Acclimation and Tolerance Strategies of Rice under Drought Stress

Rice Science, 2015, 22(4): 147−161  Copyright © 2015, China National Rice Research Institute Hosting by Elsevier B.V. All rights reserved DOI: 10.101...
0 downloads 1 Views 822KB Size
Rice Science, 2015, 22(4): 147−161 

Copyright © 2015, China National Rice Research Institute Hosting by Elsevier B.V. All rights reserved DOI: 10.1016/S1672-6308(14)60289-4 

Acclimation and Tolerance Strategies of Rice under Drought Stress Veena PANDEY, Alok SHUKLA (Department of Plant Physiology, College of Basic Sciences and Humanities, Govind Ballabh Pant University of Agriculture & Technology, Pantnagar 263145, Uttarakhand, India)

Abstract: Rice (Oryza sativa L.) is an important food crop and requires larger amount of water throughout its life cycle as compared to other crops. Hence, water related stress cause severe threat to rice production. Drought is a major challenge limiting rice production. It affects rice at morphological (reduced germination, plant height, plant biomass, number of tillers, various root and leaf traits), physiological (reduced photosynthesis, transpiration, stomatal conductance, water use efficiency, relative water content, chlorophyll content, photosystem II activity, membrane stability, carbon isotope discrimination and abscisic acid content), biochemical (accumulation of osmoprotectant like proline, sugars, polyamines and antioxidants) and molecular (altered expression of genes which encode transcription factors and defence related proteins) levels and thereby affects its yield. To facilitate the selection or development of drought tolerant rice varieties, a thorough understanding of the various mechanisms that govern the yield of rice under water stress condition is a prerequisite. Thus, this review is focused mainly on recent information about the effects of drought on rice, rice responses as well as adaptation mechanisms to drought stress. Key words: rice; water; drought stress; yield attribute; morphological characteristic; physiological characteristic; biochemical characteristic; molecular level

Water is an important factor in agricultural and food production yet it is a highly limited resource (Wang et al, 2012). Water deficit stress causes extensive loss to agricultural production worldwide, thus being a severe threat to sustainable agriculture. Feeding continuously increasing population with depleting water supply requires crop varieties that are highly adapted to dry environments (Foley et al, 2011). Rice plays a major role as a staple food, supporting more than three billion people and comprising 50% to 80% of their daily calorie intake (Khush, 2005). Drought stress severely impairs its production. Worldwide, drought affects approximately 23 million hectares of rainfed rice (Serraj et al, 2011). Climate variability severely influences the water resources, and the frequencies of droughts and floods are likely to increase in future. Crop yield depends on specific climate conditions and is highly affected by climate variations. Global rate of change in rice yield is shown in Fig. 1. The overall rice yield variability due to climate variability over the last three decades was estimated by Ray et al (2015), and it was concluded Received: 4 February 2015; Accepted: 7 April 2015 Corresponding author: Veena PANDEY ([email protected])

that approximately 53% of rice harvesting regions experiences the influence of climate variability on yield at the rate of about 0.1 t/hm2 per year and approximately 32% of rice yield variability is explained by year-toyear global climate variability (Fig. 2). With diminishing water supplies for agriculture worldwide, the needs to improve drought adaptation of rice and to screen resistant varieties are becoming increasingly important. The unpredictability of drought patterns and the complexity of the response mechanism involved have made it difficult to characterize component traits required for improved performance, thus limiting crop improvement to enhance drought resistance (Serraj et al, 2009). Drought tolerance is a complex trait, which is a combined function of various morphological, biochemical and molecular characters. The mechanisms associated with water-stress tolerance and the systems that regulate plant adaptation to water stress through a sophisticated regulatory network in rice have been extensively studied. In order to achieve a full understanding of drought-response mechanism in rice and to produce rice with improved drought tolerance, there are needs to combine the data derived from different studies and to put a figure on how various traits which affect the rice productivity respond

148

Rice Science, Vol. 22, No. 4, 2015

Fig. 1. Global map showing percentage rate of change in rice yield (Ray et al, 2013). Red areas show where yields are declining whereas the green areas show where rates of yield increase.

Fig. 2. Global rice yield variability due to climate variability over the last three decades (Ray et al, 2015).

to water deficit. Thus, this review describes some aspects of drought induced effect on morphological, physiological, biochemical, molecular, yield and its associated traits as well as acclimation and tolerant mechanism of rice to drought stress, and a model have been proposed based on these responses (Fig. 3).

Effects of drought on morphological characteristics Plant experiences drought stress either when the water supply to roots becomes difficult or when the transpiration rate becomes very high. It severely impairs growth, development and ultimately the production of rice. When water stress occurs, plants react by slowing down or stopping their growth. This is a normal plant reaction to lack of water, and it acts

as a survival technique (Zhu, 2002). Plant growth and development reduces as a consequence of poor root development, with reduced leaf-surface traits (form, shape, composition of cuticular wax, leaf pubescence and leaf color), which affect the radiation load on the leaf canopy, delay in or reduced rate of normal plant senescence as it approaches maturity, and inhibition of stem reserves (Blum, 2011). An increasing number of studies witnesses early morphological changes in rice upon exposure to drought. Drought stress induces reduction in plant growth and development of rice (Tripathy et al, 2000; Manikavelu et al, 2006). Due to the reduction in turgor pressure under stress, cell growth is severely impaired (Taiz and Zeiger, 2006). Drought affects both elongation as well as expansion growth (Shao et al, 2008), and inhibits cell enlargement more than cell

Veena PANDEY, et al. Acclimation and Tolerance Strategies of Rice under Drought Stress

149

Drought stress in rice

Morphological changes: Reduction in germination, plant height, elongation and expansion growth, plant biomass, No. of tillers, leaf number and size, increased leaf rolling

Molecular changes: Altered expression of genes which encode defence related proteins, protein kinases, transcription factors

Biochemical changes: Accumulation of osmoprotectant like proline and sugars, polyamines, antioxidants

Physiological changes: Reduced chlorophyll content, photosystem II activity, photosynthesis, transpiration, stomatal conductance, WUE, RWC, membrane stability, carbon isotope discrimination, ABA content

Yield attribute: Impaired assimilate translocation, increased spikelet sterility, reduced rate of grain filling, grain size, weight and yield

Fig. 3. Drought induced various responses in rice which ultimately affect yield. WUE, Water use efficiency; RWC, Relative water content; ABA, Abscisic acid.

division (Jaleel et al, 2009). It impairs the germination of rice seedlings (Jiang and Lafitte, 2007; Swain et al, 2014) and reduces number of tillers (Mostajeran and Rahimi-Eichi, 2009; Ashfaq et al, 2012; Bunnag and Pongthai, 2013) and plant height (Sarvestani et al, 2008; Ashfaq et al, 2012; Bunnag and Pongthai, 2013; Sokoto and Muhammad, 2014). A common adverse effect is the reduction in biomass production (Farooq et al, 2009a, 2010). Many studies indicate significant decrease in fresh and dry weights of shoots (Centritto et al, 2009; Mostajeran and Rahimi-Eichi, 2009) and roots (Ji et al, 2012) under drought. Reduced fresh shoot and root weights as well as their lengths ultimately reduce the photosynthetic rate of physiology and biochemical processes of rice (Usman et al, 2013). Effects of drought on leaf traits The importance of flag leaf in grain filling is well recognized. For grain filling to occur under drought, either a relatively uncompromised or a favourably

reprogrammed function of flag leaf is required to maintain synthesis and transport of photoassimilates. Thus, various traits of flag leaf have been proposed for selecting drought tolerant plant, i.e. higher flag leaf area, relative dry weight, excised leaf weight loss, residual transpiration, leaf glaucousness, canopy temperature depression, chlorophyll content, late senescence and higher carbon isotope discrimination (CID). There is positive correlation between these flag leaf traits and yield under drought (Biswal and Kohli, 2013). Leaf rolling is one of the acclimation responses of rice and is used as a criterion for scoring drought tolerance. Leaf rolling is hydronasty that leads to reduced light interception, transpiration and leaf dehydration (Kadioglu and Terzi, 2007). It may help in maintaining internal plant water status (Turner et al, 1986; Abd Allah, 2009; Gana, 2011; Ha, 2014). If cell turgor is maintained under drought stress, it will result in delayed leaf rolling. However, increased leaf rolling under severe stress has the advantage of preventing

150

water loss and radiation damage. Variation in leaf rolling among genotypes has a genetic basis, and QTLs associated with leaf rolling have been reported in rice (Subashri et al, 2009; Salunkhe et al, 2011). Thus, leaf rolling is an adaptive response to water deficit in rice, and leaf angle is a character usually associated with plasticity in leaf rolling when internal water deficit occurs (Chutia and Borah, 2012). Various other leaf traits are also affected by water deficit, which include reduction in number of leaves per plant (Farooq et al, 2010; Cerqueira et al, 2013; Singh et al, 2013; Sokoto and Muhammad, 2014) leaf area and leaf area index (Kumar S et al, 2014). The reduction might be due to rapid decline in cell division and leaf elongation under drought. So, leaf characters comprising of number of leaves, leaf area, leaf angle and plasticity in leaf rolling and unrolling can be used as selection criteria in selecting drought resistant rice varieties. Effects of drought on root traits Root traits have been claimed to be critical for increasing yield under water stress. The structure and development of rice root system largely determines crop function under drought. Under mild water deficit, the root growth usually maintains while shoot growth is inhibited. This is because of the facts that, adjustment like, re-establishment of water potential gradient through osmotic alteration and increase in loosening ability of the cell wall, permit roots to resume growth under low water potential. In contrast, there is no such regulation in leaves, leading to marked growth inhibition (Hsiao and Xu, 2000). Root dry mass and length are good predictor of rice yield under drought (Fageria and Moreira, 2011; Feng et al, 2012). Extensive studies on rice roots have identified many root traits that provide drought resistance. Rice genotypes that have deep, coarse roots with a high ability of branching and penetration and higher root to shoot ratio are reported as component traits of drought avoidance (Samson et al, 2002; Wang and Yamauchi, 2006; Gowda et al, 2011). Coarse roots have direct roles in drought resistance because larger diameter roots are related to penetration ability (Nguyen et al, 1997; Clark et al, 2008) and branching, and they have greater xylem vessel radii and lower axial resistance to water flux (Yambao et al, 1992). Capacity for deep root growth and large xylem diameters in deep roots may improve root acquisition of water when ample water at depth is available. While small xylem

Rice Science, Vol. 22, No. 4, 2015

diameters in targeted seminal roots save soil water deep in the soil profile for use during crop maturation. Henry et al (2012) suggested that lower xylem-sap bleeding rates from roots, more stable hydraulic conductivity with variation in soil moisture, more responsiveness of root anatomy to drought, and greater levels of aquaporin expression are component traits for drought resistance in rice. Trait like xylem pit anatomy that makes xylem less leaky also improves plant productivity in water-limited environments without negatively impacting yield under adequate water conditions (Comas et al, 2013). Thus, understanding the root physiology under drought will enable further insight of important traits that might influence crop productivity under stress and can contribute toward selection and development of drought resistant varieties, and thereby maintaining yield and ensuring global food security.

Effects of drought on physiological characteristics Drought stress affects various physiological processes and induces several physiological responses in plants, which help them to adapt to such limiting environmental conditions. Optimization of these physiological processes is prerequisite for increased water productivity under water stress (Serraj et al, 2009). The knowledge of these physiological responses of rice under drought conditions may contribute to ongoing studies on providing drought resistance in rice. An important physiological response of plants to drought is its ability to maintain turgor pressure by reducing osmotic potential as a tolerant mechanism (Maisura et al, 2014). Water deficit affects rice physiology in countless ways like it affects plant net photosynthesis (Centritto et al, 2009; Yang et al, 2014), transpiration rate (Cabuslay et al, 2002), stomatal conductance (Ji et al, 2012; Singh et al, 2013), water use efficiency (Cha-um et al, 2010), intercellular CO2, photosystem II (PSII) activity (Pieters and Souki, 2005), relative water content (Biswas and Choudhuri, 1984; Pirdashti et al, 2009; Cha-um et al, 2010) and membrane stability index (Kumar S et al, 2014). All these parameters reduce under water stress in rice (Farooq et al, 2010; Akram et al, 2013; Ding et al, 2014). Effects of drought on photosynthesis Photosynthesis is the main metabolic process determining crop production and is affected by drought stress. Drought induced reduction in photosynthetic

Veena PANDEY, et al. Acclimation and Tolerance Strategies of Rice under Drought Stress

rate of rice has been well documented (Ji et al, 2012; Lauteri et al, 2014; Yang et al, 2014). The major components limiting photosynthesis are the CO2 diffusional limitation due to early stomatal closure, reduced activity of photosynthetic enzymes, the biochemical components related to triose-phosphate formation and decreased photochemical efficiency of PSII. Change in any of these components alters the final photosynthesis rate. Stomatal (gs) and mesophyll conductance (gm) to CO2 often decrease in response to drought (Centritto et al, 2009). Thus, the ability to maintain the gm values under water-deficits determines the drought tolerance of rice varieties (Lauteri et al, 2014). Activity of PSII is crucial in providing reducing power and ATP. If PSII activity exceeds the demand, over-reduction of the photosynthetic electron transport chain may occur, and this stimulates the formation of reactive oxygen species. Therefore, there must be balance between photochemical activity and the demand for photoassimilates. Drought severely impaires PSII activity in the flag leaf of rice plants (Pieters and Souki, 2005). This may be due to drought induced degradation of D1 polypeptide, leading to the inactivation of the PSII reaction center. Severe drought conditions limit photosynthesis due to a decline in Rubisco activity, which is an enzyme of the Calvin cycle (Bota et al, 2004; Zhou et al, 2007). However, the amount of Rubisco activase, which rescues Rubisco sites from dead end inhibition by promoting ATP-dependent conformational changes, enhances under the drought stress as a protective mechanism. The up-regulation of this enzyme might alleviate the damage on Rubisco by drought stress (Ji et al, 2012). Recently, it has been observed that introduction of enzymes involved in photosynthesis of C4 plants in rice enhances the photosynthesis and crop productivity under stress. It is speculated that drought tolerance is greatly enhanced in transgenic rice plants overexpressing C4 photosynthesis enzymes like pyruvate orthophosphate dikinase and phosphoenolpyruvate carboxylase (Zhou et al, 2011; Gu et al, 2013). This is attributed to the fact that the enzymes involved in C4 photosynthesis are more tolerant to drought than those involved in C3 photosynthesis. This approach opens up new avenue in developing drought tolerance in rice. Effects of drought on photosynthetic pigments Drought causes many changes related to altered metabolic functions, and one of those is either loss of

151

or reduced the synthesis of photosynthetic pigments. This results in declined light harvesting and generation of reducing powers, which are a source of energy for dark reactions of photosynthesis. These changes in the amounts of photosynthetic pigments are closely associated to plant biomass and yield (Jaleel et al, 2009). Chlorophyll is one of the important pigments of photosynthetic apparatus which absorbs light and transfers light energy to the reaction center of the photosystem. Both chlorophyll a and b are prone to soil drying. However, other pigment carotenoids have additional roles in chloroplast photosystem structure, light harvesting and photoprotection, and partially help the plants to withstand adversaries of drought. Decreases in chlorophyll content and the maximum quantum yield of PSII (Fv/Fm) have been reported in many studies on drought stressed rice (Pirdashti et al, 2009; Cha-um et al, 2010; Sikuku et al, 2012; Ha, 2014; Maisura et al, 2014). Yang et al (2014) speculated that the reductions in chlorophyll content and the Fv/Fm of autotetraploid lines were less pronounced under drought than their corresponding diploid lines, suggesting that autotetraploid rice is more tolerant to drought stress. This reduction in chlorophyll content may occur due to stress-induced impairment in pigment biosynthetic pathways or in pigment degradation, loss of the chloroplast membrane, and increased lipid peroxidation. Effects of drought on water relations A key factor determining plant productivity under drought conditions is water use efficiency (WUE), and it is mentioned as a strategy to improve crop performance under water limited conditions (Araus et al, 2002). Agronomic parameters like photosynthetic rate, relative water content (RWC) and stomatal conductance show strong positive correlations with WUE, whereas transpiration rate expresses negative correlation with WUE under drought in basmati rice varieties (Akram et al, 2013). CID has been suggested as an indirect tool for selecting plants having higher WUE and yield potential. The physiological basis for CID variation in C3 plants is related to the variation in the internal CO2 concentration (Ci) to ambient CO2 concentration (Ca) ratio. High CID values resulting from high Ci/Ca will lead to low transpiration efficiency. Under drought conditions, CID is negatively correlated to transpiration efficiency (Dingkuhn et al, 1991; Scartazza et al, 1998;

152

Cabuslay et al, 2002; Kondo et al, 2004) and WUE (Impa et al, 2005) at the leaf level in rice. The discrimination against the heavier carbon isotope, 13C, is calculated as the 13C/12C ratio in plant material relative to the value of the same ratio in the air assimilated by plants. CID has been proposed by several authors as an indirect selection criterion for yield under drought (Condon et al, 2002; Akhter et al, 2010; Mohankumar et al, 2011). In general, water stress increases carbon isotope ratio (δ13C) and decreases CID values in rice (Kondo et al, 2004; Zhao et al, 2004; Impa et al, 2005; Centritto et al, 2009). Genotypic variation has been reported for δ13C or CID values in rice. The japonica genotypes show higher δ13C values or lower CID values than the indica ones (Takai et al, 2009; Xu et al, 2009; This et al, 2010). Recently, much attention has been focused on the differences in δ13C between plant organs. δ13C of different parts in rice plant is affected differentially under drought. The differences in carbon isotope composition among plant parts are related to the differences in fractionation processes during transport, the synthesis of metabolites, and the chemical composition of different organs, such as the amounts of lipids and lignin (Brugnoli and Farquhar, 2000). Kano-Nakata et al (2014) suggested that among various plant organs, the δ13C value of panicles may be the best indicator of plant water status in rice under drought. Effects of drought on stress hormone (abscisic acid) Abscisic acid (ABA) is a growth regulator and is also involved in stress tolerance. Several studies have confirmed its role in mediating plant responses against drought stress conditions through a series of signal transduction pathways. A dynamic accumulation of ABA in response to water stress has been well studied in rice (Wang et al, 2007; Ye et al, 2011; Ashok Kumar et al, 2013). ABA imparts drought stress tolerance in part by inducing a significant increase in antioxidant enzymes (Latif, 2014; Li et al, 2014) and improving protein transport, carbon metabolism and expression of resistance proteins (Zhou et al, 2014). Exogenous ABA application in rice enhances the recovery of the net photosynthetic rate, stomatal conductance and transpiration rate under drought, with increased expression of various drought responsive genes (Teng et al, 2014). ABA regulates stomatal movement (Ahmad et al, 2014) and thus is an important component of drought tolerance strategy for reduced water loss, by closing

Rice Science, Vol. 22, No. 4, 2015

stomata. The mechanism of action involves ABA receptor and responsive proteins. The genes for soluble ABA receptors have been identified as PYR/PYL/RCARs (pyrabactin resistance/PYR1-LIKE/ regulatory components of ABA receptors) (Ma et al, 2009; Park et al, 2009) and play major roles in ABAmediated regulation of SnRK2 kinase (sucrose nonfermenting1-related protein kinases 2) activity (Gonzalez-Guzman et al, 2012). This SnRK2 regulates guard cell channel activities by activation of the anion channel (Geiger et al, 2009; Lee et al, 2009), inducing depolarization of the guard cell membrane, resulting in the outward movement of potassium ions as well as closures of stomatal pores (Kim et al, 2010). ABA also induces the expression of many genes whose products are involved in the response to drought. These genes are mainly activated by a group of transcription factors, which specifically bind to promoters containing ABA-responsive elements (Antoni et al, 2011; Fujita et al, 2011; Rushton et al, 2012). These ABA-induced genes encode proteins involved in stress tolerance while ABA-repressed gene products are associated with growth. All these indicate the central role of ABA in plant tolerance to drought stress.

Effects of drought on biochemical characteristics As water deficit occurs, plants accumulate different types of organic and inorganic solutes in the cytosol to lower osmotic potential, thereby maintaining cell turgor (Rhodes and Samaras, 1994). This biochemical process is known as osmotic adjustment which strongly depends on the rate of plant water stress. Osmotic adjustment is achieved by the accumulation of proline, sucrose, glycinebetaine and other solutes in cytoplasm, improving water uptake from drying soil. Of these solutes, proline is the most widely studied because of its considerable importance in the stress tolerance. Drought also induces the accumulation of soluble sugars (Shehab et al, 2010; Usman et al, 2013; Maisura et al, 2014). Other biochemical response includes increase in the antioxidant activity which improves drought tolerance by scavenging reactive oxygen species. Role of proline under drought Proline plays a highly beneficial role in plants exposed to various stress conditions (Verbruggen and Hermans, 2008). The very first report, regarding the

Veena PANDEY, et al. Acclimation and Tolerance Strategies of Rice under Drought Stress

free proline accumulation due to water stress, is proposed by Kemble and Mac-Pherson (1954) in rye grasses. Proline acts as osmolyte and its accumulation contributes to better performance and drought tolerance (Vajrabhaya et al, 2001). Changes in the concentration of proline have been observed in rice exposed to drought stress (Sheela and Alexallder, 1995; Mostajeran and Rahimi-Eichi, 2009; Bunnag and Pongthai, 2013; Kumar S et al, 2014; Lum et al, 2014; Maisura et al, 2014). Besides acting as an excellent osmolyte, proline plays three major roles during stress, i.e., as a metal chelator, an antioxidative defence molecule and a signaling molecule (Hayat et al, 2012). Proline accumulation might promote plant damage repair ability by increasing antioxidant activity during drought stress. In plants under water stress, proline content increases more than other amino acids, and this effect has been used as a biochemical marker to select varieties aiming to resist to such conditions (Fahramand et al, 2014). Thus, proline content can be used as criterion for screening drought tolerant rice varieties. Role of polyamines under drought Polyamines (PAs) are small positively charged molecules (Fuell et al, 2010; Takahashi and Kakehi, 2010), which are involved in the response to drought (Calzadilla et al, 2014). Most ubiquitous PAs in plants are putrescine (Put), spermidine (Spd) and spermine (Spm). They stabilize membranes, regulate osmotic and ionic homeostasis, and act as antioxidants and interact with other signal molecules. Under drought stress conditions, higher PAs contents in plants are related to increased photosynthetic capacity, reduced water loss, improved osmotic adjustment and detoxification. However, the mechanism of action is not yet fully understood. The multiple suggested roles of PAs encompass the regulation of gene expression by enhancing the DNAbinding activity of transcription factors (Panagiotidis et al, 1995), maintenance of ion balance, prevention of senescence, radical scavenging, membrane stabilization (Bouchereau et al, 1999), involvement in protein phosphorylation and conformational transition of DNA (Martin-Tanguy, 2001). PAs accumulation is the immediate response observed after exposure to drought conditions in rice (Yang et al, 2007; Basu et al, 2010). Recent studies suggested that rice has a great capacity to enhance PAs biosynthesis, particularly Spd and Spm in free

153

form and Put in insoluble-conjugated form, in leaves earlier in response to drought stress (Yang et al, 2007). This can be considered as an important physiological trait of drought tolerance in rice. Exogenous PAs application can also alleviate drought stress. Its application improved net photosynthesis, WUE, leaf water status, production of free proline, anthocyanins and soluble phenolics and alleviate oxidative damage on cellular membranes (Farooq et al, 2009b). Studies indicate that foliar application is more effective than the seed priming, and among PAs, Spm is the most effective in improving drought tolerance in rice (Farooq et al, 2009b; Do et al, 2013). Other strategy to modify plant PAs level includes genetic engineering. Transgenic rice plants expressing the Datura adc gene (encoding arginine decarboxylase) produced much higher levels of Put under stress, promoting Spd and Spm synthesis and ultimately protecting the plants from drought (Capell et al, 2004). Thus, the production of higher PAs in transgenic by the over-expression of PAs biosynthesis gene can produce more drought-tolerant germplasm (Calzadilla et al, 2014). Role of antioxidants under drought A common effect of drought stress is the disturbance between the generation and quenching of reactive oxygen species (ROS) (Smirnoff, 1998; Faize et al, 2011). ROS includes superoxide radical, hydroxyl free radical, hydrogen peroxide and singlet oxygen, and causes peroxidation of lipids, denaturation of proteins, mutation of DNA, disrupt cellular hemeostasis and various types of cellular oxidative damage. Plant cells are protected against the detrimental effects of ROS by a complex antioxidant system comprising of the non-enzymatic as well as enzymatic antioxidants. Ascorbate (AsA) and glutathione (GSH) are served as potent non-enzymatic antioxidants within the cell. The enzymatic antioxidants include superoxide dismutase (SOD), catalase (CAT), guaiacol peroxidise (GPX), enzymes of ascorbate-glutathione cycle, ascorbate peroxidase (APX), monodehydroascorbate reductase (MDHAR), dehydroascorbate reductase (DHAR) and glutathione reductase (GR) (Noctor and Foyer, 1998). These antioxidants are critical components of the ROS scavenging system in plant, and their expressions can improve drought tolerance in rice (Wang et al, 2005). With increasing levels of drought stress in rice, the activities of AsA, GSH, APX (Selote and KhannaChopra, 2004), SOD, MDHAR, DHAR, GR (Sharma

154

and Dubey, 2005), phenylalanine ammonia-lyase and CAT (Shehab et al, 2010) consistently increase. The increases in the activities of these antioxidant defence enzymes represent the protective activity to counteract the oxidative injury promoted by drought conditions in rice. The activities of SOD, POD and CAT can effectively diminish the ROS, and thereby reducing negative impact of drought (Lum et al, 2014; Yang et al, 2014). Li et al (2012) suggested that mild drought preconditioning of rice alters antioxidant enzymes response in seedlings, so that they can acclimatize more successfully to intermediate drought stress environment. Therefore, enhancement of the naturally occurring antioxidant components (enzymatic and non-enzymatic) may be one strategy for reducing or preventing oxidative damage and improving the drought resistance of plants (Hasanuzzaman et al, 2014).

Effects of drought at molecular level At the molecular level, the response to drought stress is a multigenic trait. Through high-throughput molecular studies, a number of genes that respond to drought stress at the transcriptional level have been reported (Shinozaki and Yamaguchi-Shinozaki, 2007). Some of these genes in rice have been found to protect plants from desiccation through stress perception, signal transduction, transcriptional regulatory networks in cellular responses or tolerance to dehydration (Wang et al, 2005). The products of these stressinducible genes are classified into two groups. The first group includes proteins that directly protect against stress, probably by protecting cells from dehydration, such as the enzymes required for the biosynthesis of various osmoprotectants, late embryogenesis abundant proteins, antifreeze proteins, chaperones and detoxification enzymes. The second group are those that regulate gene expression and signal transduction in the stress response, which include transcription factors and protein kinases (Seki et al, 2003). These drought-induced regulatory and functional genes have been used to increase drought tolerance through gene transfer. Thus, it is important to analyze the functions of stress-inducible genes not only to understand the molecular mechanisms of stress responses, but also to improve the stress tolerance of crops by gene manipulation. Since drought tolerance characters are quantitative

Rice Science, Vol. 22, No. 4, 2015

traits, the dissection of these complex traits into component genetic factors is a prerequisite to manipulate the traits. The regions within genome that contain genes associated with a particular quantitative trait are known as quantitative trait loci (QTLs). Genome mapping using molecular genetic markers offers an excellent opportunity to locate genes or QTLs controlling quantitative characters (Manickavelu et al, 2006). Numerous QTLs linked to various drought resistance component traits have been mapped so far in rice using more than 15 mapping populations (Kamoshita et al, 2008). Further, some of the mapping populations were used in mapping QTLs associated with drought resistance at the reproductive stage (Liu et al, 2008; Yue et al, 2008). The identification of QTLs linked to yield under drought stress is critical (Chandra Babu, 2010). Yield being the ultimate aim, recent studies focus on mapping QTLs for yield under drought stress directly without analyzing the mechanism conferring drought resistance (Zhang et al, 2009; Dixit et al, 2014; Saikumar et al, 2014). Transcription factors (TFs), which can interact with cis regulatory sequences and regulate a series of related genes expression, are critical components of the abiotic stress signal transduction pathway. Most of these TFs fall into several large TF families, such as APETALA type 2/ethylene responsive factors (AP2/ERF), basic region/leucine zipper motif (bZIP), NAM/ATAF/CUC transcription factor (NAC), myeloblastosis (MYB), myelocytomatosis (MYC), Cys2His2 zinc-finger proteins (ZFP) and domain binding transcription factors (WRKY) (Umezawa et al, 2006). The best characterized TF groups are ABA responsive element binding protein 1 (AREB1), ABA responsive binding factor 2 (ABF2), dehydration responsive binding protein (DREB) genes, MYB genes, bZIP encoding genes and the protein kinases such as receptor like kinase 1, SNF1-related protein kinase 2C or guard cell expressing calcium dependent protein kinases (Choi et al, 2000). Thus, the knowledge of drought inducible TFs will open up avenues for development of the drought tolerant crop plants which will survive well in acute field conditions (Thapa et al, 2011). The main approaches utilized for identifying genes involved in drought stress tolerance in rice are transcript profiling via massively parallel signature sequencing (MPSS), expressed sequence tags profiling, RNA gel blot analysis, microarrays and quantitative real time PCR (Rabello et al, 2008) and comparative

Veena PANDEY, et al. Acclimation and Tolerance Strategies of Rice under Drought Stress

proteome analysis (Xiong et al, 2010). A large number of genes affected by drought stress have been identified through these approaches. However, only a small fraction of these genes have been functionally validated for their roles in enhancement of drought tolerance ability in rice (Sahoo et al, 2013). SNAC1 gene is induced predominantly in guard cells by drought and encodes a NAM, ATAF and CUC (NAC) transcription factor with transactivation activity. Stress-responsive rice SNAC genes such as SNAC1, OsNAC6/SNAC2 and OsNAC5 improve drought tolerance when over-expressed (Hu et al, 2006; Takasaki et al, 2010; Nakashima et al, 2014). Over-expression of TFs like AREB1 (Oh et al, 2005) and DREB/CBF (Oh et al, 2005; Ito et al, 2006; Datta et al, 2012) significantly improves tolerance to drought stress in rice. Many TFs have been used to produce transgenic rice lines with either constitutive or inducible promoters, such as HvCBF4 (Oh et al, 2007), AP37 (Kim and Kim, 2009; Oh et al, 2009), TaSTRG (Zhou et al, 2009), OsNAC045 (Zheng et al, 2009), ERF protein TSRF1 (Quan et al, 2010), ERF protein JERF3 (Zhang et al, 2010), OsDREB2A with the 4ABRC promoter (Cui et al, 2011), OsDREB2A with the rd29A promoter (Mallikarjuna et al, 2011), SbDREB2 (Bihani et al, 2011), OsSD1R1 (Gao et al, 2011), OsDREB1A, OsDREB1B (Datta et al, 2012), AtDREB1A (Hussain et al, 2014; Ravikumar et al, 2014), OsNAC6 (Rachmat et al, 2014) and the bZIP family (Xiang et al, 2008; Liu et al, 2014). TFHYR (higher yield rice) over expression in rice enhances photosynthesis leading to higher grain yield under drought conditions (Ambavaram et al, 2014). These TFs have been reported to enhance stress tolerance against drought in rice. Thus transcription factors are the master regulators of gene expression (Nakashima et al, 2014) and are considered to be key targets for biotechnological engineering of stress tolerance in plants (Liu et al, 2014).

Effects of drought on yield attributes Fetching greater harvestable yield is the ultimate purpose of growing crops. Rice grain yield severely reduces under drought stress (Bouman et al, 2005; Centritto et al, 2009; Pirdashti et al, 2009; Venuprasad et al, 2011; Ahadiyat et al, 2014; Maisura et al, 2014). Reduction in grain size, weight (Castillo et al, 2006; Venuprasad et al, 2007; Mostajeran and Rahimi-Eichi, 2009), seed-setting rate and 1000-grain weight (Ji et al,

155

2012) and increase in spikelet sterility (Raman et al, 2012; Kumar A et al, 2014) is commonly observed under drought stress. Drought stress at vegetative growth especially booting stage (Pantuwan et al, 2002), flowering and terminal periods can interrupt floret initiation, causing spikelet sterility and slow grain filling, resulting in lower grain weight and ultimately poor paddy yield (Kamoshita et al, 2004; Botwright Acuña et al, 2008). Drought reduces grain yield probably by shortening the grain filling period (Shahryari et al, 2008), disrupting leaf gas exchange properties, limiting the size of the source and sink tissues, impaired phloem loading and assimilate translocation (Farooq et al, 2009b). The decline in yield may also be due to drought induced reduction in CO2 assimilation rates, reduced stomatal conductance, photosynthetic pigments, small leaf size, reduced stem extension, disturbed plant water relations, reduced WUE, reduced activities of sucrose and starch synthesis enzymes and reduced assimilate partitioning, leading to a reduction in plant growth and productivity (Anjum et al, 2011). The magnitude of grain yield loss depends on the duration of drought, the stage of crop growth (Gana, 2011) and the severity of drought stress (Kumar A et al, 2014).

Perspectives Drought is recognized as an environmental disaster that impairs rice production. Drought tolerance improvement in rice is one of the challenging tasks due to its complex and unpredictable nature. To facilitate the development of tolerant varieties which can survive and give better yields under drought conditions, a thorough understanding of the various morphological, biochemical, physiological and molecular characters that govern the yield of rice under water stress condition is a prerequisite. Morphological traits viz., maintenance of turgor, initiation of leaf rolling, cuticular wax, deep and course root with greater xylem vessel radii and lower axial resistance to water flux can be used as criterions for scoring drought tolerance. Most physiological and metabolic processes are affected by water deficits which include stomatal regulation, photosynthesis, translocation, PSII activity, chlorophyll content, etc. Maintenance of these processes for prolonged period of time under drought is a desired character. Since, ABA is an important component of signalling under drought stress, efficient ABA signalling also ensures

156

Rice Science, Vol. 22, No. 4, 2015

tolerance. Biochemical parameters viz., proline and polyamine accumulation in plants under drought stress conditions can be used as criterions for screening drought tolerant rice varieties. Further, the enhancement of the naturally occurring antioxidant components (enzymatic and non-enzymatic) may be another strategy for reducing oxidative damage and can be considered vital mechanism of drought tolerance. Less reduction in grain yield during drought is the critical trait that plays an important role on tolerance against drought. Thus, yield stability under drought conditions and increased crop water productivity should be the target of all the approaches involved in drought tolerance. Molecular attributes are key traits linked to yield under drought. A very large number of genes in rice are up- or down-regulated by drought. Genetic engineering of regulatory and functional elements in rice not only enhanced the plant survival in drought conditions but also improved the crop productivity. Recently, many TFs have been identified in rice, the expression of which provides drought tolerance as well as improves yield under stressful conditions. In spite of extensive studies, there is still a strong need for more detailed characterization of the response and acclimation mechanism of rice under drought that is occurring in farmers’ fields. For this, it is essential to integrate crop physiology, molecular genetics and breeding approaches to dissect complex drought tolerance traits, and develop the nextgeneration crops which can withstand the adverse climate and ensure food security.

ACKNOWLEDGEMENTS This study was supported by the Department of Science & Technology, New Delhi, India. The authors are highly grateful to All India Coordinated Rice Improvement Project, Indian Council of Agricultural Research, New Delhi, India.

REFERENCES Abd Allah A A. 2009. Genetic studies on leaf rolling and some root traits under drought conditions in rice (Oryza sativa L.). Afr J Biotechnol, 8(22): 6241–6248. Ahadiyat Y R, Hidayat P, Susanto U. 2014. Drought tolerance, phosphorus efficiency and yield characters of upland rice lines. Emir J Food Agric, 26(1): 25–34. Ahmad M, Zaffar G, Razvi S M, Dar Z A, Mir S D, Bukhari S A, Habib M. 2014. Resilience of cereal crops to abiotic stress: A review. Afr J Biotechnol, 13(29): 2908–2921.

Akhter J, Monneveux P, Sabir S A, Ashraf M Y, Lateef Z, Serraj R. 2010. Selection of drought tolerant and high water use efficient rice cultivars through 13C isotope discrimination technique. Pak J Bot, 42(6): 3887–3897. Akram H M, Ali A, Sattar A, Rehman H S U, Bibi A. 2013. Impact of water deficit stress on various physiological and agronomic traits of three basmati rice (Oryza sativa L.) cultivars. J Anim Plant Sci, 23(5): 1415–1423. Ambavaram M M R, Basu S, Krishnan A, Ramegowda V, Batlang U, Rahman L, Baisakh N, Pereira A. 2014. Coordinated regulation of photosynthesis in rice increases yield and tolerance to environmental stress. Nat Commun, 31(5): 5302. Anjum S A, Xie X, Wang L, Saleem M F, Man C, Lei W. 2011. Morphological, physiological and biochemical responses of plants to drought stress. Afr J Agric Res, 6(9): 2026–2032. Antoni R, Rodriguez L, Gonzalez-Guzman M, Pizzio G A, Rodriguez P L. 2011. News on ABA transport, protein degradation, and ABFs/WRKYs in ABA signaling. Curr Opin Plant Biol, 14(5): 547−553. Araus J L, Slafer G A, Reynolds M P, Royo C. 2002. Plant breeding and drought in C3 cereals: What should we breed for? Ann Bot, 89(7): 925–940. Ashfaq M, Haider M S, Khan A S, Allah S U. 2012. Breeding potential of the basmati rice germplasm under water stress condition. Afr J Biotechnol, 11(25): 6647–6657. Ashok Kumar K, Suresh Kumar M, Sudha M, Vijayalakshmi D, Vellaikumar S, Senthil N, Raveendran M. 2013. Identification of genes controlling ABA accumulation in rice during drought stress and seed maturation. Int J Adv Biotechnol Res, 4(4): 481–487. Basu S, Roychoudhury A, Saha P P, Sengupta D N. 2010. Comparative analysis of some biochemical responses of three indica rice varieties during polyethylene glycol-mediated water stress exhibits distinct varietal differences. Acta Physiol Plant, 32(3): 551–563. Bihani P, Char B, Bhargava S. 2011. Transgenic expression of sorghum DREB2 in rice improves tolerance and yield under water limitation. J Agric Sci, 149(1): 95–101. Biswal A K, Kohli A. 2013. Cereal flag leaf adaptations for grain yield under drought: Knowledge status and gaps. Mol Breeding, 31(4): 749–766. Biswas A K, Choudhuri M A. 1984. Effect of water stress at different developmental stages of field-grown rice. Biol Plant, 26(4): 263–266. Blum A. 2011. Drought tolerance: Is it a complex trait? Funct Plant Biol, 38(10): 753–757. Bota J, Medrano H, Flexas J. 2004. Is photosynthesis limited by decreased Rubisco activity and RuBP content under progressive water stress? New Phytol, 162(3): 671–681. Botwright Acuña T L, Latte H R, Wade L J. 2008. Genotype and environment interactions for grain yield of upland rice backcross lines in diverse hydrological environments. Field Crops Res, 108(2): 117–125. Bouchereau A, Aziz A, Larher F, Martin-Tanguy J. 1999. Polyamines and environmental challenges: Recent development. Plant Sci, 140(2): 103–125.

Veena PANDEY, et al. Acclimation and Tolerance Strategies of Rice under Drought Stress Bouman B A M, Peng S, Castañeda A R, Visperas R M. 2005. Yield and water use of irrigated tropical aerobic rice systems. Agric Water Manag, 74(2): 87–105. Brugnoli E, Farquhar G D. 2000. Photosynthetic fractionation of carbon isotopes. In: Leegood R C, Sharkey T D, Von Caemmerer S. Photosynthesis: Physiology and Metabolism. Dordrecht: Kluwer Academic Publishers: 352–434. Bunnag S, Pongthai P. 2013. Selection of rice (Oryza sativa L.) cultivars tolerant to drought stress at the vegetative stage under field conditions. Am J Plant Sci, 4(9): 1701–1708. Cabuslay G S, Ito O, Alejal A A. 2002. Physiological evaluation of responses of rice (Oryza sativa L.) to water deficit. Plant Sci, 163(4): 815–827. Calzadilla P I, Gazquez A, Maiale S J, Rodriguez A A, Ruiz O A, Bernardina M A. 2014. Polyamines as indicators and modulators of the abiotic stress in plants. In: Anjum N A, Gill S S, Gill R. Plant adaptation to environmental change: Significance of amino acids and their derivatives. CABI, Wallingford, UK: 109–128. Capell T, Bassie L, Christou P. 2004. Modulation of the polyamine biosynthetic pathway in transgenic rice confers tolerance to drought stress. Proc Natl Acad Sci USA, 101(26): 9909–9914. Castillo E G, Tuong T P, Singh U, Inubushi K, Padilla J. 2006. Drought response of dry-seeded rice to water stress timing and Nfertilizer rates and sources. Soil Sci Plant Nutr, 52(4): 496–508. Centritto M, Lauteri M, Monteverdi M C, Serraj R. 2009. Leaf gas exchange, carbon isotope discrimination, and grain yield in contrasting rice genotypes subjected to water deficits during the reproductive stage. J Exp Bot, 60(8): 2325–2339. Cerqueira F B, Erasmo E A L, Silva J I C, Nunes T V, Carvalho G P, Silva A A. 2013. Competition between drought-tolerant upland rice cultivars and weeds under water stress condition. Planta Daninha, 31(2): 291–302. Chandra Babu R. 2010. Breeding for drought resistance in rice: An integrated view from physiology to genomics. Electron J Plant Breeding, 1(4): 1133–1141. Cha-um S, Yooyongwech S, Supaibulwatana K. 2010. Water deficit stress in the reproductive stage of four indica rice (Oryza sativa L.) genotypes. Pak J Bot, 42(5): 3387–3398. Choi H I, Hong J H, Ha J O, Kang J Y, Kim S Y. 2000. ABFs, a family of ABA-responsive element binding factors. J Biol Chem, 275(3): 1723–1730. 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 Linn.) genotypes of Assam, India: II. Protein and proline status in seedlings under PEG induced water stress. Am J Plant Sci, 3(7): 971–980. Clark L J, Price A H, Steele K A, Whalley W R. 2008. Evidence from near-isogenic lines that root penetration increases with root diameter and bending stiffness in rice. Funct Plant Biol, 35(11): 1163–1171. Comas L H, Becker S R, Cruz V M, Byrne P F, Dierig D A. 2013. Root traits contributing to plant productivity under drought. Front Plant Sci, 5(4): 442. Condon A G, Richards R A, Rebetzke G J, Farquhar G D. 2002. Improving water use efficiency and crop yield. Crop Sci, 42: 122–132.

157

Cui M, Zhang W J, Zhang Q, Xu Z Q, Zhu Z G, Duan F P, Wu R. 2011. Induced over-expression of the transcription factor OsDREB2A improves drought tolerance in rice. Plant Physiol Biochem, 49(12): 1384–1391. Datta K, Baisakh N, Ganguly M, Krishnan S, Shinozaki K Y, Datta S K. 2012. Overexpression of Arabidopsis and rice stress genes inducible transcription factor confers drought and salinity tolerance to rice. Plant Biotechnol J, 10(5): 579–586. Ding L, Li Y R, Li Y, Shen Q R, Guo S W. 2014. Effects of drought stress on photosynthesis and water status of rice leaves. Chin J Rice Sci, 28(1): 65–70. (in Chinese with English abstract) Dingkuhn M, Farquhar G D, De Datta S K, O’Toole J C. 1991. Discrimination of 13C among upland rice having different water use efficiencies. Aust J Agric Res, 42: 1123–1131. Dixit S, Singh A, Sta Cruz M T, Maturan P T, Amante M, Kumar A. 2014. Multiple major QTL lead to stable yield performance of rice cultivars across varying drought intensities. BMC Genet, 15: 16. Do P T, Degenkolbe T, Erban A, Heyer A G, Kopka J, Kohl K L, Hincha D K, Zuther E. 2013. Dissecting rice polyamine metabolism under controlled long-term drought stress. PLoS One, 8(4): e60325. Fageria N K, Moreira A. 2011. The role of mineral nutrition on root crop growth of crop plants. Adv Agron, 110: 251–331. Fahramand M, Mahmoody M, Keykha A, Noori M, Rigi K. 2014. Influence of abiotic stress on proline, photosynthetic enzymes and growth. Int Res J Appl Basic Sci, 8(3): 257–265. Faize M, Burgos L, Faize L, Piqueras A, Nicolas E, Barba-Espin G, Clemente-Moreno M J, Alcobendas R, Artlip T, Hernandez J A. 2011. Involvement of cytosolic ascorbate peroxidase and Cu/Znsuperoxide dismutase for improved tolerance against drought stress. J Exp Bot, 62(8): 2599–2613. Farooq M, Wahid A, Kobayashi N, Fujita D, Basra S M A. 2009a. Plant drought stress: Effects, mechanisms and management. Agron Sustain Dev, 29(1): 185–212. Farooq M, Wahid A, Lee D J. 2009b. Exogenously applied polyamines increase drought tolerance of rice by improving leaf water status, photosynthesis and membrane properties. Acta Physiol Plant, 31(5): 937–945. Farooq M, Kobayashi N, Ito O, Wahid A, Serraj R. 2010. Broader leaves result in better performance of indica rice under drought stress. J Plant Physiol, 167(13): 1066–1075. Feng F J, Xu X Y, Du X B, Tong H H, Luo L J, Mei H W. 2012. Assessment of drought resistance among wild rice accessions using a protocol based on single-tiller propagation and PVC-tube cultivation. Aust J Crop Sci, 6: 1205–1211. Foley J A, Ramankutty N, Braumann K A, Cassidy E S, Gerber J S, Johnston M, Mueller N D, O’Connell C, Ray D K, West P C, Balzer C, Bennett E M, Carpenter S R, Hill J, Monfreda C, Polasky S, Rockström J, Sheehan J, Siebert S, Tilman D, Zaks D P M. 2011. Solutions for a cultivated planet. Nature, 478: 337–342. Fuell C, Elliott K A, Hanfrey C C, Franceschetti M, Michael A J. 2010. Polyamine biosynthetic diversity in plants and algae. Plant Physiol Biochem, 48(7): 513–520. Fujita Y, Fujita M, Shinozaki K, Yamaguchi-Shinozaki K. 2011. ABA-mediated transcriptional regulation in response to osmotic stress in plants. J Plant Res, 124(4): 509−525.

158 Gana A S. 2011. Screening and resistance of traditional and improved cultivars of rice to drought stress at Badeggi, Niger State, Nigeria. Agric Biol J North Am, 2(6): 1027–1031. Gao T, Wu Y R, Zhang Y Y, Liu L J, Ning Y S, Wang D J, Tong H N, Chen S Y, Chu C C, Xie Q. 2011. OsSDIR1 over expression greatly improves drought tolerance in transgenic rice. Plant Mol Biol, 76(1/2): 145–156. Geiger D, Scherzer S, Mumm P, Stange A, Marten I, Bauer H, Ache P, Matschi S, Liese A, Al-Rasheid K A, Romeis T, Hedrich R. 2009. Activity of guard cell anion channel SLAC1 is controlled by drought-stress signaling kinase-phosphatase pair. Proc Natl Acad Sci USA, 106(50): 21425−21430. Gonzalez-Guzman M, Pizzio G A, Antoni R, Vera-Sirera F, Merilo E, Bassel G W, Fernandez M A, Holdsworth M J, Perez-Amador M A, Kollist H, Rodriguez P L. 2012. Arabidopsis PYR/PYL/ RCAR receptors play a major role in quantitative regulation of stomatal aperture and transcriptional response to abscisic acid. Plant Cell, 24(6): 2483−2496. Gowda V R P, Henry A, Yamauchi A, Shashidhar H E, Serraj R. 2011. Root biology and genetic improvement for drought avoidance in rice. Field Crops Res, 122(1): 1–13. Gu J F, Qiu M, Yang J C. 2013. Enhanced tolerance to drought in transgenic rice plants overexpressing C4 photosynthesis enzymes. Crop J, 1(2): 105–114. Ha P T T. 2014. Physiological responses of rice seedlings under drought stress. J Sci Devel, 12(5): 635–640. Hasanuzzaman M, Nahar K, Gill S S, Gill R, Fujita M. 2014. Drought stress responses in plants, oxidative stress and antioxidant defense. In: Gill S S, Tuteja N. Climate Change and Plant Abiotic Stress Tolerance. Blackwell, Germany: Wiley: 209–249. Hayat S, Hayat Q, Alyemeni M N, Wani A S, Pichtel J, Ahmad A. 2012. Role of proline under changing environments: A review. Plant Signal Behav, 7(11): 1456–1466. Henry A, Cal A J, Batoto T C, Torres R O, Serraj R. 2012. Root attributes affecting water uptake of rice (Oryza sativa) under drought. J Exp Bot, 63(13): 4751–4763. Hsiao T C, Xu L K. 2000. Sensitivity of growth of roots verses leaves to water stress: Biophysical analysis and relation to water transport. J Exp Bot, 51: 1595–1616. Hu H H, Dai M Q, Yao J L, Xiao B Z, Li X H, Zhang Q F, Xiong L Z. 2006. Overexpressing a NAM, ATAF, and CUC (NAC) transcription factor enhances drought resistance and salt tolerance in rice. Proc Natl Acad Sci USA, 103(35): 12987–12992. Hussain Z, Ali S, Hayat Z, Zia M A, Iqbal A, Ali G M. 2014. Agrobacterium mediated transformation of DREB1A gene for improved drought tolerance in rice cultivars (Oryza sativa L.). Aust J Crop Sci, 8(7): 1114–1123. Impa S M, Nadaradjan S, Boominathan P, Shashidhar G, Bindumadhava H, Sheshshayee M S. 2005. Carbon isotope discrimination accurately reflects variability in WUE measured at a whole plant level in rice. Crop Sci, 45(6): 2517–2522. Ito Y, Katsura K, Maruyama K, Taji T, Kobayashi M, Seki M, Shinozaki K, Yamaguchi-Shinozaki K. 2006. Functional analysis of rice DREB1/CBF-type transcription factors involved in cold-responsive gene expression in transgenic rice. Plant Cell

Rice Science, Vol. 22, No. 4, 2015 Physiol, 47(1): 141–153. Jaleel C A, Manivannan P, Wahid A, Farooq M, Al-Juburi H J, Somasundaram R, Panneerselvam R. 2009. Drought stress in plants: A review on morphological characteristics and pigments composition. Int J Agric Biol, 11: 100–105. Ji K X, Wang Y Y, Sun W N, Lou Q J, Mei H W, Shen S H, Chen H. 2012. Drought-responsive mechanisms in rice genotypes with contrasting drought tolerance during reproductive stage. J Plant Physiol, 169(4): 336–344. Jiang W, Lafitte R. 2007. Ascertain the effect of PEG and exogenous ABA on rice growth at germination stage and their contribution to selecting drought tolerant genotypes. Asian J Plant Sci, 6(4): 684–687. Kadioglu A, Terzi R. 2007. A dehydration avoidance mechanism: Leaf rolling. Bot Rev, 73(4): 290–302. Kamoshita A, Rofriguez R, Yamauchi A, Wade L J. 2004. Genotypic variation in response of rainfed lowland to prolonged drought and re-watering. Plant Prod Sci, 7(4): 406–420. Kamoshita A, Chandra Babu R, Boopathi N M, Shu F K. 2008. Phenotypic and genotypic analysis of drought-resistance traits for development of rice cultivars adapted to rainfed environments. Field Crops Res, 109: 1–23. Kano-Nakata M, Tatsumi J, Inukai Y, Asanuma S, Yamauchi A. 2014. Effect of various intensities of drought stress on δ13C variation among plant organs in rice: Comparison of two cultivars. Am J Plant Sci, 5(11): 1686–1693. Kemble A R, Macpherson H T. 1954. Liberation of amino acids in perennial rye grass during wilting. Biochem J, 58(1): 46–49. Khush G S. 2005. What it will take to feed 5.0 billion rice consumers in 2030. Plant Mol Biol, 59(1): 1–6. Kim T H, Bohmer M, Hu H, Nishimura N, Schroeder J I. 2010. Guard cell signal transduction network: Advances in understanding abscisic acid, CO2, and Ca2+ signaling. Annu Rev Plant Biol, 61: 561−591. Kim Y S, Kim J K. 2009. Rice transcription factor AP37 involved in grain yield increase under drought stress. Plant Signal Behav, 4(8): 735–736. Kondo M, Pablico P P, Aragones D V, Agbisit R. 2004. Genotypic variations in carbon isotope discrimination, transpiration efficiency, and biomass production in rice as affected by soil water conditions and N. Plant Soil, 267(1): 165–177. Kumar A, Dixit S, Ram T, Yadaw R B, Mishra K K, Mandal N P. 2014. Breeding high-yielding drought-tolerant rice: Genetic variations and conventional and molecular approaches. J Exp Bot, 65(21): 6265–6278. Kumar S, Dwivedi S K, Singh S S, Bhatt B P, Mehta P, Elanchezhian R, Singh V P, Singh O N. 2014. Morphophysiological traits associated with reproductive stage drought tolerance of rice (Oryza sativa L.) genotypes under rain-fed condition of eastern Indo-Gangetic Plain. Ind J Plant Physiol, 19(2): 87–93. Latif H H. 2014. Physiological responses of Pisum sativum plant to exogenous ABA application under drought conditions. Pak J Bot, 46(3): 973–982. Lauteri M, Haworth M, Serraj R, Monteverdi M C, Centritto M.

Veena PANDEY, et al. Acclimation and Tolerance Strategies of Rice under Drought Stress 2014. Photosynthetic diffusional constraints affect yield in drought stressed rice cultivars during flowering. PLoS One, 9(10): e109054. Lee S C, Lan W, Buchanan B B, Luan S. 2009. A protein kinase phosphatase pair interacts with an ion channel to regulate ABA signaling in plant guard cells. Proc Natl Acad Sci USA, 106(50): 21419−21424. Li C N, Yang L T, Srivastava M K, Li Y R. 2014. Foliar application of abscisic acid improves drought tolerance of sugarcane plant under severe water stress. Int J Agric Innov Res, 3(1): 101–107. Li X M, Zhang L H, Li Y Y. 2012. Preconditioning alters antioxidative enzyme responses in rice seedlings to water stress. Proc Environ Sci, 11: 1346–1351. Liu C T, Mao B G, Ou S J, Wang W, Liu L C, Wu Y B, Chu C C, Wang X P. 2014. OsbZIP71, a bZIP transcription factor, confers salinity and drought tolerance in rice. Plant Mol Biol, 84(1/2): 19–36. Liu G L, Mei H W, Yu X Q, Zou G H, Liu H Y, Hu S P, Li M S, Wu J H, Chen L, Luo L J. 2008. QTL analysis of panicle neck diameter, a trait highly correlated with panicle size, under wellwatered and drought conditions in rice (Oryza sativa L.). Plant Sci, 174(1): 71–77. Lum M S, Hanafi M M, Rafii Y M, Akmar A S N. 2014. Effect of drought stress on growth, proline and antioxidant enzyme activities of upland rice. J Anim Plant Sci, 24(5): 1487–1493. Ma Y, Szostkiewicz I, Korte A, Moes D, Yang Y, Christmann A, Grill E. 2009. Regulators of PP2C phosphatase activity function as abscisic acid sensors. Science, 324: 1064−1068. Maisura, Chozin M A, Lubis I, Junaedinand A, Ehara H. 2014. Some physiological character responses of rice under drought conditions in a paddy system. J Int Soc Southeast Asian Agric Sci, 20(1): 104–114. Mallikarjuna G, Mallikarjuna K, Reddy M K, Kaul T. 2011. Expression of OsDREB2A transcription factor confers enhanced dehydration and salt stress tolerance in rice (Oryza sativa L.). Biotechnol Lett, 33: 1689–1697. Manikavelu A, Nadarajan N, Ganesh S K, Gnanamalar R P, Chandra Babu R. 2006. Drought tolerance in rice: Morphological and molecular genetic consideration. Plant Growth Regul, 50(2/3): 121–138. Martin-Tanguy J. 2001. Metabolism and function of polyamines in plants: Recent development (new approaches). Plant Growth Regul, 34(1): 135–148. Mohankumar M V, Sheshshayee M S, Rajanna M P, Udayakumar M. 2011. Correlation and path analysis of drought tolerance traits on grain yield in rice germplasm accessions. J Agric Biol Sci, 6(7): 70–77. Mostajeran A, Rahimi-Eichi V. 2009. Effects of drought stress on growth and yield of rice (Oryza sativa L.) cultivars and accumulation of proline and soluble sugars in sheath and blades of their different ages leaves. Am-Eur J Agric Environ Sci, 5(2): 264–272. Nakashima K, Yamaguchi-Shinozaki K, Shinozaki K. 2014. The transcriptional regulatory network in the drought response and its crosstalk in abiotic stress responses including drought, cold, and heat. Front Plant Sci, 5: 1–7.

159

Nguyen H T, Babu R C, Blum A. 1997. Breeding for drought resistance in rice: Physiological and molecular genetics considerations. Crop Sci, 37(5): 1426–1434. Noctor G, Foyer C H. 1998. Ascorbate and glutathione: Keeping active oxygen under control. Annu Rev Plant Physiol Plant Mol Biol, 49: 249–279. Oh S J, Song S I, Kim Y S, Jang H J, Kim S Y, Kim M, Kim Y K, Nahm B H, Kim J K. 2005. Arabidopsis CBF3/DREB1A and ABF3 in transgenic rice increased tolerance to abiotic stress without stunting growth. Plant Physiol, 138(1): 341–351. Oh S J, Kwon C W, Choi D W, Song S I, Kim J K. 2007. Expression of barley HvCBF4 enhances tolerance to abiotic stress in transgenic rice. Plant Biotechnol J, 5(5): 646–656. Oh S J, Kim Y S, Kwon C W, Park H K, Jeong J S, Kim J K. 2009. Over-expression of the transcription factor AP37 in rice improves grain yield under drought conditions. Plant Physiol, 150(3): 1368–1379. Panagiotidis C A, Artandi S, Calame K, Silverstein S J. 1995. Polyamines alter sequence-specific DNA-protein interactions. Nucl Acids Res, 23(10): 1800–1809. Pantuwan G, Fukai S, Cooper M, Rajatasereekul S, O’Toole J C. 2002. Yield responses of rice (Oryza sativa L.) genotypes to drought under rainfed lowlands: 2. Selection of drought resistant genotypes. Field Crops Res, 73(2/3): 169–180. Park S Y, Fung P, Nishimura N, Jensen D R, Fujii H, Zhao Y, Lumba S, Santiago J, Rodrigues A, Chow T F, Alfred S E, Bonetta D, Finkelstein R, Provart N J, Desveaux D, Rodriguez P L, McCourt P, Zhu J K, Schroeder J I, Volkman B F, Cutler S R. 2009. Abscisic acid inhibits type 2C protein phosphatases via the PYR/PYL family of START proteins. Science, 324: 1068−1071. Pieters A J, Souki S E. 2005. Effects of drought during grain filling on PSII activity in rice. J Plant Physiol, 162(8): 903–911. Pirdashti H, Sarvestani Z T, Bahmanyar M A. 2009. Comparison of physiological responses among four contrast rice cultivars under drought stress conditions. Proc World Acad Sci Engin Technol, 49: 52–53. Quan R D, Hu S J, Zhang Z L, Zhang H W, Zhang Z J, Huang R F. 2010. Over expression of an ERF transcription factor TSRF1 improves rice drought tolerance. Plant Biotechnol J, 8(4): 476–488. Rabello A R, Guimarães C M, Rangel P H N, da Silva F R, Seixas D, de Souza E, Brasileiro A C M, Spehar C R, Ferreira M E, Mehta Â. 2008. Identification of drought-responsive genes in roots of upland rice (Oryza sativa L.). BMC Genom, 9: 485. Rachmat A, Nugroho S, Sukma D, Aswidinnoor H, Sudarsono S. 2014. Overexpression of OsNAC6 transcription factor from Indonesia rice cultivar enhances drought and salt tolerance. Emir J Food Agric, 26(6): 497–507. Raman A, Verulkar S B, Mandal N P, Variar M, Shukla V D, Dwivedi J L, Singh B N, Singh O N, Swain P, Mall A K, Robin S, Chandrababu R, Jain A, Ram T, Hittalmani S, Haefele S, Piepho H P, Kumar A. 2012. Drought yield index to select high yielding rice lines under different drought stress severities. Rice, 5(31): 1–12. Ravikumar G, Manimaran P, Voleti S R, Subrahmanyam D, Sundaram R M, Bansal K C, Viraktamath B C, Balachandran S M. 2014. Stress-inducible expression of AtDREB1A transcription

160 factor greatly improves drought stress tolerance in transgenic indica rice. Transgenic Res, 23(3): 421–439. Ray D K, Mueller N D, West P C, Foley J A. 2013. Yield trends are insufficient to double global crop production by 2050. PLoS One, 8(6): e66428. Ray D K, Gerber J S, MacDonald G K, West P C. 2015. Climate variation explains a third of global crop yield variability. Nat Commun, 6: 5989. Rhodes D, Samaras Y. 1994. Genetic control of osmoregulation in plants. In: Strange S K. Cellular and Molecular Physiology of Cell Volume Regulation. Boca Raton: CRC Press: 347–361. Rushton D L, Tripathi P, Rabara R C, Lin J, Ringler P, Boken A K, Langum T J, Smidt L, Boomsma D D, Emme N J, Chen X F, Finer J J, Shen Q J, Rushton P J. 2012. WRKY transcription factors: Key components in abscisic acid signalling. Plant Biotechnol J, 10(1): 2−11. Sahoo K K, Tripathi A K, Pareek A, Singla-Pareek S L. 2013. Taming drought stress in rice through genetic engineering of transcription factors and protein kinases. Plant Stress, 7(1): 60–72. Saikumar S, Gouda P K, Saiharini A, Varma C M K, Vineesha O, Padmavathi G, Shenoy V V. 2014. Major QTL for enhancing rice grain yield under lowland reproductive drought stress identified using an O. sativa/O. glaberrima introgression line. Field Crops Res, 163: 119–131. Salunkhe A S, Poornima R, Prince K S, Kanagaraj P, Sheeba J A, Amudha K, Suji K K, Senthil A, Babu R C. 2011. Fine mapping QTL for drought resistance traits in rice (Oryza sativa L.) using bulk segregant analysis. Mol Biotechnol, 49(1): 90–95. Samson B K, Hasan H, Wade L J. 2002. Penetration of hardpans by rice lines in the rainfed lowlands. Field Crops Res, 76(2/3): 175–188. Sarvestani Z T, Pirdashti H, Sanavy S A, Balouchi H. 2008. Study of water stress effects in different growth stages on yield and yield components of different rice (Oryza sativa L.) cultivars. Pak J Biol Sci, 11(10): 1303–1309. Scartazza A, Lauteri M, Guido M C, Brugnoli E. 1998. Carbon isotope discrimination in leaf and stem sugars, water-use efficiency and mesophyll conductance during different developmental stages in rice subjected to drought. Aust J Plant Physiol, 25(4): 489–498. Seki M, Kamei A, Yamaguchi-Shinozaki K, Shinozaki K. 2003. Molecular responses to drought, salinity and frost: Common and different paths for plant protection. Curr Opin Biotechnol, 14(2): 194–199. Selote D S, Khanna-Chopra R. 2004. Drought-induced spikelet sterility is associated with an inefficient antioxidant defence in rice panicles. Physiol Plant, 121(3): 462–471. Serraj R, Kumar A, McNally K L, Slamet-Loedin I, Bruskiewich R, Mauleon R, Cairns J, Hijmans R J. 2009. Improvement of drought resistance in rice. Adv Agron, 103: 41–98. Serraj R, McNally K L, Slamet-Loedin I, Kohli A, Haefele S M, Atlin G, Kumar A. 2011. Drought resistance improvement in rice: An integrated genetic and resource management strategy. Plant Prod Sci, 14(1): 1–14. Shahryari R, Gurbanov E, Gadimov A, Hassanpanah D. 2008.

Rice Science, Vol. 22, No. 4, 2015 Tolerance of 42 bread wheat genotypes to drought stress after anthesis. Pak J Biol Sci, 11(10): 1330–1335. Shao H B, Chu L Y, Shao M A, Jaleel C A, Mi H M. 2008. Higher plant antioxidants and redox signaling under environmental stresses. Comp Rend Biol, 331: 433–441. Sharma P, Dubey R S. 2005. Drought induces oxidative stress and enhances the activities of antioxidant enzymes in growing rice seedlings. Plant Growth Regul, 46(3): 209–221. Sheela K R, Alexallder V T. 1995. Physiological response of rice varieties as influenced by soil moisture and seed hardening. Ind J Plant Physiol, 38(3): 269–271. Shehab G G, Ahmed O K, El-Beltagi H S. 2010. Effects of various chemical agents for alleviation of drought stress in rice plants (Oryza sativa L.). Not Bot Hort Agrobot Cluj-Napoca, 38(1): 139–148. Shinozaki K, Yamaguchi-Shinozaki K. 2007. Gene networks involved in drought stress response and tolerance. J Exp Bot, 58(2): 221–227. Sikuku P A, Onyango J C, Netondo G W. 2012. Physiological and biochemical responses of five nerica rice varieties (Oryza sativa L.) to water deficit at vegetative and reproductive stage. Agric Biol J North Am, 3(3): 93–104. Singh A, Sengar K, Sengar R S. 2013. Gene regulation and biotechnology of drought tolerance in rice. Int J Biotechnol Bioeng Res, 4(6): 547–552. Smirnoff N. 1998. Plant resistance to environmental stress. Curr Opin Biotechnol, 9(2): 214–219. Sokoto M B, Muhammad A. 2014. Response of rice varieties to water stress in Sokoto, Sudan Savannah, Nigeria. J Biosci Med, 2(1): 68–74. Subashri M, Robin S, Vinod K K, Rajeswari S, Mohanasundaram K, Raveendran T S. 2009. Trait identification and QTL validation for reproductive stage drought resistance in rice using selective genotyping of near flowering RILs. Euphytica, 166(2): 291–305. Swain P, Anumalla M, Prusty S, Marndi B C, Rao G J N. 2014. Characterization of some Indian native land race rice accessions for drought tolerance at seedling stage. Aust J Crop Sci, 8(3): 324–331. Taiz L, Zeiger E. 2006. Plant Physiology. 4th edn. Sunderland, MA: Sinauer Associates: 7–64. Takahashi T, Kakehi J I. 2010. Polyamines: Ubiquitous polycations with unique roles in growth and stress responses. Ann Bot, 105(1): 1–6. Takai T, Ohsumi A, San-oh Y, Laza M R, Kondo M, Yamamoto T, Yano M. 2009. Detection of a quantitative trait locus controlling carbon isotope discrimination and its contribution to stomatal conductance in japonica rice. Theor Appl Genet, 118(7): 1401–1410. Takasaki H, Maruyama K, Kidokoro S, Ito Y, Fujita Y, Shinozaki K, Yamaguchi-Shinozaki K, Nakashima K. 2010. The abiotic stress-responsive NAC-type transcription factor OsNAC5 regulates stress-inducible genes and stress tolerance in rice. Mol Genet Genom, 284(3): 173–183. Teng K Q, Li J Z, Liu L, Han Y C, Du Y X, Zhang J, Sun H Z, Zhao Q Z. 2014. Exogenous ABA induces drought tolerance in upland rice: The role of chloroplast and ABA biosynthesisrelated gene expression on photosystem II during PEG stress. Acta Physiol Plant, 36(8): 2219–2227. Thapa G, Dey M, Sahoo L, Panda S K. 2011. An insight into the

Veena PANDEY, et al. Acclimation and Tolerance Strategies of Rice under Drought Stress drought stress induced alterations in plants. Biol Plant, 55(4): 603–613. This D, Comstock J, Courtois B, Xu Y B, Ahmadi N, Vonhof W M, Fleet C, Setter T, McCouch S. 2010. Genetic analysis of water use efficiency in rice (Oryza sativa L.) at the leaf level. Rice, 3(1): 72–86. Tripathy J N, Zhang J X, Robin S, Nguyen T T, Nguyen H T. 2000. QTLs for cell-membrane stability mapped in rice (Oryza sativa L.) under drought stress. Theor Appl Genet, 100(8): 1197–1202. Turner N C, O’Toole J C, Cruz R T, Namuco O S, Ahmad S. 1986. Responses of seven diverse rice cultivars to water deficits: I. Stress development, canopy temperature, leaf rolling and growth. Field Crops Res, 13: 257–271. 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 Biotechnol, 17(2): 113–122. Usman M, Raheem Z F, Ahsan T, Iqbal A, Sarfaraz Z N, Haq Z. 2013. Morphological, physiological and biochemical attributes as indicators for drought tolerance in rice (Oryza sativa L.). Eur J Biol Sci, 5(1): 23–28. Vajrabhaya M, Kumpun W, Chadchawan S. 2001. The solute accumulation: The mechanism for drought tolerance in RD23 rice (Oryza sativa L.) lines. Sci Asia, 27: 93–97. Venuprasad R, Lafitte H R, Atlin G N. 2007. Response to direct selection for grain yield under drought stress in rice. Crop Sci, 47(1): 285–293. Venuprasad R, Impa S M, Vowda Gowda R P, Atlin G N, Serraj R. 2011. Rice near-isogenic-lines (NILs) contrasting for grain yield under lowland drought stress. Field Crops Res, 123(1): 38–46. Verbruggen N, Hermans C. 2008. Proline accumulation in plants: A review. Amino Acids, 35(4): 753–759. Wang F Z, Wang Q B, Kwon S Y, Kwak S S, Su W A. 2005. Enhanced drought tolerance of transgenic rice plants expressing a pea manganese superoxide dismutase. J Plant Physiol, 162(4): 465–472. Wang H, Yamauchi A. 2006. Growth and function of roots under abiotic stress in soil. In: Huang B R. Plant-Environment Interactions. 3rd edn. New York: CRC Press: 271–320. Wang J H, Geng L H, Zhang C M. 2012. Research on the weak signal detecting technique for crop water stress based on wavelet denoising. Adv Mat Res, 424/425: 966–970. Wang S X, Xia S T, Peng K Q, Kuang F C, Yong C, Xiao L T. 2007. Effects of formulated fertilizer synergist on abscisic acid accumulation, proline content and photosynthetic characteristics of rice under drought. Rice Sci, 14(1): 42–48. Xiang Y, Tang N, Du H, Ye H Y, Xiong L Z. 2008. Characterization of OsbZIP23 as a key player of the basic leucine zipper transcription factor family for conferring abscisic acid sensitivity and salinity and drought tolerance in rice. Plant Physiol, 148(4): 1938–1952. Xiong J H, Fu B Y, Xu H X, Li Y S. 2010. Proteomic analysis of PEG-simulated drought stress responsive proteins of rice leaves

161

using a pyramiding rice line at the seedling stage. Bot Stud, 51(2): 137–145. Xu Y B, This D, Pausch R C, Vonhof W M, Coburn J R, Comstock J P, McCouch S R. 2009. Leaf-level water use efficiency determined by carbon isotope discrimination in rice seedlings: Genetic variation associated with population structure and QTL mapping. Theor Appl Genet, 118(6): 1065–1081. Yambao E B, Ingram K T, Real J G. 1992. Root xylem influence on the water relations and drought resistance of rice. J Exp Bot, 43(7): 925–932. Yang J C, Zhang J H, Liu K, Wang Z Q, Liu L J. 2007. Involvement of polyamines in the drought resistance of rice. J Exp Bot, 58(6): 1545–1555. Yang P M, Huang Q C, Qin G Y, Zhao S P, Zhou J G. 2014. Different drought-stress responses in photosynthesis and reactive oxygen metabolism between autotetraploid and diploid rice. Photosynthetica, 52(2): 193–202. Ye N H, Zhu G H, Liu Y G, Li Y X, Zhang J H. 2011. ABA controls H2O2 accumulation through the induction of OsCATB in rice leaves under water stress. Plant Cell Physiol, 52(4): 689–698. Yue B, Xue W Y, Luo L J, Xing Y Z. 2008. Identification of quantitative trait loci for four morphologic traits under water stress in rice (Oryza sativa L.). J Genet Genom, 35(9): 569–575. Zhang Y S, Luo L J, Liu T M, Xu C G, Xing Y Z. 2009. Four rice QTL controlling number of spikelets per panicle expressed the characteristics of single mendelian gene in near isogenic backgrounds. Theor Appl Genet, 118(6): 1035–1044. Zhang Z J, Li F, Li D J, Zhang H W, Huang R F. 2010. Expression of ethylene response factor JERF1 in rice improves tolerance to drought. Planta, 232(3): 765–774. Zhao B Z, Kondo M, Maeda M, Ozaki Y, Zhang J B. 2004. Wateruse efficiency and carbon isotope discrimination in two cultivars of upland rice during different developmental stages under three water regimes. Plant Soil, 261(1/2): 61–75. Zheng X N, Chen B, Lu G J, Han B. 2009. Overexpression of a NAC transcription factor enhances rice drought and salt tolerance. Biochem Biophys Res Commun, 379(4): 985–989. Zhou B Y, Ding Z S, Zhao M. 2011. Alleviation of drought stress inhibition on photosynthesis by overexpression of PEPC in rice. Acta Agron Sin, 37(1): 112–118. (in Chinese with English abstract) Zhou L, Xu H, Mischke S, Meinhardt L W, Zhang D P, Zhu X J, Li X H, Fang W P. 2014. Exogenous abscisic acid significantly affects proteome in tea plant (Camellia sinensis) exposed to drought stress. Hort Res, 1: 14029. Zhou W, Li Y, Zhao B C, Ge R C, Shen Y Z, Wang G, Huang Z J. 2009. Overexpression of TaSTRG gene improves salt and drought tolerance in rice. J Plant Physiol, 166(15): 1660–1671. 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): 1207–1217. Zhu J K. 2002. Salt and drought stress signal transduction in plants. Annu Rev Plant Biol, 53: 247–273.

Suggest Documents