Biochar soil amendment on alleviation of drought and ...

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2016; Usman et al. 2016). ...... compared to the nonsaline irrigation (Usman et al. 2016). ..... Usman ARA, Al-Wabel MI, Abdulaziz AH, Mahmoud WA, El-Naggar.
Biochar soil amendment on alleviation of drought and salt stress in plants: a critical review Shafaqat Ali, Muhammad Rizwan, Muhammad Farooq Qayyum, Yong Sik Ok, Muhammad Ibrahim, Muhammad Riaz, Muhammad Saleem Arif, et al. Environmental Science and Pollution Research ISSN 0944-1344 Volume 24 Number 14 Environ Sci Pollut Res (2017) 24:12700-12712 DOI 10.1007/s11356-017-8904-x

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Author's personal copy Environ Sci Pollut Res (2017) 24:12700–12712 DOI 10.1007/s11356-017-8904-x

REVIEW ARTICLE

Biochar soil amendment on alleviation of drought and salt stress in plants: a critical review Shafaqat Ali 1 & Muhammad Rizwan 1 & Muhammad Farooq Qayyum 2 & Yong Sik Ok 3 & Muhammad Ibrahim 1 & Muhammad Riaz 1 & Muhammad Saleem Arif 1 & Farhan Hafeez 4 & Mohammad I. Al-Wabel 5 & Ahmad Naeem Shahzad 6

Received: 28 March 2016 / Accepted: 20 March 2017 / Published online: 3 April 2017 # Springer-Verlag Berlin Heidelberg 2017

Abstract Drought and salt stress negatively affect soil fertility and plant growth. Application of biochar, carbon-rich material developed from combustion of biomass under no or limited oxygen supply, ameliorates the negative effects of drought and salt stress on plants. The biochar application increased the plant growth, biomass, and yield under either drought and/or salt stress and also increased photosynthesis, nutrient uptake, and modified gas exchange characteristics in drought and salt-stressed plants. Under drought stress, biochar increased the water holding capacity of soil and improved the physical and biological properties of soils. Under salt stress, biochar decreased Na+ uptake, while increased K+ uptake by plants. Biochar-mediated increase in salt tolerance of plants is primarily associated with improvement in soil properties, thus Responsible editor: Hailong Wang * Muhammad Rizwan [email protected]

1

Department of Environmental Sciences and Engineering, Government College University, Allama Iqbal Road, Faisalabad 38000, Pakistan

2

Department of Soil Sciences, Faculty of Agricultural Sciences and Technology, Bahauddin Zakariya University, Multan, Pakistan

3

Korea Biochar Research Centre and Department of Biological Environment, Kangwon National University, Chuncheon 24341, South Korea

4

Department of Environmental Sciences, COMSATS Institute of Information Technology, Abbottabad, Pakistan

5

Soil Sciences Department, College of Food and Agricultural Sciences, King Saud University, P.O. Box 2460, Riyadh 11451, Saudi Arabia

6

Department of Agronomy, Faculty of Agricultural Sciences and Technology, Bahauddin Zakariya University, Multan, Pakistan

increasing plant water status, reduction of Na+ uptake, increasing uptake of minerals, and regulation of stomatal conductance and phytohormones. This review highlights both the potential of biochar in alleviating drought and salt stress in plants and future prospect of the role of biochar under drought and salt stress in plants. Keywords Abiotic stress . Soil reclamation . Soil salinity . Soil remediation . Black carbon . Charcoal . Slow pyrolysis

Introduction The world population is increasing at an alarming rate and is expected to reach 9.6 billion by 2050 (FAO 2009). Additional food required to feed this increasing population is putting pressure on existing natural resources. Agricultural crops are frequently exposed to abiotic stresses such as salinity, drought, and heavy metal stress (Osakabe et al. 2014; Parihar et al. 2015; Rizwan et al. 2016a). Among the abiotic stresses, drought and soil salinity are the most critical threats to agricultural production. At the world level, ∼800 × 106 million ha of land is affected by salt with an annual increase of ∼1–2% (Munns and Tester 2008). Land degradation due to salinity is causing an annual economic loss of USD 27.2 billion in terms of crop loss in irrigated agriculture (Qadir et al. 2014). Loss in revenue is estimated to accelerate to 69%, if no action is taken to prevent the land degradation. In addition, higher emission of carbon (C) from degraded lands further adds to the cost of reclamation. The excess soluble salts have negative effects on the soil physicochemical and biological properties through various ways. Sustainable crop production depends on the interaction between salinity and soil moisture conditions (Maas and Grattan 1999). The major effect of salinity is the decrease in the biomass production leading to lower C inputs,

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thus deteriorating soils (Wong et al. 2009). Drought stress is another key environmental factor responsible for the reduction of growth and yield of plants (Wang et al. 2014a, b; Bodner et al. 2015). In the recent past, drought has severely affected terrestrial agriculture. For example, Xia et al. (2015) reported that drought stress increased Cd uptake in peanuts grown in a Cd-contaminated calcareous soil. Both drought and salt stresses adversely affect plants, including the reduction in leaf water contents, nutrient uptake, photosynthesis, growth, and yield of plants (Gupta and Huang 2014; Noman et al. 2015; Siddiqui et al. 2015). In addition, drought and salt stress cause oxidative stress in plants through the production of reactive oxygen species (ROS) (De Carvalho 2008; Abbasi et al. 2015). Thus, combating drought and salt stress is a challenging task for achieving food security worldwide. Pyrolysis of biomass under limited oxygen supply results in production of carbon-rich material, known as biochar. Applications of biochar have received significant attention for its ability to enhance soil fertility, carbon sequestration, bio-energy production, and immobilization of organic and inorganic pollutants (Fiaz et al. 2014; Ok et al. 2011, 2015; Rajapaksha et al. 2016. Rizwan et al. 2016b; Abbas et al. 2017a). A significant body of knowledge reported that biochar application increased plant growth and biomass and nutrient uptake under drought and salt stress (e.g., Akhtar et al. 2014, 2015a; Haider et al. 2015; Kim et al. 2016). Biochar also improved soil physicochemical properties including soil pH, cation exchange capacity (CEC), soil structure, water holding capacity (WHC), and surface area under abiotic stresses (Chaganti and Crohn 2015; Hammer et al. 2015; Andrenelli et al. 2016; Bamminger et al. 2016; Lim et al. 2016). Biochar application also reduced sodium ion (Na+) uptake and increased potassium (K+) uptake under salt stress (Wu et al. 2014; Drake et al. 2016; Usman et al. 2016). However, a comprehensive review on the beneficial effects of biochar on drought and salt stress in plants is not there in the literature. Herein, we review the biochar application in agricultural production under drought and salt stresses, as much attention has been given for the improvement of soil health to feed the increasing population.

Effects of drought and salt stress on soil properties Drought and salt stress adversely affect soil properties, plant growth, and overall productivity (Ohashi et al. 2014; Rath and Rousk 2015). Drought results in frequent wetting and drying cycles which strongly affect soil microbial activity, soil respiration, fungal properties, and litter decomposition (Geng et al. 2015; Mariotte et al. 2015). However, Ohashi et al. (2014) reported no significant effects of short-term drought stress on the CO2 efflux from a tropical seasonal rainforest soil.

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In general, salt-affected soils are classified as saline, sodic or saline-sodic which is mainly based on their electrical conductivity (EC), sodium adsorption ratio (SAR), and exchangeable sodium percentage (ESP) of the saturated paste extracts (Richards 1954). Among saline soils, saline-sodic soils are highly degraded and least productive which is mainly due to the effect of both salinity and sodicity on soil properties (Rengasamy and Olsson 1991) and if these soils are dispersed then water infiltration and hydraulic conductivityisreducedwhichnegativelyaffectedtheplantgrowth (Suarez et al. 2006). Salinity stress negatively correlates with soil properties such as organic matter and C:N ratio (Morrissey et al. 2014). Soil salinity reduces the microbial activity and biomass and alters the microbial community structure in the soil (Yan et al. 2015). Rath and Rousk (2015) reviewed the effects of salinity on soil microbial communities and C cycling and concluded that the soil respiration is inhibited under short- or long-term salinity stress and is linked with changes in the soil microbial communities and enzyme activities. The effect of salinity on net respiration also depends on the residue properties. The negative effects of salinity are pronounced in the soils containing materials with low decomposability (Hasbullah and Marschner 2014).

Effects of drought and salt stress on plant biomass and yield Drought affects the plant growth and biomass accumulation by inhibiting leaf expansion and stomatal leading to lower photosynthetic rates (Osakabe et al. 2014; Tardieu et al. 2014). It has been widely reported that drought stress negatively affected the plant growth and yield and caused oxidative stress (Basu et al. 2010; Rizwan et al. 2015; Guzman et al. 2016; Anjum et al. 2017). The reduction in plant growth under drought is controlled by a number of processes such as plant hydraulic status, phytohormones, osmotic adjustment, and ROS signaling (Tardieu et al. 2014; Khan et al. 2015). Farooq et al. (2009) extensively reviewed the effects of drought stress on plant growth. It has been well established that salt stress adversely affected the process of seed germination in plants (Parihar et al. 2015). Salt stress negatively affected the plant growth, nutrient uptake, and yield (Azeem et al. 2015; Hussain et al. 2015; Rehman et al. 2016). Similarly, salt stress caused oxidative stress in plant and caused the reduction in antioxidant enzyme activities (Khaliq et al. 2015; Mohamed et al. 2017). Salinity reduces crop growth by affecting multiple processes which are either dependent or independent of salt accumulation in shoots (Roy et al. 2014; Rehman et al. 2016; Mohamed et al. 2017). The independent processes reduce shoot biomass predominately by closing stomata and inhibiting leaf expansion. Depending on the intensity and duration of salt exposure, shoot biomass is further reduced due to premature leaf senescence on the accumulation of salts in leaves to toxic levels. Plant initial responses to salt stress are

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generally the reduction in leaf expansion and partial/full closure of stomata to conserve water resource (Tardieu et al. 2014). These responses are coordinated by an increased accumulation of stress hormones, particularly abscisic acid (ABA). An increased level of ABA in xylem stream is an indication of plant roots facing osmotic stress. Drought and salt stress at reproductive growth stage affect the grain setting and grain filling which reduce grain yields. Reduction in crop yields under stress conditions are associated with the disruptions in carbon metabolism and transport (Muller et al. 2011).

Production and physicochemical characteristics of biochar amendments Biochar is produced by thermochemical combustion of organic materials under limited supply of oxygen. Traditionally, charcoal was prepared in earth above-ground piles, while combusting large wood stocks (Mohan et al. 2006). Feedstock type significantly affects the properties of biochar being prepared. The use of biochar as a soil amendment is dated back to pre-Columbian Indios who used to add charcoal in soils repeatedly to maintain the fertility, resulting in a nutrient-rich Terra Preta do Indio (Terra Preta) soils (Glaser et al. 2002). The use of biochar is being considered as a winwin practice for achieving multiple benefits of sustainable agriculture. The tremendous increase in the number of publications using a variety of biochars in the last decade shows a high interest and scope of biochar. Woolf et al. (2010) presented an overview of the sustainable biochar concept. Rotating kilns, vertical silo-type reactors, gasification, hydrothermal carbonization, and pyrolysis (fast and slow) are common techniques used for biochar production. The detailed methodology and description of each technique are not in the scope of this review. Biochars are characterized with a high concentration of total organic carbon (30 to 70%) depending on the pyrolysis conditions (temperature, aeration, and time), high mineral contents (Na, K, Mg, Fe, etc.), high pH, high EC, and a low concentration of ash and volatile matter (Jindo et al. 2014; Qayyum et al. 2015). However, the feedstock type significantly affects the biochar properties (Ronsse et al. 2013). The sophisticated techniques of characterization include the quantification and identification of surface functional groups, aromatic compounds, polycyclinc aromatic hydrocarbon, active surface area, and scanning electron microscopy (Hale et al. 2012; Harris et al. 2013). Thus, biochars should be carefully analyzed prior to their utilization (Kuppusamy et al. 2016).

Functional properties of biochar Adsorption capacity of biochar is an important property of biochar amendments which is due to the presence of surface

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functional groups produced and/or modified during the pyrolysis depending on the feedstock and temperature. The pyrolysis of organic feedstock loses easily degradable compounds such as cellulose and lignin at 300 °C. With increasing temperature, the aromatic compounds are condensed and surface area is increased (Chun et al. 2004, Ahmad et al. 2012, Inyang et al. 2016). Zhang and Luo (2014) investigated the surface functional properties of biochar derived from the leaves of Eucalyptus plant (EBC) and anaerobically digested garden wastes (ADB) through FTIR, Boehm titrations, and scanning electron microscopy. The total amount of functional groups was higher in EBC as compared to that in ADB; however, the ADB contained higher carboxyl, phenolic, and basic functional groups, but lesser lactonic groups than in the EBC. Zhang et al. (2014) investigated the functional properties of four biochars differing in the feedstock (wood, bamboo, rice husk, and rice husk ash) and compared with biochars derived using a variety of feedstock published previously. Their results show more carboxyl, lactones, and phenolic groups in wood biochar as compared to all other biochars. Similarly, Qayyum et al. (2012) reported high aromaticity in wood biochar (charcoal) as compared to the hydrothermal carbonization coal (HTC) and low-temperature conversion coal (LTC) derived using sewage sludge. The FTIR of three biochars showed the higher amounts of decomposable organic groups in HTC as compared to charcoal and LTC. The functional groups of pine-needles-derived biochar as determined through Boehm titrations showed the removal of acidic functional groups such as carboxylic, phenolic, and lactones, with the accumulation of basic functional groups such as ketones, pyrones, and chrome (Ahmad et al. 2013). The presence of these and other functional groups in biochar make them a suitable and economical choice for the removal of contaminants and pollutants in soils and water through sorption (Ahmad et al. 2014; Rajapaksha et al. 2016).

Biochar and drought stress Effects of biochar on plant growth, photosynthetic rate, and biomass under drought stress The beneficial effects of the biochar application under limited water conditions have been widely reported (e.g., Artiola et al. 2012; Akhtar et al. 2014; Batool et al. 2015; Paneque et al. 2016). The biochar application increased growth and biomass of drought-stressed plants (Fig. 1, Table 1). For example, biochar increased the plant height and leaf area of okra (Batool et al. 2015) and maize (Haider et al. 2015) under drought stress. Similarly, application of biochar increased biomass of fieldgrown wheat under semiarid Mediterranean conditions (Olmo et al. 2014). Biochar also increased fruit yield and quality, total soluble solids, and titratable acidity of drought-stressed tomato

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Fig. 1 Possible effects of biochar on drought and salt stress in plants at both soil and plant levels. Bold biochar effects related to only salt stress

Biochar effects under drought and salt stress

Soil

Sorption of Na on biochar

plants (Akhtar et al. 2014). Mulcahy et al. (2013) reported that biochar application increased tomato seedling resistance to wilting in sandy soil. In addition, the biochar application in silt clay soil increased tomato growth as compared to the unamended control (Vaccari et al. 2015). Githinji (2014) reported that the leaf quality rate of tomato increased with biochar application in sandy loam soil as compared to the unamended control. Application of 1% straw gasification biochar increased the shoot and root growth of barley grown in the coarse sandy subsoil under water. However, there was no effect of gasification biochar on barley growth under water stress in sandy loam soil (Hansen et al. 2016). Studies have reported that the biochar application improved the photosynthesis in drought-stressed plants (Akhtar et al. 2014; Lyu et al. 2016; Paneque et al. 2016; Xiao et al. 2016). Akhtar et al. (2014) found that biochar significantly improved the chlorophyll contents, stomatal conductance (Gs), photosynthetic rate (Pn), water use efficiency (WUE), and relative water contents (RWC), and increased stomatal density of drought-stressed tomato leaves. Biochar application increased the leaf RWC, transpiration rate, and osmotic potential of drought-stressed maize as compared to the control (Haider et al. 2015). In addition, biochar increased the WUE of maize in sandy soil (Uzoma et al. 2011). Similarly, biochar increased the WUE of Chenopodium quinoa wild under drought stress (Kammann et al. 2011). In another study, biochar (Lantana camara, 450 °C) increased the photosynthesis, the WUE, and Gs of okra (Abelmoschus esculentus L. Moench) under drought stress as compared to the control (Batool et al. 2015). Similarly, biochar application increased the Pn and Gs of grape leaves as compared to the control (Baronti et al. 2014). The biochar-mediated improvements in gas exchange characteristics, WUE, RWC, and Pn indicate improvement in the water status of plants under drought stress. However, biochar application at a rate of 1.0 and 2.0% did not affect the chlorophyll contents and gas exchange traits in drought-stressed milk thistle seedlings grown in fine sandy

Plant Water holding capacity

Mineral nutrients

Aggregate stability

Photosynthesis

Soil biological activity

Water use efficiency

Aeration

Crop productivity

Soil bulk density

Oxidative stress

Potassium uptake

Sodium uptake

loam soil (Afshar et al. 2016). This showed that biochar response under drought stress may vary with soil and biochar type and plant species. Artiola et al. (2012) studied the effect of pine forest waste biochar on the growth of romaine lettuce (Lactuca sativa L.) and Bermuda grass (Cynodon dactylon) in alkaline loamy sand soil under greenhouse conditions. The results showed that the growth of lettuce initially decreased in the first trial with a higher rate of biochar (4%), while increased in the second and third trials with no additional biochar application. In contrast, the biomass of drought-stressed Bermuda grass increased to 2 and 4% with the biochar application as compared to the control. They suggested that the decrease in the lettuce growth in the first trial might be because of increasing soil pH with biochar application, and thus a period of biochar soil adjustment might be required for the higher lettuce biomass production, and warm season grasses may benefit with pine forest waste biochar soil application under drought stress. The biochar applied in the vineyard field increased the vine yield especially in the years receiving lowest rainfall, whereas no effect was observed on the grape quality parameters such as brisk, total acidity, and anthocyanins (Genesio et al. 2015). Afshar et al. (2016) have shown that biochar soil usage (0, 1.0, and 2.0% w/w) has not significantly affected the leaf, plant and stem weight, leaf area, and plant height of milk thistle (Silybum marianum L. Gaertn) under moderate (60% of control) and severe (40% of control) drought stress compared to the control (50% of field capacity). Studies have shown that biochar may alleviate water stress in plants when applied with microorganisms (Mickan et al. 2016; Liu et al. 2017). Inoculation of biochar with Bradyrhizobium sp. increased the growth, biomass, nitrogen (N), and phosphorus (P) uptake and nodulation in droughtstressed lupin (Lupinus angustifolius L.) seedlings compared to the only microbial inoculation (Egamberdieva et al. 2017). In another study, biochar (birch wood, 500 °C) inoculation with Rhizophagus irregularis decreased the potato leaf area,

Author's personal copy Kammann et al. 2011

Haider et al. 2015

Batool et al. 2015

Artiola et al. 2012

Leaf dry weights significantly increased as compared to the control Okra Increased leaf area, plant height, photosynthesis, Gs, and WUE Maize Increased stem and leaf dry mass, RWC, and photosynthesis Chenopodium quinoa Willd Increased plant growth and WUE but higher BC rate did not improved the plant growth as compared to the lower rate Bermuda grass

Tomato

Akhtar et al. 2014

Increased fruit yield, Gs, Pn, RWC and WUE of leaves Seedling resistance increased against wilting

0, 100, and 200 t ha−1

0, 1, and 3%

Biomass of Lantana camara, 450 °C Wood-chip sievings at 550–600 °C Peanut hull

0, 1.5, and 3%

0, 2, and 4% Pine forest waste, 450–500 °C

0, 15, and 30%

Sandy loam, pot 0 and 5% W/W

Rice husk + shell of cotton seed, 400 °C Wood pellets

Full irrigation, deficit and partial root zone drying Sandy loam 35-Day-old plants were transplanted and stopped irrigation after 24 days of transplanting Loamy sand, pots After 2 months of growth, irrigation stopped for 1 month Sandy loam, pot After 30 days, 100 and 60% of FC for 2 weeks Sandy soil, pot After 28 days, 60 and 25–30% of WHC until 66th days of growth Sandy soil, pot After 9 days, 60 and 20% of WHC for more 50 days

Tomato

Reference Soil type

Drought stress

Plant species

Effects

Mulcahy et al. 2013

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Feedstock and pyrolysis conditions Rate of application

Table 1 Beneficial effects of biochar in drought-stressed plants. WHC water holding capacity, Gs stomatal conductance, Pn photosynthetic rate, RWC relative water content, WUE water use efficiency, FC field capacity

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WUE, N, and P while did not affect the biomass of roots and soil pH under limited root zone water compared to the respective treatments without biochar application (Liu et al. 2017). However, wood-derived biochar (30 Mg ha−1) soil amendment had no significant effect on soil biota groups (protozoa, nematodes, bacteria, fungi, and arthropods) under limited irrigation (Pressler et al. 2017). This showed that application of biochar with other amendments such as microbial inoculation might be helpful in reducing drought stress in plants depending upon biochar type along with other factors. Effects of biochar on soil physicochemical and biological properties Several studies have shown that biochar improved soil physical properties under drought stress (Baronti et al. 2014; Bruun et al. 2014). The pine forest waste biochar application (2 and 4% for 4 months) decreased the soil bulk density (BD) and decreased the soil microbial activity (Artiola et al. 2012). Similarly, Bruun et al. (2014) also reported that biochar application in coarse sandy soil decreased the BD of the soil. Abel et al. (2013) showed that biochar application in sandy soil decreased the soil BD and increased the total pore space and water retention at permanent wilting point. In an incubation study, biochar application decreased BD of sandy soil (Basso et al. 2013). The equilibration of corn residue biochar in a sandy loam soil for 30 days decreased the BD and increased WHC of the soil (Igalavithana et al. 2017). The biochar-mediated decrease in the BD and an increase in the soil water contents have been observed in a wide variety of soils differing in soil texture (Herath et al. 2013; Jeffery et al. 2015; Igalavithana et al. 2017). However, research on the effects of biochar on the physical properties of clayey soils is limited (Castellini et al. 2015). Baiamonte et al. (2015) reported that biochar application increased the aggregate stability of sandy-clay soil. The increase in the aggregate stability might be effective in enhancing soil water retention, especially under the limited supply of water. However, studies that are more detailed are needed to evaluate the effect of biochar on soil aggregate stability under crop cultivation. In general, biochar application improved the soil physical properties under limited water supply and will be helpful for plant growth under semiarid conditions. However, further investigations are needed with regard to the biochar application under real drought stress conditions. In addition, biochar aging may affect the soil properties, and studies are needed to evaluate the effect of soil properties under drought stress (Arthur et al. 2015). In addition, soil water retention may vary with biochar sources and rate of application (Brantley et al. 2015). Conte et al. (2014) reported that water retention in biochar varied with the biochar preparation

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methods. Further studies by using different biochars, different pyrolysis conditions, and rate of application might be helpful to better understand the effect of biochar on the soil WHC under drought stress (Lee et al. 2015). The addition of biochar increases the WHC of the soil, which is a key factor in enhancing plant growth and yield under drought (Artiola et al. 2012; Pereira et al. 2012; Akhtar et al. 2014; Bruun et al. 2014; Lu et al., 2015a, b; Agegnehu et al. 2016; Foster et al. 2016). An increase in the WHC of soil under drought stress might be because of higher CEC and porous structure of biochar (Artiola et al. 2012). Studies reported that biochar application increased the soil CEC as compared (Cornelissen et al. 2013). Artiola et al. (2012) reported that the application of pine forest waste biochar in the soil retained water in the soil, but a significant portion of biochar pores still remained empty under laboratory conditions. However, there might be the difference in the WHC of biochar under field conditions, which need to be explored in the near future. The biochar applied in the vineyard field increased the soil water content measured at different time periods (Baronti et al. 2014). Biochar application improved the soil moisture contents without affecting the maize yield in a 4-year field study (Haider et al. 2017). Ajayi et al. (2016) observed that biochar application in two types of soils (fine-sand or sandy loamy silt) increased the saturated hydraulic conductivity of sandy loamy silt under 4 cycles of wetting and drying during 300 days. Ajayi and Horn (2016) compared the potential of clay and biochar in improving water retention and mechanical resilience of sandy soil. The results showed that soil water retention capacity was higher with Na-bentonite at more negative matric potentials, while biochar was more effective in increasing soil water retention capacity at saturation which might be due to the increase in soil porosity (Ajayi and Horn 2016). The application of biochar in the sandy loam soil increased the WHC of the soil under rice cultivation (de Melo Carvalho et al. 2014). In another study, it increased the WHC of silty sand under maize cultivation in pots (Haider et al. 2015). The field application of biochar in vertisol increased the ability of the soil to retain water and wheat growth under semiarid Mediterranean conditions (Olmo et al. 2014). Andrenelli et al. (2016) reported that application of biochar in the field increased the macroporosity of silty clay loam soil. These studies showed that biochar might be effective in enhancing the WHC of soils, and most of the studies were conducted on sandy soils. However, more studies are required to explore the role of biochar in increasing the WHC of soil varying in texture and environmental conditions.

Biochar and salt stress Reversal of salt-affected soils requires long-term management; therefore, interim/short-term management strategies could be useful options to increase farm income (Qadir et al. 2014).

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Biochar is known to increase plant tolerance to salt stress (Fig. 1). The beneficial effects of biochar on plants under salt stress have been reviewed and summarized in Table 2. Improvements in soil physicochemical and biological properties The application of biochar has been shown to be effective in reducing salinity stress by improving soil physicochemical and biological properties directly related to Na removal such as Na leaching, Na adsorption ratio, and EC (e.g., Chaganti et al. 2015; Diacono and Montemurro, 2015; Oo et al. 2015; Drake et al. 2016; Sun et al. 2016). Biochar could improve the soil physicochemical and biological properties under conditions of abiotic stresses (Rizwan et al. 2016b). Lu et al. (2015a, b) reported that biochar poultry-manure compost (BPC) with pyroligneous solution (PS) in the saline soil increased microbial biomass carbon and the activities of urease, invertase, and phosphatase in bulk soils and rhizosphere soils under maize cultivation. Similarly, Bhaduri et al. (2016) concluded that the effects of biochar on soil enzyme activities in saline soil vary with biochar rate applied, incubation time, and soil enzyme types. Studies have also shown that the application of organic amendments improved the physicochemical properties of saline soil (Wang et al. 2014a, b). However, little data is available on the effect of biochar on the saline soil properties (Thomas et al. 2013; Wu et al. 2014; Almaroai et al. 2014). The biochar application in salt-stressed soil, 30 g m−2, did not affect the soil pH, but increased the soil EC as compared to the control (Thomas et al. 2013). Similarly, furfural biochar in saline soil decreased pH, while increasing the SOC and CEC and available P in the soil (Wu et al. 2014). When applied in saline soils, composted biochar increased the soil organic matter content and CEC and decreased the exchangeable Na and soil pH (Luo et al. 2017). These studies showed that biochar addition in saline soils could improve the plant growth by improving the soil biological activity and physicochemical properties. Regulation of stomatal conductance and phytohormones A notable number of studies reported that biochar decreased salt stress in plants by lower production of phytohormones (Akhtar et al. 2015a; Lashari et al. 2015). Combined BPC and PS applications in the saline soil under field conditions decreased the maize leaf sap ABA (Lashari et al. 2015). In another study, biochar decreased ABA concentrations in leaf and xylem sap of salt-stressed potato (Akhtar et al. 2015a). Biochar in combination with endophytic bacteria also decreased the xylem ABA contents in wheat and maize under saline conditions as compared to the unamended controls (Akhtar et al. 2015b, 2015c).

Sandy loam, pot

Sandy loam, pot

0 and 5%

0 and 5%

A mixture of hardwood (80%) and softwood (20%), 500 °C

Residual effect of BC hardwood (80%) and softwood (20%), 500 °C

0, 1.37%

0, 4, and 8%

Conocarpus wood waste, 400 °C

Maize

Wheat

Wheat

Maize

Potato

Lashari et al. 2013

Akhtar et al. 2015c

Akhtar et al. 2015b

Akhtar et al. 2015a

Reference

Increased shoot and root dry weights; decreased Na and increased K uptake by plants Increased plant height, fresh and dry weight, fruit length and fruit fresh and dry weight, and total yield

Increased maize biomass and decreased Na uptake and activities of antioxidant enzymes

Usman et al. 2016

Hammer et al., 2015

Kim et al. 2016

Increased plant height, plant density, Lashari et al. 2015 root length, leaf area index, photosynthesis, and grain yield

Increased tuber yield, shoot and root growth, Gs, Pn, and WUE; decreased [Na+]/[K+] ratio in the xylem sap Increased leaf area, root volume, growth and nutrient uptake by plants and decreased xylem Na+ concentrations Increased growth and yield of wheat; increased Gs, Pn, stomatal density, and chlorophyll contents while decreased [Na+]/[K+] ratio in the xylem sap Increased grain yield and decreased Na+ in the soil

Plant species Effects

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Pellets of coniferous wood, 500 °C

5.36 g Na+ kg−1 of soil

5.62 ± 0.22 g Na+ kg−1 of soil

Residual effect of saline irrigation (0, 25 and 50 mM NaCl solution)

Saline irrigation (0 and 25 mM NaCl solution)

Saline irrigation (0, 25 and 50 mM NaCl solution)

Salt stress

Exchangeable Na = 8.5 Maize cmolc kg−1 and irrigated with 0.1% NaCl after 1 week of transplantation for 6 weeks at 3 day interval Albic luvisol 0.5 M NaCl solution for 8 Lettuce days to reach 4 g NaCl kg−1 soil Sandy soil, greenhouse Saline water with an average Tomato EC of 3.6 dS m−1

0, 0.15 t ha−1 pyroligneous Aqui-entisol, field Wheat straw at 350–550 °C, solution spray on soil then mixed with poultry manure then 0, 12 t ha−1 BPC in a ratio of 1:3 (PM/BC), v/v and composted for 6 weeks (called PBC) Wheat straw at 350–550 °C, then 0, 0.15 t ha−1 pyroligneous Aqui-entisol, field mixed with poultry manure in a solution spray on soil ratio of 1:3 (PM/BC), v/v and then 0, 12 t ha−1 BPC composted for 6 weeks (called PBC) Rice hull, 500 °C 0, 1, 2, and 5% Reclaimed tidal land soil, silt loam

Sandy loam, pot

0 and 5%

A mixture of hardwood (80%) and softwood (20%), 500 °C

Soil type

Rate of application

Beneficial effects of biochar in salt-stressed plants

Feedstock and pyrolysis conditions

Table 2

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The biochar-mediated improvement in plant growth under salt stress is often correlated with an increase in stomatal conductance. Many recent studies have shown that biochar application to saline soils improved the stomatal density and stomatal conductance in wheat, tomato, and herbaceous plants (Thomas et al. 2013; Akhtar et al. 2015b, 2015c). Improved soil properties, increased soil moisture, and Na binding in biochar-amended soils decrease the root sensitivity to osmotic stress (Akhtar et al. 2015c). Roots then decrease the production of ABA, and in response, stomatal conductance and leaf growth are increased. Reduction in oxidative stress Salinity is known to cause oxidative stress in plants by excessive production of reactive oxygen species (Parihar et al. 2015; Fazal and Bano 2016; Farhangi-Abriz and Torabian 2017). Organic amendments have been shown to alleviate salt stress in plants by regulating the synthesis of antioxidant enzymes in plants (Tartoura et al. 2014). However, a few studies reported the effects of biochar on the oxidative stress and antioxidant enzyme activities in plants grown in saline soils. For example, the biochar application decreased the ascorbate peroxidase (APX) and glutathione reductase (GR) activities in maize under salt stress as compared to the control (Kim et al. 2016). Lashari et al. (2015) reported that poultry manure compost plus diluted pyroligneous solution application decreased the malondialdehyde (MDA) contents in maize leaf sap. It has recently been reported that biochar reduced antioxidant enzyme activities and oxidative stress in bean seedlings under salt stress compared to the control (Farhangi-Abriz and Torabian 2017). These studies suggested that biochar could improve plant growth and biomass under salt stress by reducing oxidative stress and enhancing the activities of antioxidant enzymes. Effects on plant growth, biomass and photosynthesis Application of biochar in saline soils is reported to improve plant growth, biomass, and photosynthesis. For example, hardwood- and softwood-derived biochar increased shoot biomass, root length, tuber yield, and Pn in salt-stressed potato (Akhtar et al. 2015a). Similarly, rice hull biochar increased maize growth and biomass grown in reclaimed tidal land soils containing higher concentrations of exchangeable sodium as well as higher concentrations of soluble salts (Kim et al. 2016). In another study, biochar application increased tomato growth and biomass under saline, 3.6 dS m−1, irrigation as compared to the nonsaline, 0.9 dS m−1, irrigation (Usman et al. 2016). Thomas et al. (2013) studied the effect of biochar (Fagus grandifolia sawdust pyrolyzed, 378 °C at 50 t ha−1) on the growth and biomass of two herbaceous, Abutilon theophrasti and Prunella vulgaris, under salt stress, increasing

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the biomass of the both plant species under salt stress as compared to the untreated control. However, biochar did not significantly affect the WUE, photosynthetic carbon gains, and chlorophyll fluorescence (Fv/Fm) in both the species under salt stress. Overall, the biochar response under salt stress varied with plant species. The composted biochar application could also improve plant growth and biomass under saline conditions. For example, Lashari et al. (2013) conducted a field experiments and reported that the biochar application for 6 weeks called as BPC, along with PS spray in the saline soil, increased wheat grain yield as compared to the control. In another 2-year field study, similar BPC and PS treatments in the saline soil increased plant height, plant density, root length, leaf area index, photosynthetic pigments, and grain yield of maize in both years (Lashari et al. 2015). Similarly, composted biochar application increased the growth and biomass of two halophyte species under saline conditions compared to the control (Luo et al. 2017). Biochar application along with suitable microbial inoculants is reported to further improve the plant growth and biomass under saline conditions as compared to the control and biochar only treatments (Nadeem et al. 2013; Fazal and Bano 2016). For example, exogenous application of plant growthpromoting rhizobacteria (PGPR) has been shown to increase the growth and biomass of plants under saline conditions (Nadeem et al. 2013). Akhtar et al. (2015b, 2015c) studied the effect of biochar and endophytic bacteria on the growth and biomass of wheat and maize crops under saline conditions. The results showed that biochar application increased leaf area, shoot and root biomass, root volume, and Pn in both crops, and the effect increased with bacterial inoculation as compared to the only biochar treatment. In another study, biochar together with arbuscular mycorrhizal (AM) fungi increased salt-stressed lettuce biomass as compared to the treatments alone (Hammer et al. 2015). These studies have shown that biochar ameliorating effect could be further enhanced with the application of PGPR and/or symbiotic microorganisms in the growth medium. However, the beneficial effects of different types of biochars in combination with different microbes on the growth of plants under saline conditions need further study. Reduction in Na ion toxicity in plants The application of biochar significantly decreased Na+ concentrations in the xylem sap of potato, while increasing K+ concentrations and Na+/K+ ratio in the xylem sap as compared to the control (Lashari et al. 2015; Akhtar et al. 2015a). Similarly, biochar decreased Na uptake by lettuce under salt stress (Hammer et al. 2015). In another study, it decreased Na uptake and increased K uptake in salt-stressed maize (Kim et al. 2016). In a field study, biochar increased maize leaf sap K, P, and N and decreased Na as well as Na/K ratio

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(Lashari et al. 2015). The biochar application in a Cdcontaminated saline soil decreased Na and increased K concentrations in wheat seedlings (Abbas et al. 2017b). The beneficial effect of biochar on ion-homeostasis under saline stress could be further enhanced by co-application of biochar with endophytic bacteria (Akhtar et al. 2015b, 2015c). These studies showed that biochar might be effective in reducing Na+ uptake by plants grown in saline soils.

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& &

Increase in mineral nutrient uptake & Studies have shown that biochar application in saline soils may enhance plant tolerance to salt stress by enhancing the uptake and accumulation of mineral nutrients in plants. For example, the biochar and AM application increased the P and Mn concentrations in lettuce plants under salt stress (Hammer et al. 2015). Biochar application increased the P concentration in maize tissues under salt stress in a dose-dependent manner (Kim et al. 2016). In another study, biochar increased P, K, Fe, Mn, Zn, and Cu in tomato plants with saline irrigation as compared to the nonsaline irrigation (Usman et al. 2016). However, the combined application of wheat straw-derived biochar and P increased the phosphate precipitation/sorption in the saline sodic soil and decreased P concentrations in plants (Xu et al. 2016). These studies showed that biochar application may increase the mineral uptake by plants under saline conditions. However, further detailed studies are needed to evaluate the mechanisms of biochar-mediated mineral uptake by plants under saline conditions both at the soil and plant levels.

Conclusion and future perspectives Crop growth and yield are severely decreased by drought and salt stress. Studies reported above showed that biochar application increased the plant growth and biomass under drought and salt stress. Biochar soil usage increased the photosynthesis, nutrient uptake, and modified gas exchange characteristics in plants. Biochar decreased Na+ uptake, while increased K+ uptake in salt-stressed plants. The biochar-mediated enhancement in salt tolerance of plants is mainly associated with a reduction of Na+ uptake, accumulation of minerals, and regulation of stomatal conductance and phytohormones. Overall, this review could contribute to a better understanding of the biochar-mediated tolerance mechanisms in plants under either salt or drought stress. However, more focused research is needed to explore the mechanisms of both soil and plant levels including the following: &

The effect of different types of biochars in more species under diverse environmental conditions including drought and salt stress

&

More studies are required to evaluate the role of biochar under both drought and salt stress conditions. The abovementioned studies showed that biochar application along with microbes could further enhance the plant tolerance against salt and drought stress. However, detailed and time-course studies are required to determine the longterm effectiveness of biochar + microbes on the growth and Na uptake by plants and to separate the effects of biochar on different stages of microbial life cycles under prevailing conditions of limited water and saline stress. Different pilot scale studies are needed for the development of models for the better recommendation of biochar rate based on soil, plant, and environmental conditions. The economic feasibility of different feedstock for the biochar preparation should also be investigated.

Acknowledgments The financial support from Government College, University Faisalabad, Pakistan, is gratefully acknowledged. Yong Sik Ok’s work was supported by the National Research Foundation of Korea (NRF) grant funded by the Korea government (MSIP) (NRF2015R1A2A2A11001432, Contribution: 80%).

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