Carnivorous Plants

16 downloads 0 Views 635KB Size Report
Keywords : Carnivorous Plants, Nepenthes, Nepenthes khasiana, carnivory, ... there exists no dividing line between carnivorous and have been discovered ...
DOI No. 10.5958/2322-0996.2014.00015.5

REVIEW ARTICLE

Carnivorous Plants: The molecular biology behind the wonder plants 1

1

Amrita Saxena , Richa Raghuwanshi and H. B. Singh*

2

1

Department of Botany, Mahila Mahavidyalaya, Banaras Hindu University, Varanasi, U.P. - 221005 Department of Mycology and Plant Pathology, Institute of Agricultural Sciences, Banaras Hindu University, Varanasi, U.P. - 221005 2

Abstract

Downloaded From IP - 14.139.225.181 on dated 24-Mar-2015

www.IndianJournals.com

Members Copy, Not for Commercial Sale

Nature has a plethora of fascinations with its microbial diversity to its unusual live forms. One of the many fascinations that have caught the interest of both scientists as well as common man are the insect eating plants. Against the conventionally prevailing norm of autotrophy among plants, this group has been successful in setting ripples in the scientific world. This article gives brief information regarding the habitat and nutrition of the group along with its evolutionary history describing the diversity that persists. The role of molecular biology in solving many unsolved mysteries concerning the mechanisms involved in the probable adaptation of carnivory by the group has been elucidated. The only species endemic to India, Nepenthes khasiana, has been described with its conservation and cultivation strategies employed. Owing to their different mode of nutrition, appearance and habitat, these can be referred to as the “Non-Veggies” of plant kingdom!! Keywords : Carnivorous Plants, Nepenthes, Nepenthes khasiana, carnivory, digestive enzymes.

Introduction

Insectivorous plants have derived their name

wonderful plant of the world”. No doubt Venus fly trap has been reported to be having the most fastest trapping mechanisms known in plants2, 3. However, not all were so thrilled and captivated by these strange members of plant kingdom. The great Swedish naturalist Carl Linnaeus, on knowing about insect trapping by Venus Fly trap declared the act, “against the order of nature as willed by the God”.

from their unusual mode of hetrotrophy found in the autotrophic group of plants. This group has attracted botanists; evolutionary ecologists and horticulturists since many centuries. This group for the first time was collected for study by Thomas Jefferson in 1970. He collected Venus fly traps near Charleston, South Carolina, for study. Further, it was Charles Darwin who completely described the group and confirmed their carnivorous syndrome in his book

Many scientists have worked on defining the group, however, only few records could are found available that clearly defines the Carnivorous plants.

“Insectivorous Plants”1. He gave experimental evidences confirming the hetrotrophic mode of nutrition of these plants with experiments explaining the hair trigger speed of the traps of Venus fly trap on coming in contact with an insect. He even compared the swiftness in closing of traps with muscle contraction found in animals calling Dionaea muscipula Ellis (Venus fly trap) as “one of the most

According to Givinsh4 there are two major conditions to be fulfilled by the plant to be said carnivorous. A plant must be able to absorb nutrition from dead animals juxtaposed to their surfaces and should demonstrate increment in its growth, survivability, pollen and seed production. Also, it should have an unambiguous adaptation which demands for active attraction, capture and digestion of prey. However,

*Corresponding Author Email : [email protected]

27

there exists no dividing line between carnivorous and non carnivorous plants as reported by Jan Schlauer.

have been discovered based on the kind of trapping mechanisms used and their geographic distribution (Figure1).

Evolutionary History

Nutrition and Habitat

Due to the unavailability of fossils records for the group of plants, a clear evolutionary history of the plants could not be deciphered. Being a fascination for evolutionary ecologists, botanists and horticulturists for centuries, it has been reported that these plants have evolved over six times independently within different angiosperms subclasses involving both monocotyledons and

Carnivorous plants are inhabitants of nutrient poor environments and supplement normal photolithotrophic mode of nutrition by trapping and utilizing prey, typically consisting of members from

Downloaded From IP - 14.139.225.181 on dated 24-Mar-2015

dicotyledons5. Among the million known species of flowering plants, only 630 species of plants have been known to develop as carnivorous plants. Ecologists suggest the role of nutrition, environmental stress and availability of resources for

Members Copy, Not for Commercial Sale

www.IndianJournals.com

REVIEW ARTICLE

Dionaea (Venus' flytrap) • Single species • Found in South-eastern North Carolina and adjacent South Carolina

Nepenthes (Tropical pitcher plant) About 75 species are known Generally found in Southeast Asian tropics, Australia, Malaysia, and India to Madagascar

Darlingtonia (California pitcher plant) • Single species known • Found in Northem California and adjacent Oregon

Drosera (Sundew) • About 100 species • Found worldwide, especially South Africa and Australia

Heliamphora (South American pitcher plant) • Approximately 5 species known • Generally found in Venezuela, Guyana, Brazil

Cephalotus (Australian Pitcher plant) • Single species known • Found in Western Australia Sarracenia (Trumpet pitcher plant) • Approximately 10 species known • Generally found in Southeastern United States, with one species extending a cross Canada

Fig. 1: The different classes of insectivorous plants and their geographical distribution

the development of possible carnivory in this group of plants. They have been considered as a model system for addressing wide array of ecological and evolutionary questions owing to their convergent evolution. Many genuses of insectivorous plants 28

crustaceans, mites, rotifers and protozoa6. Wet meadows and peat bog moss have been reported to be common habitats for these plants, while some are reported to be found in still fresh water ponds or even on wet, seeping rock cliff7. Extensive growth of insectivorous plants has been reported in areas and forests that have periodic fires owing to the decreased competition and open habitat available for them to flourish8. Uptake of important nutrients like nitrogen, phosphorous and organic carbon has been well discussed and reported to be obtained from the prey digestion and its subsequent absorption in the respective traps of the plants9. However, some species of Utricularia have been reported to photosynthesize signifying the fact that it derives its requirement of organic C from conversion of solar energy while only the mineral uptake required by the plant is fulfilled by capture, digestion and absorption of the prey10. Also, it has been testified that the organic C obtained through photosynthesis aids the microbial community dwelling in the traps that eventually supplies the plant with the required nutrients just similar to the situation of the rhizosphere interaction in terrestrial plant11. But still, in nutrient poor soils, these plants are at an advantage over normal plants in acquiring nutrition in a more efficient manner which cannot be 12

obtained through conventional means . Also, in Biotech Today, Vol. 4, No. 1, January-June 2014

REVIEW ARTICLE

bogs, sunlight is found abundantly, so even a less capable carnivorous plant can survive by photosynthesizing and catching prey. Actually, these plants have made up for the shortage of nutrients in their habitat by trapping and digesting insects that act as supplement to their diet13. Types of Traps

Downloaded From IP - 14.139.225.181 on dated 24-Mar-2015

www.IndianJournals.com

Members Copy, Not for Commercial Sale

These plants are grouped on the basis of the traps they expertise for catching their prey. Sometimes, even their names give the hint of the kind of traps that group uses. However, it is interesting to note that all the kinds of traps these plants use; they all are actually modifications of their leaves. Also, two types, active and passive traps have been reported on the basis of their effectiveness to the prey (Figure 2) and much studies have been carried out to study the

mechanisms involved in prey catching14, 15.

Role of Molecular Biology

The evolutionary roots of this group is found to be linked to India, with the aqueous plant commonly called by name snap trap (Aldrovanda vesiculosa)

which was first reported from India in 169616. Interestingly, the genome of this group is found to contain 97% of useful genes while only 3% of the whole genome was found to contain junk genes. This is in contrast to what is generally found in human and

other higher organisms. This was related to the consecutive evolution of the group through different subclasses of angiosperms deleting the junk DNA from the genome 17 and thereby keeping only relative gene set required for their unusual assembly for trapping preys. Some species like Utricularia gibba and Genlisea aurea possess the smallest haploid genomes in angiosperms having genome size of 80 and 60 megabases respectively, almost less than half of the genome size of Arabidopsis thaliana with varying number of bacterial sized chromosomes between species18 .Not to be surprised by the fact that special and modified protocols for the isolation of the genetic material have been developed which had undoubtedly facilitated the molecular studies19. Molecular tools and techniques have given clarification for many inexplicable queries regarding the mode of nutrition and carnivorous nature of the plant furnishing better perspective of these wonder plants. The transcriptomic studies have yet opened new ventures throwing light on the mechanisms responsible for the successful adaptation of these plants to carnivory and the probable involvement of different parts of the plant in acquisition of nutrition. Studies have reported that the traps and leaves have the most similar transcriptome confirming traps to be the modification of leaves. Further, it was reported that phosphate uptake and genes responsible for respiration mainly occur in traps while nitrogen uptake takes place at other vegetative parts of the plants20. Not only the physiology is made clear through trancriptomic studies, evolutionary linkages have been redefined. In a recent study by Srivastave

Fig. 2: Different classes of Traps found in insectivorous plants

Biotech Today, Vol. 4, No. 1, January-June 2014

et al.17 it have been reported that Sarracenia species are genetically related to Vitis vinifera, from the order Ericales. 29

REVIEW ARTICLE

The prevalence of digestive enzymes has been reported to be found in trap fluid and traps of carnivorous plants21 22. Also, significant enzymatic secretions have been attributed to the commensal organisms residing in the traps of these plants11. The digestive enzymes found to play important role in carnivory belong to the class of chitinases, hydrolases and phosphatases. Nepenthes khasiana was found to demonstrate differential expression of subclass 1a and 1b chitinases when secretory region

Downloaded From IP - 14.139.225.181 on dated 24-Mar-2015

chitin24. Recently, protein modeling studies have been done to study the molecular and functional evolution of chitinases responsible for the carnivory

Members Copy, Not for Commercial Sale

www.IndianJournals.com

of the trap was analyzed23. It was further studied in Drosera species that subclass1a is constitutively expressed in secretory tips while subclass 1b was found to show elevated expression in response to

in Caryophyllales25. Interesting finding was reported by Kurup et

26

al showing the role of blue fluorescence in prey trapping by pitcher plants. Also, the development of the emissions gradually increases with the development of the pitcher which decreases with the ageing of the plant. Carnivorous plants specially pitcher plants have been reported to provide a

proving to be an ideal system for recombinant protein farming27. A lot have been contributed to the knowledge of the carnivorous plants, still much need to be done. The genomic information of few species will provide a blue print to study the anomalous behavior of these groups of plants. Nepenthes khasiana: The Indian demon flower The genus Nepenthes is notably one of the most glorious and spectacular genus of carnivorous plants owing to their enormous and dangerously looking traps and is the only genus in the family Nepenthaceae. First records about the pitcher plants were given by the Governor of French colony Etienne de Flacourt in 165827 while the name was coined by Linnaeus recalling the narcotic (nepenthe) used by the Helen of the Troy to intoxicate her guests. Mostly, it is also called by names such as tropical pitcher plants or monkey cups. The genus has a geographic distribution ranging from Southeast Asia which constitutes its centre of diversity and then westwards into Seychellas and eastern Madagascar and south to Australia28,29,30. More than 100 species are known to fall in this genus and vary in their structure of pitcher, positioning of pitcher traps (lower pitchers, upper pitchers) and sometimes to the alleviation of their habitat from sea level (lowland species, highland species)31. In India, pitcher plant (Nepenthes khasiana) is found in Khasi hills of Meghalaya, named tiewrakot by the local people, meaning demon flower or devouring-plant (Figure 3, 4 and 5). It is supposed to be the only known species of pitcher plant in India which has a much localised distribution and is

Fig. 3: Nepenthes khasiana plant growing outside a house in Nagaland, India

suitable inducible system for protein secretion 30

reported to be critically endangered32,33. For its conservation, many steps have been taken like propagation of pitcher plants through tissue culture. In north eastern India, these plants are also sold as Biotech Today, Vol. 4, No. 1, January-June 2014

REVIEW ARTICLE

decorative plants, the idea perpetuated by Prof. Pramod Tandon, an eminent botanist and former Vice Chancellor, North Eastern Hill University, Shillong, who have pioneered in technique for mass propagation of the endangered species though tissue culture. Numerous nurseries have adopted their method and have commercialised the propagation of these plants in different cities of India like Delhi, Mumbai and Bangalore. Conclusion

Nature has created a balance by developing some strange and some unique creatures that bear the responsibility of maintaining homeostasis, but the continuous human intervention has resulted in an imbalance in nature. Though the insects and flies might feel happy at the decreasing number of insectivorous plants but it would be dismay at our part to let loose the extraordinary creation of Nature.

Downloaded From IP - 14.139.225.181 on dated 24-Mar-2015

www.IndianJournals.com

Members Copy, Not for Commercial Sale

Inspite of being a wonder in them, certain group of

these plants are at a higher risk of being endangered. Environmental changes have not left this group of plants unaffected. Release of industrial wastes in bogs has extensively increased the nitrogen content which is proving fatal for the survival of the carnivorous plants. Also human interference such as poaching has threatened the sheer existence of these plants so much that the botanists are keeping the location of rare species a secret. Development of residential areas by removing or filling bogs and meadows has also resulted in sharp fall in the number of carnivorous plants. Also, the competition by other plants is pressing against their growth and development.

Fig. 4: Pitcher plants cultivated at the campus of North -Eastern Hill University, Shillong, India

Fig. 5: It is our responsibility to protect the diversity of “Nature” Biotech Today, Vol. 4, No. 1, January-June 2014

References 1.

Darwin C. (1875). Insectivorous Plants, Appleton and Company.

2.

Iijima T and Sibaoka T. (1985). Membrane potentials in excitable cells of Aldrovanda vesiculosa trap-lobes. Plant and Cell Physiology 26: 1-14.

3.

Karlsson PS, and Pate JS. (1992). Contrasting effects of supplementary feeding of insects or mineral nutrients on the growth and nitrogen and phosphorus economy of pygmy species of Drosera. Oecologia 92 (1): 8–13.

4.

Givnish TJ, Burkhardt EL, Happel RE and Weintraub JD. (1984). Carnivory in the bromeliad Brocchinia reducta, with a 31

REVIEW ARTICLE

cost/benefit model for the general restriction of carnivorous plants to sunny, moist nutrientpoor habitats. American Naturalist 124: 479497. 5.

Jobson RW and Morris EC. (2001). Feeding ecology of a carnivorous bladderwort (Utricularia uliginosa, Lentibulariaceae). Australasian Ecology 26(6):680-69.

7.

Siene R, Porembski S and Barthlott W. (1996). A neglected habitat of carnivorous plants: Inselbergs. Feddes Report 106: 555562.

Members Copy, Not for Commercial Sale

9.

Downloaded From IP - 14.139.225.181 on dated 24-Mar-2015

6.

8.

www.IndianJournals.com

Ellison AM and Gotelli NJ. (2001). Evolutionary ecology of carnivorous plants, Trends in ecology and evolution 16: 623-629.

Barker NG and Williamson GB. (1988). Effects of a winter fire on Sarracenia alata and S. psittacina. American Journal of Botany 75: 138–143. Ellison AM and Gotelli NJ. (2009). Energetics and the evolution of carnivorous plantsDarwin's “most wonderful plants in the world”. Journal of Experimental Botany 60(1): 19-42.

10. Sirová D, Adamec L and Vrba J. (2003). Enzymatic activities in traps of four aquatic species of the carnivorous genus Utricularia. New Phytologist 159(3): 669-675. 11. Sirová D, Borovec J, Cerná B, Rejmánková E, Adamec L and Vrba J. (2009). Microbial community development in the traps of aquatic Utricularia species. Aquatic Botany 90(2):129136. 12. Thoren LM and Karlsson PS. (1998). Effects of supplementary feeding on growth and reproduction of three carnivorous plant species in a subarctic environment. Journal of Ecology 86 (3): 501–510. 32

13. Williams S E. (2002). Comparative physiology of the Droseraceae sensu strict How do tentacles bend and traps close? Proceedings of the 4th International Carnivorous Plant Society Conference. Tokyo, Japan. 77-81. 14. Poppinga S, Hartmeyer SRH, Seidel R, Masselter T, Hartmeyer I and Speck T. (2012). Catapulating tentacles in a sticky carnivorous plant. PLoS ONE 7(9): e45735. doi:10.1371/journal.pone.0045735. PMC 3458893. PMID 23049849. 15. Kundu SR, Basu S and Chakraverty RK. (1996). Aldrovanda vesiculosa Linn.—its maiden appearance and disappearance from India: a review. Journal of Economic and Taxonomic Botany 20: 719–724. 16. Srivastava A, Rogers WL, Breton CM, Cai L and Malmberg RL. (2011). Transcriptome Analysis of Sarracenia, an Insectivorous Plant. DNA Research 18: 253–261. 17. Greilhuber J, Borsch T, Müller K, Worberg A, Porembski S. and Barthlott W. (2006). Smallest Angiosperm Genomes Found in Lentibulariaceae, with Chromosomes of Bacterial Size. Plant Biology 8(6):770-777. 18. Bekesiova I, Nap JP and Narova LA. (1999). Isolation of High Quality DNA and RNA from Leaves of the Carnivorous Plant Drosera rotundifolia.. Plant Molecular Biology Reporter 17: 269–277. 19. Ibarra-Laclette E, Albert VA, Pérez-Torres CA, Zamudio-Hernández F, Estrada MJO, Herrera-Estrella A and Herrera-Estrella L. (2011). Transcriptomics and molecular evolutionary rate analysis of the bladderwort (Utricularia), a carnivorous plant with a minimal genome. BMC Plant Biology 11:101. 20. Sirová D, Borovec J, Santruckova H, Biotech Today, Vol. 4, No. 1, January-June 2014

REVIEW ARTICLE

21.

Downloaded From IP - 14.139.225.181 on dated 24-Mar-2015

22.

www.IndianJournals.com

Members Copy, Not for Commercial Sale

23.

24.

25.

Santrucek J, Vrba J and Adamec L. Utricularia (2010). Carnivore revisited: plants supply photosynthetic carbon to traps. Journal of Experimental Botany 61(1): 99-103. Plachno BJ, Adamec L, Lichtscheidl IK, Peroutka M, Adlassnig W and Vrba J. (2006). Fluorescence Labelling of Phosphatase Activity in Digestive Glands of Carnivorous Plants. Plant Biology 8(6):813-820. Matusíková I, Salaj J, Moravcíková J, Mlynárová L, Nap JP and Libantová J. (2005). Tentacles of in vitro-grown round-leaf sundew (Drosera rotundifolia L.) show induction of chitinase activity upon mimicking the presence of prey. Planta 222:1020–1027. Eilenberg H, Pnini-Cohen S, Schuster S, Movtchan A and Zilberstein A. (2006) Isolation and characterization of chitinase genes from pitchers of the carnivorous plant Nepenthes khasiana. Journal of Experimental Botany 57:2775-2784. Renner T and Specht CD. (2013). Molecular and functional evolution of class I chitinases for plant carnivory in the Caryophyllales, MBE Advance Access, 1-51. Kurup R, Johnson AJ, Sankar S, Hussain AA, Kumar CS, Baby S. (2013). Fluorescent prey traps in carnivorous plants. Plant Biology 15(3): 611–615.

26. Rosa BA, Malek L and Qin W. (2009). The development of the pitcher plant Sarracenia purpurea into a potentially valuable recombinant protein production system. Biotechnology and Molecular Biology Reviews 3 (5): 105-110. 27. de Flacourt É. (1658) Histoire de la Grande Isle de Madagascar. 28. Jebb MHP and Cheek M. (1997). A skeletal revision of Nepenthes (Nepenthaceae). Blumea 42:1-106. 29. Clarke CM. Nepenthes of Borneo and Kota Kinabalu. (1997) Natural History Publications. 30. Clarke CM. (2001). Nepenthes of Sumatra & Peninsular Malaysia. Kota Kinabalu. Natural History Publications. 31. Kato M, Hotta M, Tamin R and Itino T. (1993). Inter- and intraspecific variation in prey assemblages and inhabitant communities in Nepenthes pitchers in Sumatra. Tropical Zoology 6:11-25. 32. Ziemer, B. (2010). Exciting conservation news: the Rare Nepenthes Collection project! Carnivorous Plant Newsletter 39(3): 67. 33. Bourke G. (2010). A new conservation initiative: the Rare Nepenthes Collection project. Captive Exotics Newsletter 1(2): 5–6.

Received : September, 2013; Revised : November, 2013; Accepted: December, 2013

Biotech Today, Vol. 4, No. 1, January-June 2014

33