 146150 Plasma membrane intrinsic protein (PIP), 76, 433434, 439440 Pod borers, 45 Polychlorinated biphenyl (PCB), 462 Polyethylene glycols (PEGs), 323 Polygalacturonase (PG), 179180 Polyols, 389, 406409 Polyunsaturated fatty acids (PUFA), 280281 Populus catahayana 3 P. kangdingensis C Wang et Tung, 27t Populus catahayna Rehder, 27t Populus cathahayana, 33 Populus deltoides, 27t Populus deltoides 3 Populus nigra, 27t, 33 Populus euphratica, 49t, 52 Populus tremula 3 P. tremuloids, 49t Populus 3 euramericana plants, 27t, 3233 Porteresia coarctata, 46 Portulaca, 52 Post-translational modification (PTM) pattern, 4647 Potassium, 38t deficiency, 360362 Potassium and K1/Na1 ratio, 81 Powdery mildew, 194195, 204 Pratylenchus minyus, 181

Index

Proline metabolism, 417 as osmoprotectant, 410 in salinity tolerance, 391392 Proteolytic bacteria, 471 Proteome, 25 Proteomics, 4647 and metabolomics techniques, 37 Proton-dependent oligopeptide transport (POT) family protein, 4344 Prunus persica, 49t, 53, 55, 8182 Pseudane, 116t Pseudomonas, 100 Pseudomonas aeruginosa, 112t Pseudomonas alcaligenes, 164 Pseudomonas chlororaphis, 101102, 115 Pseudomonas fluorescence, 460 Pseudomonas fluorescens, 112t, 114117 Pseudomonas mendocina, 101102 Pseudomonas pseudoalcaligenes, 164 Pseudomonas putida, 114115, 118, 166 Pseudomonas sp., 99100, 112t Pseudopeziza medicaginis, 3 Puccinia hordei, 204205 Puccinia striiformis f. sp. tritici (Pst), 197 Pyoluteorin (PLT), 115, 116t Pyoverdin, 114 Pyrenophora tritici-repentis, 199 Pyrroline-5-carboxylate reducatse (P5CR), 391 Pyrroline-5-carboxylate synthase (P5CS), 391 Pyrrolnitrin (PRN), 115 Pyrrolnitrin, 116t Pythium aphanidermatum, 78, 181 Pythium oligandrum, 176 Pythium parasitica, 78

Q Quantitative trait loci (QTL), 12, 199200, 323, 326328 Quaternary ammonium compounds, 411 Quercus ilex, 27t, 33 Quercus robur L, 27t

R Raffinose family oligosaccharides (RFOs), 407408, 414 Rain-fed agriculture, 318 improvement of crop production in, 292296 Rainwater harvesting, 295 Ralstonia, 100 Ralstonia solanacearum, 114115 Random amplified polymorphic DNA (RAPD) markers, 6 Reaction centers (RCs), 351

511

Reactive nitrogen species, 249250 Reactive oxygen species (ROS), 24, 35, 76, 101, 118, 215, 220, 250251, 267, 276, 280, 321, 438, 451452 Reduced glutathione (GSH), 250 Regulated deficit irrigation (RDI), 297298 Resource allocation, dilemma of, 150152 Rhizobacteria, biological control of fungal disease by, 161 biological control, 164166 plant growth-promoting rhizobacteria (PGPR), 163164 mechanisms of action of, 166167 salinity and plant pathogens, 162 Rhizobium, 99100 Rhizobium meliloti, 114115 Rhizobium tropici, 101 Rhizoctonia solani, 3, 164166, 202 Rhizofilteration, 454t Rhopalosiphum padi, 176177 Rhynchosporium secalis, 203 Rice, prevention of potential diseases of, 201203 bacterial leaf blight and leaf streak, 202203 blast, 201 brown spot, 202 sheath blight, 202 Rice cropping in low-efficient irrigation systems, 296297 Root-associated bacteria, 163164 Root-knot nematode (RKN) disease, 205206 Rumex acetosella L., 81

S Saccharomyces cerevisiae, 176 S-adenosylmethionine (SAM), 53, 101 SAG12-ipt gene, 235 Salicylic acid (SA), 110 Saline-adapted fungal pathogens, crop plants under, 173 behavior of, 182183 effects of salinity on crop plants, 174176 effects of salinity on fungi, 176182 negative effects of salinity on fungal growth, 176179 negative effects on plant growth of salinity in combination with fungi, 180182 positive effects of salinity on fungal growth, 179180 pathological defense mechanisms under salt stress, 183184 pathological responses of salt-tolerant plants, 184 Salinity -induced ionic and osmotic stress and tolerance mechanisms, 386388 and legume production, 10 tocopherol and, 275276

512

Index

Salinity stress, 254, 356357, 416418, 438 Salinity tolerance future prospects, 395 inorganic osmolytes in, 389390 organic osmolytes in, 391395 carbohydrates and, 393395 glycinebetaine, 392393 proline, 391392 Salt overly sensitive (SOS) pathway, 386387 Salt stress, 4547, 118, 119t, 386 pathological defense mechanisms under, 183184 in Triticum dicoccum, 393 Salt-responsive proteins, 46 Salt-tolerance mechanism in plants, 387f Salt-tolerant plants, pathological responses of, 184 Salt-tolerant rhizobacteria, 163164 Salvia lyrata L., 81 Salvia officinalis, 234235 Sansa vergine, 476 Sarcocornia fruticosa L., 357 Scald, 203204 Scanalyzer 3D, 326 Schizaphis graminum, 176177 Sclerocystis dussii, 78 Sclerotinia sclerotiorum, 182 Sclerotium rolfsii, 179180, 182 Sedum alferdii, 461 Serial analysis of gene expression (SAGE), 333 Sesbania aegyptiaca, 80 Sesbania grandiflora, 80 Sesuvium portulacastrum, 459 Sheath blight, 202 Side (lateral) channels, 304 Siderophore, 114115 “Silent reaction centers” (RCsi), 351 Small basic intrinsic proteins (SIP), 434 S-nitrosoglutathione (GSNO), 250, 257 S-nitrosylation, 250 Sodium nitroprusside (SNP), 253259 Soil fertility, 471, 476 Soil particulate microaggregation, 143144 “Soil remediation” 449 Soilplant water relationship, 291294 Solana pyrones, 6 Solanum chilense, 46 Solanum lycopersicum, 40, 235, 418 Solanum nigrum, 257 Solanum tuberosum, 27t Sorbitol, 409 Sorbitol-6-phosphate dehydrogenase (S6PDH), 409

Soybean, 1115 drought resistance biotechnological intervention for, 1112 marker-assisted selection for, 12 genetic engineering, 1315 Spartina maritima, 459 Spirulina platensis, 259 Spodoptera litura Fab., 4 Spot blotch, 205 Sr2 gene, 195198 Sr2/Yr30 genes, 196 Stagonospora nodorum, 198199 Staphylococcus, 99100 Stemphylium vesicarium, 3 Stenotrophomonas strain, 166 Sterility Mosaic Disease, 4 Stewart’s disease, 200 Streptomyces, 99 Streptomyces marcescens, 112t Streptosporangium, 99 Streptoverticillium, 99 Stress affecting legume crop production, 2 behavior of auxins under, 230231 behavior of cytokinins under, 233235 behavior of gibberellic acids under, 231233 -tolerant plants, 24 Striga gesnerioides, 5 Strigolactones, 7071 Suaeda salsa, 52 Subsurface pipeline drainage systems, 306307 Sucrose phosphate synthase (SPS), 394 Sugars and polyols, 406409 Sulphur deficiency, 363 Superoxide dismutase (SOD), 222223, 321 Superoxide radicals forming peroxynitrite, 249 Surface drainage systems, 305306 Sustainable soil managements, 471475 future prospects, 477478 using in situ compost production, 476477 “Sustainable” (ST) soil management system, 473475 Sweet bean, 4 Swingle citrumelo plants, 415416 Symbiodinium microadriaticum, 253 Synthetic chelating agents, 455 Systemic acquired resistance (SAR), 110111

T Tainung 67 (TNG 67), 48 TaMYB73 gene, 233 Tan spot, 199 Telluric microorganisms, 471

Index

Telomeric segmentation, 205206 Temperature and ChlF technique, 367369 Temperature and legume production, 10 Temperature extremes tocopherol and, 277278 Temperature stress, 4755, 118, 119t, 412414 cold stress, 5355 heat stress, 4852 Thellungiella halophila, 25, 49t, 5354 Thinopyrum ponticum, 46 Tilletia indica, 198 Tobacco caterpillar (Spodoptera litura Fab.), 4 Tobacco necrosis virus (TNV), 114115 Tocopherol, 267268 and abiotic stress tolerance, 274279 drought, 276277 extreme temperature, 277278 metal toxicity, 278 ozone, 279 salinity, 275276 UV radiation, 279 antioxidative role of, 279282 biosynthesis and accumulation in plants, 270272 chemistry and types of, 268269 forms of, 267268 future prospects, 282 in plant growth and physiology, 272274 Tomato (Solanum lycopersicum), 40 Tonoplast intrinsic protein (TIP), 232233, 434 Transcriptomic tools, 12 Transgenic Arabidopsis thaliana, 281282 Transgenic Chlamydomonas reinhardtii, 419 Transgenic Oryza sativa, 419 Transgressive segregation, 205 Trehalose, 408 Trehalose phosphate synthetase (TPS), 408 Trichoderma harzianum, 78 Trifolium alexandrium, 80 Trifolium subterraneum, 3 Triticum aestivum, 27t, 46, 49t, 53, 195, 419 Triticum boeoticum, 195 Triticum durum, 27t Tunisian agriculture, 485 climatic change parameters that influence evapotranspiration, 492496 constraints, 486491 agricultural characteristics, 489491 climate, 486 water resources and distribution, 486488, 488f future prospects, 497 vulnerability to climate change, 485 wheat production, impact of climate change on, 491492

513

Turnip crinkle virus (TCV), 114115 Tyrosine aminotransferase (TAT), 270271 Tyrosine nitration, 249250

U Ubiquitin (Ub)/proteasome-mediated proteolysis, 37 Uromyces, 3 Uromyces anthyllidis, 3 Uromyces striatus, 3 UV radiation tocopherol and, 279 UV-B radiation, 258259

V Vanadium, sources of, 217t Vegetative storage protein (VSP), 113114 Verticillium albo-atrum, 179180, 182184 Verticillium dahliae, 164166, 181 Verticillium species, 176 Verticillium wilt, 206 Vicia faba, 80, 223225 Vigna radiata, 16, 226227, 230 Vigna unguiculata, 1516, 99 Vitamin E. See Tocopherol Vitis vinifera L, 27t Volatile organic compounds (VOCs), 115116, 118 Volatiles, 115117 Vulpia ciliate var. ambigua, 78

W Water deficit, 414416 crop growth and response to, 320321 as major abiotic factor limiting crop yields, 320 Water scarcity, 291, 315 Water stress, 2637, 309 drought stress, 2634 flooding stress, 3437 Water-deficient agroecosystems, strategies for improving crop production in, 292299 irrigated agriculture, 296299 rain-fed agriculture, 292296 Waterland management strategies, 291 Waterlogged agroecosystems, improving crop production in, 299309 agriculture under waterlogging conditions of hydromorfic soils, 302 general, large-scale strategies, 304305 specific, small-scale strategies, 305309 types of waterlogging and impact on crop production, 299302

514

Index

Waterlogging stress, 3435, 251252 Water-use efficiency (WUE), 292, 293f, 297 drought yield adaptation, 324 Weevils, 45 Wheat, prevention of potential diseases of, 194199 fusarium head blight, 198 Karnal bunt, 198 powdery mildew, 194195 Stagonospora nodorum blotch, 198199 wheat rust disease, 195197 Wheat rust disease, 195197 Wheat-associated bacteria, 166167 White lupine (Lupinus albus), 41 Wild soybean, 1112

X X (for unrecognized) intrinsic proteins (XIPs), 434 Xanthobaccin A, 116t Xanthomonas, 99100

Xanthomonas campestris, 99100 Xanthomonas malvacearum, 164166 Xanthomonas oryzae pv. oryzae (Xoo), 202 Xylariaceae, 9899 Xylariaceous fungi, 98 Xylella fastidiosa, 99100

Y Yr26 gene, 197

Z Zabrodes subfasciatus, 45 Zea mays, 27t, 31, 39, 101, 221, 224, 234235 Zeaxanthin, 356357 Zinc, 147149, 257 sources of, 217t Zn-phytates, 458 Zwittermicin A, 116t