Emerging Role of Osmolytes in Enhancing Abiotic Stress Tolerance in Rice

CHAPTER

EMERGING ROLE OF OSMOLYTES IN ENHANCING ABIOTIC STRESS TOLERANCE IN RICE

33

Mirza Hasanuzzaman1, Taufika I. Anee1, Tasnim F. Bhuiyan2, Kamrun Nahar2 and Masayuki Fujita3 1

Department of Agronomy, Faculty of Agriculture, Sher-e-Bangla Agricultural University, Dhaka, Bangladesh 2 Department of Agricultural Botany, Faculty of Agriculture, Sher-e-Bangla Agricultural University, Dhaka, Bangladesh 3Laboratory of Plant Stress Responses, Faculty of Agriculture, Kagawa University, Kagawa, Japan

33.1 INTRODUCTION In the era of climate change, the various abiotic stresses are being considered as the most complex environmental constraints restricting crop production worldwide. Crop yield losses of about 50% of the total crop yield have been accounted, due to the prevailing abiotic stresses (Acquaah, 2007; Nahar et al., 2016a,b,c). The alterations in the morphology, physiology, biochemistry, and even molecular mechanisms of plants affected by abiotic stress lead to a substantial reduction in plant growth and productivity. However, depending on the type of stressor, duration, magnitude, crop species, growth stage, as well as other environmental factors the intensity of effects may vary (Hasanuzzaman et al., 2012). In addition, plants grown in nature can never be considered as absolutely abiotic stress free. So, this is a crucial time to be concerned about the possible ways of preventing the harmful effects caused by abiotic stress to protect from the yield losses of many important crops including rice (Oryza spp.). Rice is consumed as a staple food by a large portion of the world population especially in Asia. More than three billion people around the world depend on rice for the major share of their daily calorie intake (Pandey and Shukla, 2015). As the world climate is changing, it is negatively affecting the rice yield worldwide (Ray et al., 2015) is estimated to be about in 53% of rice growing areas. Among all the abiotic stresses, drought stress alone has been accounted for affecting about 23 million hectares of rainfed rice (Serraj et al., 2011). Saline soils or salinity conditions are also reported to severely affect rice growth and yield (Rahman et al., 2017). Other environmental stress conditions like toxic metal/metalloids and extreme temperatures also account for a significant reduction in rice yields (Cao et al., 2013; Wang et al., 2016). However, to survive the stress conditions plants themselves have some inbuilt defense mechanisms and other exogenous techniques have been revealed by researchers. The introduction of stress-tolerant crop cultivars is the most auspicious way of surviving these constraints and to produce these types of tolerant crops several bioengineering mechanisms

Advances in Rice Research for Abiotic Stress Tolerance. DOI: https://doi.org/10.1016/B978-0-12-814332-2.00033-2 Copyright © 2019 Elsevier Inc. All rights reserved.

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involved in stress signaling are being adopted. One example of these kinds of manipulations is osmotic adjustment, as osmolytes are naturally accumulated in plants as a response of stress. Osmolytes or osmoprotectants are highly soluble, nontoxic, electrically neutral, low molecular weight compounds which are very small in size but capable of retaining the osmotic balance and protecting membranes, proteins, and other biomolecules under adverse conditions (Slama et al., 2015). They are classified into three types based on their chemical properties and those are betaines, amino acids, and nonreducing sugars, and sugar alcohols. Examples of some betaines are glycine betaine (GB), β-alanine betaine, choline-O-sulfate, etc., amino acids are proline (Pro), pipecolic acid, ectoine, etc., and nonreducing sugars and sugar alcohols are trehalose (Tre), sorbitol, mannitol, inositol, etc. (Slama et al., 2015; Nahar et al., 2016a). Diverse studies have been done to demonstrate the role of osmoprotective compounds in minimizing the abiotic stress damage and enhancing the stress tolerance of most of the cultivated crops including rice (Zeid, 2009; Rezaei et al., 2012; Hasanuzzaman et al., 2014a; Raza et al., 2014). This chapter has been designed to provide information and discuss the apparent and promising roles of the most familiar osmoprotective compounds in conferring abiotic stress tolerance in rice.

33.2 NATURE, TYPES, AND FUNCTIONS OF OSMOLYTES IN PLANT BIOLOGY Plants encounter various unavoidable abiotic stresses in their natural habitat. To combat the harmful effects of environmental stresses, plants have developed advanced adaptive mechanisms. To survive under extreme osmotic and oxidative stress, one such common approach adopted by plants is the production and accumulation of organic solutes referred to as compatible solutes or osmolytes (Hasanuzzaman et al., 2014a; Per et al., 2017). Osmolytes are low molecular weight, highly soluble, small organic compounds which are nontoxic to intracellular metabolisms at high cellular concentrations (Nahar et al., 2016a). Naturally, 5 50 μmol g21 FW of osmolytes can be synthesized by plants and usually remains in the cytosol, chloroplast and other components of the cytoplasm (Rhodes and Hanson, 1993). Osmolytes are also commonly called osmoprotectants due to their functions in protecting cellular components against dehydration injury. Diverse types of osmoprotective compounds have been identified. Osmolytes predominantly include amino acids (Pro, ectoine, pipecolic acid, γ-aminobutyric acids, etc.,), betaines (GB, β-alanine betaine, choline-O-sulfate), sugars (glucose, fructose, sucrose, Tre, raffinose, fructans), sugar alcohols or polyols (sorbitol, mannitol, glycerol, inositol), and tertiary sulfonium compound dimethylsulfoniopropionate (DMSP) (Ashraf and Foolad, 2007). However, there are three well recognized types of osmoprotectants based on chemical composition: (1) the amino acids Pro and ectoine, (2) quaternary ammonium compounds such as GB, β-alanine betaine, choline, and DMSP, and (3) polyols, sugars, and sugar alcohols such as Tre, sorbitol, and mannitol, etc. (Nahar et al., 2016a). Depending on the types of stress, environmental conditions, and plant species the concentration and structure of the accumulated solutes varies considerably (Kumar, 2009; Evers et al., 2010). In addition, growing conditions and nutritional and environmental factors also regulate the cellular compartmentalization of osmolytes (Ashraf and Foolad, 2007).

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The major role of osmolytes in plants is cellular osmotic regulation (Hasegawa et al., 2000). In response to stresses, osmolytes contribute to maintaining cell turgidity through osmotic adjustment, protecting cellular components, replacing inorganic ions, and alleviating ionic toxicity. Thus, osmolytes develop stress tolerance by stabilizing proteins, protecting biological membranes and other cellular structures, detoxifying the accelerated production of reactive oxygen species (ROS), and maintaining cellular redox balance (Krasensky and Jonak, 2012). Osmolytes perform vital functions in the regulation of proper protein folding which facilitates protein functioning and mediates stress signaling (Rosgen, 2007). Osmolytes also help in the stabilization of photosynthetic machineries and thylakoid membranes, thereby, stabilizing photosynthesis, mitochondria, and metabolisms (Alam et al., 2014). Osmoprotective compounds through directly scavenging toxic ROS, protect antioxidant enzymes, thus, strengthen the overall antioxidant defense system in plants (Matysik et al., 2002; Hasanuzzaman et al., 2014a). Moreover, osmolytes have functions in the activation of defense responsive genes under various stresses (Banu et al., 2009).

33.2.1 PROLINE Among the widely distributed osmolytes, Pro is the most fundamental one and is predominantly found in higher plants. Being an amino acid and characteristically rigid, it performs vital roles in response to various kinds of abiotic stress through adaptation, signaling, and recovery mechanisms (Kavi Kishor et al., 2005; Per et al., 2017). Pro is found to accumulate in the chloroplast and cytoplasm and when plants are exposed to stress, considerably elevated accumulation of Pro is associated with stress tolerance (Ahmad et al., 2016). Under stressful environmental conditions, higher Pro accumulation provides protection to cells through osmotic adjustment and toxic free radical scavenging (Kaur and Asthir, 2015). Besides osmoregulation, Pro acts as an efficient molecular chaperone, stabilizing the subcellular components including photosystem II (PS II), membranes, proteins, and enzymes (Banu et al., 2009). For example, with higher Pro levels, protein aggregation was inhibited and various enzymes were stabilized under high temperature, toxic metal, osmotic, and arsenic stresses, respectively (Rajendrakumar et al., 1994; Sharma and Dubey, 2005; Mishra and Dubey, 2006). Pro has been proposed as an antioxidative defense molecule which efficiently scavenges toxic ROS, confers detoxification processes, and reduces oxidative damages through stabilizing antioxidant enzymes (De Carvalho et al., 2013). However, research suggests that Pro is incapable of detoxifying the other ROS, except hydroxyl radical, which may warrant further investigation (Signorelli et al., 2014). Accelerated Pro under abiotic stress effectively participates in the regulation of the cellular redox state, maintaining the cytosolic pH level, and thus, balancing the Nicotinamide adenine dinucleotide phosphate (NADP1)/ NADPH ratios for proper metabolism. Pro also has a role in decreasing photoinhibition and the destruction of photosynthetic machineries (Sz´ekely et al., 2008; Hayat et al., 2012). Furthermore, Pro is a protein precursor, energy restorer, and a cellular N/C source (Nahar et al. 2016a). Pro helps to maintain cellular ionic homeostasis and also induces proper K1/Na1 ratio under salt stress (Nounjan et al., 2012). In addition, Pro appeared to function as a signaling molecule which uplifted defense responsive genes (Banu et al., 2009). Through uplifting the tolerant genes, Pro alleviated the damaging effects of multiple stresses including salt (Teh et al., 2015) and drought (Moustakas et al., 2011).

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CHAPTER 33 EMERGING ROLE OF OSMOLYTES IN ENHANCING ABIOTIC

33.2.2 GLYCINE BETAINE The quaternary ammonium compound GB (N,N,N-trimethylglycine), also referred to as original betaine, is a methylated glycine derivative. Among the betaines, GB is the most abundant in plants and was excessively produced in response to dehydration caused by different abiotic stresses like drought, salinity, and extreme temperatures (Chen and Murata, 2011; Rasheed et al., 2014). Some plant species including Beta vulgaris, Spinacia oleracea, Zea mays, and Hordeum vulgare, referred to as GB accumulators, produce GB in their leaves subjected to stress and render tolerance from the damaging effects of stress (Nyyssola et al., 2000). GB predominantly occurs in the chloroplast where it maintains photosynthetic regulation by protecting the thylakoid membrane and osmotic adjustment (Zhang et al., 2008). GB contributes to the decreased accumulation and detoxification of ROS by restoring photosynthesis and reducing oxidative stress (Chen and Murata, 2008). It takes part to stabilize the membranes and macromolecules. It is also involved in the stabilization and protection of photosynthetic components such as Ribulose-1,5-bisphosphate carboxylase/oxygenase, PS II, and quaternary enzyme and protein complex structures under environmental stress (Yang et al., 2008). GB was found to perform as a chaperon in induced protein disaggregation (Diamant et al., 2003). In addition, GB can confer stress tolerance in low concentrations and it acts to activate defense responsive genes with stress protection (Chen and Murata, 2008). It was demonstrated that GB has specific protective effects on plant reproductive organs under water deficit and cold stress (Chen and Murata, 2008; Sakamoto and Murata, 2001). However, insufficient endogenous GB accumulation in plants, has developed its demand to be used externally as stress protector (Cha-um et al., 2013; Hasanuzzaman et al., 2014a).

33.2.3 TREHALOSE A disaccharide sugar of nonreducing category known as Tre and α-α-(1 - 1) glycosidic linkage between the two glucose molecules (α-D-glucopyranosyl-1 and 1-α-D-glucopyranoside) results in the formation of this Tre sugar. It has resistance to heat and acidic hydrolysis due to its reducing molecular properties, and thus, it also shows stability under heat and desiccation (Richards et al., 2002). Under extreme desiccation stress, Tre accumulation was detectable in Selaginella lepidophylla, and Myrothamnus flabellifolius renaissance plants (Scott, 2000). In plants, although present in trace amounts, Tre plays a tremendous role in the mitigation of abiotic stresses like cold, heat, desiccation, and salt. Tre confers stress tolerance by activating the signal transduction pathways and synthesizing different kinds of proteins, osmolytes, and photosynthetic pigments (Roelofs et al., 2008). Tre has the capacity to convert into a glassy state or replace the water molecules under dehydration or desiccation stress. Thus, it efficiently stabilizes the membranes and biomolecules by rehydrating them (Crowe and Crowe, 2000; Richards et al., 2002). Tre plays a vital role in the regulation of embryo maturation, vegetation, and reproduction of plants. Theerakulpinsut and Gunnula (2012) found that exogenous Tre application alleviated salt-induced damages by increasing endogenous Tre levels.

33.2.4 SUGARS AND SUGAR ALCOHOLS Sugars such as glucose, fructose, sucrose, Tre, raffinose family oligosaccharides (RFOs) (raffinose, stachyose, and verbascose), and fructans, etc., are potentially involved in tolerance to abiotic stress

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681

(Drennan et al., 1993; Keunen et al., 2013). As osmolytes, they participated in osmotic adjustment and membrane stabilization under drought stress (Lokhande and Suprasanna, 2012). Reports have shown the vital roles of glucose, sucrose, fructose, and fructans against salinity and water deficit stresses (Kerepesi and Galiba, 2000; Murakeo¨zy et al., 2003). Sugars play important regulatory functions for gene expression, like those involved in essential metabolic processes including photosynthesis, respiration, and carbohydrate metabolism (Hare et al., 1998). Tre, being a sugar of great importance contributes remarkably to conferring stress protection (Delorge et al., 2014). The accumulation of fructan improves drought stress tolerance. It can also protect plants from dehydration and freezing (Olien and Clark, 1995; Pilon-Smits et al., 1995). RFOs showed a protective function against dehydration, cold, and heat stresses through the generation of energy, thus, maintaining cellular integrity (ElSayed et al., 2014). Linear sugar alcohols such as mannitol, sorbitol, inositol, xylitol, ribitol, and the cyclic pinitol, are called polyols, are highly effective at mitigating abiotic stresses as well as osmotic and oxidative damages. Under drought and salinity, mannitol, sorbitol, and inositol, reduced damaging stress effects through maintaining osmotic balance and redox state (Williamson et al., 2002; Tari et al., 2010). Polyols including myo-inositol, D-pinitol, and D-ononitol are effective ROS scavengers and reported to scavenge hydroxyl radical under stress (Gill and Tuteja, 2010). Enhanced tolerance to abiotic stress was documented after increased accumulation of myo-inositol (Tan et al., 2013). Sugars also ensure protection by activating signal transduction pathways (Radomiljac et al., 2013). The overexpression of mtlD led to salt tolerance through mannitol accumulation in a number of plants such as Triticum aestivum (Abebe et al., 2003), Populus tomentosa (Hu et al., 2005), and Pinus radiata (Tang et al., 2005). In another report the overaccumulation of pinitol was found in halophytic wild rice and inferred salt tolerance through the activation of the inositol methyl transferase 1 (PcIMT1) gene (Sengupta et al., 2008).

33.2.5 OTHERS Besides Pro, higher plants subjected to abiotic stresses accumulate amino acid group osmolytes, including arginine, alanine, glycine; amides, including asparagine and glutamine; and nonprotein amino acids, such as γ-aminobutyric acid (GABA), ornithine (Orn), citrulline, and pipecolic acid (Mansour, 2000). Under numerous adverse environmental conditions the rapid accumulation of elevated levels of GABA has been evident (Renault et al., 2010) and stress (salinity, flooding) protection was associated with efficient GABA induced osmoregulation, C:N balance, and detoxification of ROS (Renault et al., 2010; Song et al., 2010; Liu et al., 2011). Polyamines such as putrescine, spermidine, and spermine are correlated positively with stress (salt, toxic metal, cold, drought) tolerance by facilitating membrane protection and osmoregulation (Groppa and Benavides, 2008; Nahar et al., 2016b,c). Polyamines imparted salt and Cd stress tolerance in Vigna radiata L. by upregulating the antioxidant defense and glyoxalase systems and down-regulating toxic ROS and methylglyoxal (MG) overproduction and damages (Nahar et al., 2016b,c). Different forms of betaines such as Pro betaine, hydroxyproline betaine, choline-O-sulfate, etc., are important quaternary ammonium compounds which efficiently protect plants under abiotic stress (Vinocur and Altman, 2005; Koyro et al., 2012). A tertiary sulfonium compound named DMSP act mainly as an excess sulfur detoxifier, an antioxidant molecule as well as an osmoregulator. In Spartina alterniflora, DMSP was greatly accumulated in leaf tissues and provided osmoprotection (Otte et al., 2004).

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33.3 OSMOLYTE SYNTHESIS AND METABOLISM IN PLANTS 33.3.1 PROLINE There are a number of proposed pathways for Pro biosynthesis in higher plants. Pro biosynthesis enzymes are localized in the cytosol and chloroplasts and so, the Pro biosynthesis process is proposed to occur in these sites. In most higher plants (Fig. 33.1), glutamate is first converted into γ-glutamyl phosphate, then into intermediate glutamic semialdehyde (GSA) and then converted to pyrroline-5-carboxylate (P5C). The Δ1-P5C synthetase (P5CS) catalyzing the reaction. This P5C is catalyzed by Δ1-P5C reductase in order to biosynthesize Pro (Singh et al., 2015; Van Oosten et al., 2016). Pro can also be biosynthesized from ornithine (Orn). Orn is converted into GSA, then P5C and then into Pro. This Orn can be converted to α-keto-δ-aminovalerate (KAV) catalyzes by Orn δ-aminotransferase. The KAV is gradually converted to pyrroline 2-carboxylase (P2C) and at last P2C is catalyzed by P2C reductase to generate Pro (Kavi Kishor et al., 2005). The interaction between plants’ endogenous sense and environmental factors regulates Pro biosynthesis or transportation to the site of action of Pro (Verslues and Sharma, 2010). The upregulation of Pro has been demonstrated to recover drought injury and maintain better cellular water status in several studies (Nahar et al., 2015a, 2017a). Without drought stress, up-regulation of Pro under different other stresses like high temperature, salinity, low temperature, and toxic metal stresses showed positive correlation with the tolerance of those stresses. In these studies, the results evidenced that Pro not only acted as an osmoprotectant to alleviate physiological drought induced by these stresses and maintained better water status, but it also acted as an ROS scavenger to decrease oxidative stress (Nahar et al., 2015b,c,d; 2016a,c; 2017a,b). Pro transportation from the site of biosynthesis to the site of requirement is vital for plant adaptation to environmental stresses. Inter- and intracellular transportation are vital in this case. Decreased water potential caused the accumulation of Pro in the elongation zone of Z. mays roots due to increased transport rather than biosynthesis which enhanced tolerance (Verslues and Sharp, 1999). Pro in grapevine increased due to higher transport of Pro but not due to the expression of the P5CS gene (Stines et al., 1999). The enhanced biosynthesis and increased transport of Pro from the stems and roots increased Pro levels in the leaves and new buds which helped Periploca sepium recover from severe drought stress (An et al., 2013). In halophyte Limonium latifolium, Pro was sequestered to the vacuoles in nonstressed plants. In contrast, in salt-stressed plants, a high Pro content was detected in the cytosol, suggesting the importance of de-novo Pro biosynthesis as well as transport for Pro accumulation which were also correlated with salt tolerance (Gagneul et al., 2007). Compartmentalization of Pro biosynthesis and degradation in the cytosol, chloroplast, and mitochondria are also an important part of Pro metabolism to modulate Pro homeostasis in cells. Higher Pro biosynthesis in the chloroplast regulates redox balance and smoothens electron transport in the electron transport chain during stress (Hancock et al., 2016). Pro catabolism in the mitochondria can modulate oxidative respiration and energy production to recommence growth after stress. Pro regulates cytoplasmic acidosis and maintains appropriate NADP1/NADPH ratio compatible with cell metabolism (Filippou et al., 2014). Pro is a metabolic signal altering developmental processes (Kim et al., 2017). Pro catabolism has been reported in the mitochondria where Pro dehydrogenase or Pro oxidase (POX) generates P5C from Pro, and P5C dehydrogenase changes P5C to glutamate. Pro accumulation can be modulated by transferring the Pro content or accumulation modulated by

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FIGURE 33.1 Pathway of proline biosynthesis in higher plants. P5CS, Δ1-Pyrroline-5-carboxylate synthetase; GK, γ-Glutamyl kinase; GPR, γ-Glutamyl phosphate reductase; P5CR, Pyrroline-5-carboxylate synthetase; δ-OAT, Ornithine δ-aminotransferase; P2CR, Pyrroline 2-carboxylase. Modified with permission from Springer. Nahar, K., Hasanuzzaman, M., Fujita, M., 2016a. Roles of osmolytes in plant adaptation to drought and salinity. In: Iqbal, N., Nazar, R., Khan, N.A., (Eds.), Osmolytes and Plants Acclimation to Changing: Emerging Omics Technologies. Springer, New Delhi, pp. 37 68.

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genes liable for biosynthesis or degradation. Higher expressions of KvP5CS1 and KvProT and lower expression of KvPDH for Pro catabolism were responsible for Pro accumulation under salt stress (Wang et al., 2015). HtP5CS enzyme activity during NaCl stress along with HtOAT and HtPDH were repressed in salt imposed Jerusalem artichoke (Helianthus tuberosus L.) plantlets (Huang et al., 2013). Pro content decreases when P5CS in Arabidopsis is knocked-out, thereby, decreasing Pro synthesis (Sz´ekely et al., 2008). Antisense suppression boosted Pro degradation which helped Arabidopsis thaliana plants become more tolerant to cold and salt stress (Nanjo et al., 1999).

33.3.2 GLYCINE BETAINE In higher plants, GB is biosynthesized in the chloroplast. GB protects the thylakoid membrane of chloroplasts (Genard et al., 1991). GB is biosynthesized from choline (Fig. 33.2) in higher plants. Choline is oxidized by a ferredoxin-dependent choline monooxygenase. Betaine aldehyde is catalyzed by betaine aldehyde dehydrogenase (BADH) incorporating NAD1 for generating GB. Studies evidenced that the overexpression of BADH enhanced GB biosynthesis and improved osmotolerance (Sakamoto and Murata, 2001; Sulpice et al., 2003). The accumulation of GB in various plants like sugar beet, spinach, barley, wheat, sorghum, and rice improved stress tolerance (Weimberg et al., 1984; McCue and Hanson, 1990; Rhodes and Hanson, 1993; Yang et al., 2003; Hasanuzzaman et al., 2014b). The exogenous addition of GB or its precursor choline was added to the plant growing media and as a result the endogenous level of GB increased (Huang et al., 2000; Hasanuzzaman et al., 2014b). For some plants tolerance of genotypes is positively correlated to GB accumulation. But, for some plants GB accumulation is not positively correlated to tolerance (Ashraf and Foolad, 2007). Increased levels of GB did not alleviate the adverse effects of salt stress in Triticum, Agropyron, and Elymus (Wyn Jones et al., 1984). Accumulation of choline and betaine was higher in salt-sensitive rather than salt-tolerant lines of Egyptian clover on exposure to salinity (Varshney et al., 1988). Plant species which do not naturally produce GB, when engineered with genes for overproducing GB showed improved adaptation to salt, cold, drought, or high temperature stress. Rice, mustard, Arabidopsis, and tobacco are some examples of such plants (Rhodes and Hanson, 1993). Enzymes for GB synthesis were exploited to engineer tobacco and other plants that were short of GB which showed some extent of stress tolerance. GB is not substantially degraded in plants (Nuccio et al., 1998) which results in GB catabolism which is a less vital issue while engineering GB plants (Rontein et al., 2002). The available research findings about GB biosynthesis in plants showed differential responses with the differences in plant species, cultivars, or stressors.

33.3.3 TREHALOSE There are several pathways for Tre biosynthesis. But in plants, the most studied one is the Tre phosphate synthase (TPS)—Tre phosphate phosphatase (TPP) route (Fig. 33.3). Tre-6-phosphate (T6P) is synthesized from Uridine diphosphate (UDP)-glucose to glucose-6-phosphate where the enzyme TPS catalyzes the reaction. Later on the phosphate group of T6P is hydrolyzed by TPP to synthesize Tre (Avonce et al., 2006). This pathway was demonstrated in S. lepidophylla and A. thaliana (Bl´azquez et al., 1998; Zentella et al., 1999).

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FIGURE 33.2 Glycine betaine biosynthesis pathway in plants. CMO, Choline monooxygenase; BADH, betaine aldehyde dehydrogenase Modified with permission from Springer. Nahar, K., Hasanuzzaman, M., Fujita, M., 2016a. Roles of osmolytes in plant adaptation to drought and salinity. In: Iqbal, N., Nazar, R., Khan, N.A., (Eds.), Osmolytes and Plants Acclimation to Changing: Emerging Omics Technologies. Springer, New Delhi, pp. 37 68.

The UDP-glucose and glucose-6-phosphate are vital molecules from which major cellular functions are generated. In addition, respiratory energy is obtained from these. Carbon skeletons for the structural constituents of cellulose and cell wall polysaccharides, starch, lipids, proteins, and sucrose are received from these compounds. Thus, Tre metabolism is vital for plant growth and development. Synthesis of T6P and Tre can potentially act as an effective indicator of the G6P and UDPG pool size (Paul et al., 2008). Tre is a nonreducing disaccharide that acts as an

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FIGURE 33.3 Trehalose biosynthesis route in higher plants. TPS, Trehalose phosphate synthase; TPP, Trehalose phosphate phosphatase Modified with permission from Springer. Nahar, K., Hasanuzzaman, M., Fujita, M., 2016a. Roles of osmolytes in plant adaptation to drought and salinity. In: Iqbal, N., Nazar, R., Khan, N.A., (Eds.), Osmolytes and Plants Acclimation to Changing: Emerging Omics Technologies. Springer, New Delhi, pp. 37 68.

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osmoprotectant (Avonce et al., 2006). Trehalase is accountable for the catabolism of Tre which is converted into two α-D-glucose molecules (Avonce et al., 2006). Tre in plants regulates carbon metabolism and hormone signals to various stresses (Schluepmann et al., 2003; Avonce et al., 2004). Transgenic management of Tre metabolism in different plants has been reported to exert positive effects on different plant species under different stress conditions. Rice plants encoding OtsA and OtsB genes showed better phenotype and tolerance against drought, salinity, and low temperature stress (Garg et al., 2002). Arabidopsis expressing a yeast chimaeric gene coding for the TPS performed better under drought, salinity, and low and high temperature stress (Miranda et al., 2007; Iturriaga et al., 2009). Potato expressing TPS1 gene showed drought tolerance (Kondr´ak et al., 2011).

33.4 OSMOLYTE-INDUCED ABIOTIC STRESS PROTECTION Researchers around the world have been discovering new ways for both animal and plant kingdoms to cope with or fight against various abiotic stress conditions. One of these strategies is the use of osmolytes for conferring stress tolerance. Besides performing osmoregulatory actions as a primary response, osmolytes have the capability to protect the membrane, photosynthetic and mitochondrial structures, to diminish ionic toxicity and to detoxify toxic molecules like ROS and MG (Nahar et al., 2016a). Those are the mechanisms by which these osmoprotective compounds enable a plant to survive under adverse environmental conditions. The mechanism of performing a signaling role is another important feature of osmoprotectants though it has not been well explained yet. However, osmolyte-induced protective roles against different types of abiotic stresses have been demonstrated in many crop species including rice. We will discuss the role of different osmoprotective compounds in conferring abiotic stress tolerance in rice (Fig. 33.4).

33.4.1 SALINITY Both osmotic stress and ionic toxicity occur under saline conditions which results in reduced seed germination (%) and seedling growth, impaired development and reproduction, hampered metabolic processes, delayed maturity, and even the death of plants (Nahar et al., 2016a). The generation of ROS is another harsh outcome of salt stress which causes acute cellular damage by oxidizing the lipids, proteins, and nucleic acids (Apel and Hirt, 2004). Except halophytes, salinity negatively affects most of the crops survival including rice. In general, rice is considered to be a salt-sensitive type of crop though it can withstand some extent of salt water depending on the species and growth stage (Rahman et al., 2017). However, several salt stress tolerance mechanisms have been introduced into rice plants including the introduction of tolerant cultivars through genetic engineering and the use of different phytoprotectants (e.g., osmoprotectants, plant hormones, signaling molecules, etc.). Osmoprotectants are generally synthesized and accumulated in plant cells under stressful conditions in order to survive salt-induced osmotic stress through the stabilization of proteins and membranes besides maintaining osmotic balance (Rahman et al., 2017). The exogenous application of several osmoprotectants like Pro, Tre, GB, and sorbitol have been evidenced by many studies to have notable roles in conferring protection against salt stress (Table 33.1).

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Salinity

Osmotic stress

Drought

Toxic metal

Oxidative stress

Ionic stress

Heat

Seed soaking

Foliar application Application of osmolytes

With irrigation

Hydroponic medium

Detoxification of ROS and MG

Osmoregulation

Protection of other biomolecules

Stabilization of protein and membrane

Reduction of ionic toxicity

Abiotic stress tolerance FIGURE 33.4 Mechanism of osmolyte-induced abiotic stress protection.

Teh et al. (2016b) used two Malaysian rice (MR) cultivars (MR 220 and MR 253) which were grown under in vitro conditions to study the protective roles of Pro (5 and 10 mM) against salt stress (150 mM). They recorded after 30 days of callus culture that, Pro application has positive effects on rice shoots which helps reduce salt-induced damages. Seeds from the same cultivars were soaked in Pro for 12 h and when exposed to high concentrations of salt (400 mM) and grown in petri dishes in a growth chamber, the ameliorative effects on salt stress damage were evidenced (Deivanai et al., 2011). In a pot experiment with one salt-sensitive (BRRI dhan29) and another moderately salt-tolerant cultivar (BRRI dhan47) it was observed that higher doses of Pro (25 and 50 mM) had beneficial effects under saline conditions mostly in the salt-sensitive cultivar by enhancing growth and grain yield, maintaining higher K1/Na1 ratio, and increasing Pro

Table 33.1 Protective Effects of Exogenous Osmolytes in Mitigating Abiotic Stress-Induced Damages in O. sativa Cultivars

Stress Dose and Duration

Doses of Osmolytes

Protective Effects

References Theerakulpisut and Phongngarm (2013) Wutipraditkul et al. (2015)

PK and PT60

170 mM NaCl; 10 days

10 mM Tre

• Enhanced growth and chlorophyll content

KDML105

160 mM NaCl; 3 days

1 mM GB and 30 mM Pro

Nipponbare and Pokkali PK and KDML105

100 mM NaCl; 7 days 200 mM NaCl; 6 days

1 mM Pro or 1 mM GB; 12 h

KDML105

170 mM NaCl; 24 h

5 and 10 mM Tre and 5 and 10 mM sorbitol

• Increased photosynthetic pigments and reduced H2O2 • Modulated activity of superoxide dismutase (SOD), catalase (CAT), GR, and ascorbate peroxidase (APX) • Increased FW, chlorophyll content, and K1/Na1 ratio • Reduced SOD and POX activity • Na1/K1 ratio was enhanced by exogenous Pro but reduced by Tre • Reduced malondialdehyde (MDA) and H2O2 contents

Pokkali and IR-28

120 mM NaCl; 7 days

15 mM GB

Nipponbare

25 mM NaCl; 7 days 300 mM NaCl; 48 h

1 or 5 mM Pro and 1 or 5 mM GB; 12 h 5 mM Pro and 5 mM GB

100 mM NaCl; 6 days 25 mM NaCl; 15 days

10 mM Pro and 10 mM Tre

400 mM NaCl

1 mM Pro

BRRI dhan49 and BRRI dhan54 KDML105 BRRI dhan29 and BRRI dhan47 MR 220 and MR232

10 mM Pro and 10 mM Tre

25 mM Pro

• Increased fresh weight (FW), dry weight (DW), and chlorophyll content • Reduced Pro content in IR-28 • Reduced Na1 uptake • Increased relative water content (RWC), chlorophyll and Pro contents • Reduced MDA and H2O2 contents • Enhanced antioxidant enzyme activity • Reduced Na1/K1 ratio • Decreased activity of SOD and POX • Enhanced growth • Increased chlorophyll and ascorbate (AsA) contents • Increased POX and APX activity • Improved growth • Increased chlorophyll, protein and Pro contents

Sobahan et al. (2012) Nounjan and Teerakulpisut (2012) Theerakulpisut and Gunnula (2012) Demiral and Turkan (2006) Sobahan et al. (2009) Hasanuzzaman et al. (2014a)

Nounjan et al. (2012) Bhusan et al. (2016)

Deivanai et al. (2011) (Continued)

Table 33.1 Protective Effects of Exogenous Osmolytes in Mitigating Abiotic Stress-Induced Damages in O. sativa Continued Cultivars

Stress Dose and Duration

Doses of Osmolytes

Protective Effects

References

Giza178 and Giza177

60 mM NaCl; 21 days

25 mM Tre (seed soaking for 12 h)

Abdallah et al. (2016)

MR 220 and MR 253 Nipponbare

150 mM NaCl

5 and 10 mM GB

25 mM NaCl; 14 days 150 mM NaCl; 30 days

1 mM Pro and 1 mM GB; 12 h

• Increased FW, DW, RWC, and photosynthetic pigments • Reduced Pro content and SOD and POX activity • Increased CAT activity • Enhanced FW, DW, and chlorophyll contents • Reduced MDA content • Reduced H2O2 and lipid peroxidation

Bas-385 and Bas-2000

50, 100 and 150 mM NaCl; 14 days

10 and 20 mM Tre

Super-basmati

Drought: 50% FC; 7 days

0.85 and 1.28 mM GB

PT1

Drought: 25% soil water content Drought: 14% soil moisture content Drought: 30 40% FC; 7 days Drought: 50% FC; 4 days

100 mM GB

MR 220 and MR 253

KS-282 and Basmati-385 Transgenic lines 1, 4, 22 and 23 Super-basmati

5 and 10 mM Pro

100 mM GB

10 and 20 mM GB

1.28 mM GB

• Improved growth attributes • Reduced root nitrate ion content and increased NR activity • Improved growth, yield and chlorophyll contents • Reduced MDA and H2O2 and free Pro contents • Declined activity of SOD and peroxidase (POD) • Reduced Na1 uptake • Increased FW, DW, and RWC • Reduced electrolyte leakage, MDA and H2O2 contents • Enhanced antioxidant enzyme activity • Enhanced photosynthetic ability • Increased plant height, panicle length and weight, fertility (%), and hundred grain weight • Increased Pro, sugar and starch contents in both leaves and panicles • Improved yield attributes • Induced different genes involved in stress responses, signal transduction, hormone signaling, and cellular metabolism • Improved seedling FW and DW • Increased leaf RWC and free Pro content • Reduced MDA, H2O2 and electrolyte leakage • Increased SOD, CAT and APX activity

Teh et al. (2016a) Sobahan et al. (2016) Teh et al. (2016b) Shahbaz et al. (2017)

Farooq et al. (2008)

Cha-um et al. (2013) Jalal-ud-Din et al. (2015) Kathuria et al. (2009) Farooq et al. (2010)

F60, F733, and F473

35 and 40 C; 5 h

Endogenous Pro accumulation

Kaybonnet

35 C and 26 C day/night; 4 week 50 C

Endogenous accumulation of Pro, L-glutamic acid, GABA and arginine 1 M of Pro and betaine Endogenous Pro accumulation

• Increased tolerance to high night temperatures

1.823 M of GB

• Reduced the negative effects on grain yield and SS

1.823 M of GB

PR 118

High night temperature; 30 C High night temperature; 27 and 32 C High night temperature; 32 C 42/37 C

PR 116 and PR 118

35/30, 40/35, 45/ 40 C

Enhanced endogenous Pro

Panvel-3 and Sahyadri-3

An increase of 12 C mean temperature High temperature stress 45 and 50 C

Enhanced endogenous Pro

• • • • • • • • • • •

Enhanced endogenous Tre

Hg21; 0.2 mM

2 mM of Pro; 12 h

Hitomebore and IR-28 F60

Cocodrie

Cocodrie

PB-1

PAU-369913-2-1-1 and PR122 Zhonghua 11

1 mM of GABA

Endogenous sucrose accumulation

• Restored leaf photosynthesis • Reduced oxidative damages in tolerant F473 as compared to sensitive F60 cultivar • Enhanced tolerance to heat stress

S´anchez-Reinoso et al. (2014)

• Protected the activity of Rubisco

Dionisio-Sese et al. (2000) AlvaradoSanabria et al. (2017) Mohammed and Tarpley (2011)

• • • • • • •

Increased growth Enhanced antioxidant enzyme activity Decreased heat induced oxidative damages Increased synthesis of osmolytes Improved RWC and photosynthesis Enhanced antioxidant activity Reduced oxidative damages as well as heat stress Provided heat stress tolerance Improved water status Protected membrane Improved heat stress tolerance

Increased rate of photosynthesis Increased synthesis of sugar carbohydrates Rendered higher tolerance to heat stress Reduced SS activity Increased AI activity Enhanced grain development Reduced oxidative damages by scavenging toxic ROS • Chelation of metal and maintaining osmoregulation

El-kereamy et al. (2012)

Mohammed and Tarpley (2009) Nayyar et al. (2014)

Kumar et al. (2012) Kumar et al. (2016) Garg et al. (2002) Sharma and Sharma (2017) Wang et al. (2009)

(Continued)

Table 33.1 Protective Effects of Exogenous Osmolytes in Mitigating Abiotic Stress-Induced Damages in O. sativa Continued Cultivars

Stress Dose and Duration

Doses of Osmolytes

Protective Effects

References

Xiushui 63

Cd; 50 μM

100 μM of GB; 24 h

Cao et al. (2013)

Pant-12 and Malviya-36 Malviya-36 and Pant-12 Malviya-36 and Pant-12 IR-29 and Nonabokra

Al31; 160 μM

1 mM of Pro, GB and sucrose

NiSO4; 200 and 400 μM Ni21; 0 2500 μM CdCl2; 0.1, 0.25, 0.5 and 1.5 mM

Higher endogenous Pro

• Improved growth retardation and lowered lipid peroxidation • Increased FW and DW of shoot and root • Improved chlorophyll contents and antioxidant (SOD, POD) activity • Protected the nitrate reductase enzyme from the damaging effects of Al31 • Prevented desiccation

Higher endogenous Pro

• Protected the RNase enzyme activity

Higher endogenous Pro, reducing sugar, spermine, spermidine

• Higher antioxidant enzymes (APX, GPX, CAT) activity • Higher activity of carotenoids, anthocyanin • Greater protection against oxidative damages • Uplifted nonenzymatic (GSH and GSSG) and enzymatic (SOD, POD, CAT, APX) antioxidants • Enhanced synthesis of soluble sugars. • Higher accumulation and activity of Pro and antioxidant enzymes • Reduced oxidative damages by scavenging toxic ROS • Chelation of metal and maintaining osmoregulation

GXZ and NX-18 Yangliangyou 6 Zhonghua 11

Pb21; 0, 400, 800 and 1200 μM Ni; 10, 50, 100, and 200 μM Hg21; 0.2 mM

Higher endogenous Pro

Higher endogenous Pro 2 mM of Pro; 12 h

Sharma and Dubey (2005) Mishra and Dubey (2013) Maheshwari and Dubey (2007) Roychoudhury et al. (2012)

Ashraf and Tang (2017) Rizwan et al. (2017) Wang et al. (2009)

AI, Acid invertase; GB, Glycine betaine; MR, Malaysian rice; NR, Nitrate reductase; POX, Proline oxidase; Pro, Proline; PT1, Pathumthani 1; ROS, Reactive oxygen species; SS, Sucrose synthase; Tre, Trehalose.

33.4 OSMOLYTE-INDUCED ABIOTIC STRESS PROTECTION

693

accumulation and the antioxidant defense system (Bhusan et al., 2016). Two rice cultivars differing in tolerance levels (salt-sensitive Sakha 103 and salt-tolerant Agami M5) were studied by Abdelgawad et al. (2014) and it was observed that with higher accumulation of Tre, rice seedlings tend to get less affected by salt treatment which denotes the positive role of Tre in improving salt stress tolerance. Rice seedlings grown under 170 mM NaCl containing MS medium showed reduced growth and destruction of photosynthetic pigments which were possible to recover with the supplementation of 10 mM Tre treatment, however, under the same stress conditions 5 mM of neither Tre, Pro or sorbitol, or even 10 mM of Pro or sorbitol could make any remarkable changes when compared with the stressed plants (Theerakulpisut and Phongngarm, 2013). But, in a greenhouse under natural conditions, when compared, 10 mM Tre and 10 mM Pro application on saltsensitive KDML105 cultivar (grown under 100 or 200 mM NaCl for 6 days), both Tre and Pro seemed to have positive roles against salt stress (Nounjan et al., 2012; Nounjan and Teerakulpisut, 2012). Shahbaz et al. (2017) selected two rice cultivars Bas-385 and Bas-2000 and grew those under four levels of salt stress (0, 50, 100, and 150 mM NaCl) and three levels of Tre (0, 20 and 30 mM) treatments. The results proved that both cultivars can cope with salt stress conditions by reducing lipid peroxidation, Na1 uptake, and through the modulation of antioxidant enzymes with foliar application of Tre (Shahbaz et al., 2017). Seed priming with 25 mM Tre for 12 h was also reported to confer salt stress (30 and 60 mM NaCl) tolerance in rice plants (Abdallah et al., 2016). Another osmoprotective compound GB was also used in several studies at different doses and its protective roles against salt stress in rice were documented whether used as a pre-treatment (Demiral and Turkan, 2006) or a co-treatment (Teh et al., 2016a). Some researchers used both Pro and GB to compare their regulatory effects in salt-stressed rice plants. Nipponbare rice cultivar was treated with 1 mM of Pro and GB for 12 h and grown under different concentrations of salt. At every level of salt stress, both Pro and GB application were reported to reduce the harmful effects of salinity by reducing Na1 uptake (Sobahan et al., 2009), or increasing K1/Na1 ratio (Sobahan et al., 2012), or else by diminishing lipid peroxidation (Sobahan et al., 2016). Reduced lipid peroxidation and H2O2 contents, along with increased photosynthetic pigments and the up-regulation of the antioxidant defense system were reported in rice seedlings under salt stress conditions when treated with either Pro or GB (Hasanuzzaman et al., 2014a; Wutipraditkul et al., 2015). However, a co-application of Pro (30 mM) and GB (1 mM) has been observed to confer salt-stress tolerance to some extent too (Wutipraditkul et al., 2015).

33.4.2 DROUGHT Drought stress is one of the most devastating abiotic stresses for crop plants. About half of the world rice production has been accounted to be at risk because of water stress which is extremely alarming for the large rice-dependent population (Hisyam et al., 2017). A reduction in net photosynthesis, disturbance in transpiration, PS II activity, stomatal conductance, membrane stability index, and plant-water relations along with reduced growth and yield are some of the effects of drought stress on rice plants that have been documented so far by different studies (Cha-um et al., 2013; Khairi et al., 2016). Rice plants exhibiting drought-induced oxidative stress denoted by higher lipid peroxidation or ROS generation and activation of the antioxidant defense system have been reported by several researchers (Hussain et al., 2017; Selvaraj et al., 2017). Though a number of drought-tolerant rice varieties have been introduced, the use of exogenous phytoprotectants can be

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considered as another promising method for combating drought stress. Considering this fact, the role of some osmolytes or osmoprotective compounds in conferring drought stress tolerance has been discussed here. One aromatic rice cultivar, Super-basmati, when grown under water deficit (50% field capacity) conditions, showed reduced biomass, RWC, stomatal conductance, leaf CO2 net assimilation rate, α-amylase activity, and soluble sugars content and increased electrolyte leakage, leaf H2O2, and MDA contents which were reversed by both seed soaking and foliar application of GB at a concentration of 0.85 and 1.28 mM, compared to the well-watered plants (Farooq et al., 2008). Farooq et al. (2010) also reported similar results with foliar application of GB (1.28 mM). The activity of antioxidant enzymes (SOD, CAT, and APX) were decreased under drought stress which were then increased by GB supplementation (Farooq et al., 2008; 2010). Reduction of plant height, panicle length, panicle weight, fertility percentage, hundred grain weight, and net photosynthesis rate along with elevated Pro levels were reported by Cha-um et al. (2013) in rice plants grown in water deficit conditions (25% soil water content). With the exogenous application of 100 mM GB, the Pro content further increased and the growth attributes improved which demonstrates the role of GB in mitigating drought-induced damages. In another experiment, irrigation was withheld from panicle initiation at the soft dough stage after a period of GB (100 mM) spraying for three days. After the completion of treatment period, leaves and panicles of KS-282 and Basmati-385 cultivars were collected and the data showed that the contents of Pro, sugar, and starch were higher in the GB treated plants compared to the nontreated drought stressed plants (Jalal-ud-Din et al., 2015). They also recorded the positive effect of GB application on yield attributes like panicle weight and seed panicle21.

33.4.3 HIGH TEMPERATURE In rice, high temperatures severely affects almost all growth stages from germination to harvesting and is estimated that it will be the cause of yield reductions of 41% by the late 21st century (Ceccarelli et al., 2010). Fortunately, for the development of tolerance against HT stress, besides the use of different HT tolerant varieties, plants themselves have evolved some protective mechanisms in their bodies. The accumulation of osmoprotective compounds is one of the most important approaches to resist heat induced damages. In addition, in different research findings, the use of exogenous osmolytes have also been found to be beneficial. In Oryza sativa, an increase of 12 C mean temperature during the full flowering stage significantly increased the Pro content along with high accumulation of MDA and elevated activity of antioxidant enzymes (SOD, POX, and CAT) (Kumar et al., 2016). Three O. sativa cultivars (F60, F733, and F473), when subjected to heat stress (35 and 40 C, 5 h), and as a result showed significantly increased Pro contents. A significant reduction in leaf photosynthesis along with the elevated levels of Pro, respiration, electrolyte leakage, and lipid peroxidation were evident in sensitive F60 cultivar compared to the tolerant F473 (S´anchez-Reinoso et al., 2014). To demonstrate the protective effects of Pro and betaine, an experiment was conducted with two O. sativa (Hitomebore and IR-28) cultivars. Heat stress (50 C) induced the inactivation of ribulose-1,5-bisphosphate carboxylase/oxygenase (Rubisco) in crude extracts in rice seedlings were protected by the supplementation of 1 M of Pro and betaine (Dionisio-Sese et al., 2000). Transgenic O. sativa plants overexpressing the OsMYB55 gene showed higher heat stress (35/26 C day/night, 4 week) tolerance particularly due to the enhanced biosynthesis and metabolism of total amino acid (Pro, L-glutamic acid, GABA, and arginine) contents (El-kereamy et al., 2012). Alvarado-Sanabria et al. (2017) investigated the

33.4 OSMOLYTE-INDUCED ABIOTIC STRESS PROTECTION

695

effect of high night temperatures (30 C) on an indica rice cultivar (F60) where, increased respiration rate and concentration of Pro were observed as adaptive mechanisms to tolerate high night temperatures. High night temperatures (27 and 32 C), significantly affected grain development, yield, and spikelet sterility in O. sativa. The exogenous application of GB (1.823 M) remarkably reduced the negative effects on grain yield and sucrose synthase (SS) (Mohammed and Tarpley, 2011). Mohammed and Tarpley (2009) in another experiment exposed O. sativa cv. Cocodrie to high night temperatures (32 C). They revealed that exogenous GB (1.823 M) and SA (1 mM) increased the crop growth, percentage of pollen germination, spikelet fertility as well as the yield of rice possibly by increasing antioxidant activity and decreasing heat induced oxidative damages. GB application was also found to ameliorate the heat stress-induced leaf dark respiration rate and electrolyte leakage, thereby, increasing the yield of O. sativa. High accumulation of Tre in O. sativa rendered higher heat stress tolerance by increasing the rate of photosynthesis and the synthesis of sugar carbohydrates (Garg et al., 2002). The enhanced accumulation of (soluble sugars) in O. sativa genotypes PAU-3699-13-2-1-1 (chalky) and PR122 (translucent) under high temperatures was reported by Sharma and Sharma (2017). Reduced SS activity along with increased acid invertase activity might have some roles in acclimation to high temperatures by providing hexoses in grain development. Severe heat stress (42/37 C) in O. sativa resulted in a marked reduction of growth and survival. Exogenous treatment with GABA (1 mM) resulted in the increased synthesis of osmolytes, improved photosynthesis, RWC, antioxidant activity, reduced oxidative damages as well as heat stress tolerance (Nayyar et al., 2014). Kumar et al. (2012) reported that O. sativa cultivars (PR 116 and PR 118) subjected to varying heat stress (35/30, 40/35, 45/40 C) depressed the membrane, chlorophyll contents, and the water status particularly at 45/40 C. Enhanced Pro synthesis was found as a measure of heat stress tolerance.

33.4.4 TOXIC METALS/METALLOIDS In the present world, an increasing population, urbanization and industrialization are some unavoidable phenomena, which in conjunction results in the accumulation and contamination of vast amounts of toxic metals in the atmosphere (Hasanuzzaman and Fujita, 2012). However, osmolyteinduced metal toxicity alleviation in plants have been demonstrated by several studies. In a comparative study between two indica rice varieties (IR-29 and Nonabokra), with Cd toxicity (CdCl2, 0.1, 0.25, 0.5, and 1.5 mM), a higher tolerance to CdCl2 stress was found in Nonabokra (tolerant). Cd induced the higher accumulation of osmolytes (Pro, reducing sugar, spermine, spermidine), higher activities of carotenoids, and anthocyanin and antioxidant enzymes (APX, GPX, CAT) in Nonabokra which rendered greater tolerance and protection against oxidative damages (Roychoudhury et al., 2012). According to Ashraf and Tang (2017), under Pb21 (0, 400, 800, and 1200 μM) toxicity, between two aromatic rice cultivars, GXZ and NX-18, GXZ showed higher tolerance to Pb toxicity by inhibiting yield reduction, and accumulating higher Pro and soluble sugars as well as uplifting nonenzymatic (GSH and GSSG) and enzymatic (SOD, POD, CAT, APX) antioxidants. Rizwan et al. (2017) reported that in O. sativa cv. yangliangyou 6, toxic Ni (10, 50, 100, and 200 μM) induced oxidative damages were decreased by triggering the enhanced accumulation and activity of Pro and antioxidant enzymes, respectively. Wang et al. (2009) reported that japonica rice (O. sativa cv. Zhonghua 11) subjected to Hg21 stress (0.2 mM), developed oxidative damages by over-accumulating MDA and H2O2. Apart from osmoregulation, pre-treatment with Pro (2 mM,

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CHAPTER 33 EMERGING ROLE OF OSMOLYTES IN ENHANCING ABIOTIC

12 h), significantly reduced oxidative damages by facilitating ROS scavenging and metal chelation. Tre (10 mM) induced Cu stress (100 μM CuSO4) tolerance in O. sativa cv. BRRI dhan29 was investigated through the supplementation of GB (100 μM, 24 h), in Cd stressed (50 μM) O. sativa cv Xiushui 63, which improved the Cd induced growth retardation and lowered the lipid peroxidation with increasing fresh and dry weight of shoots and roots, chlorophyll contents, and antioxidant (SOD, POD) activity (Cao et al., 2013). Mishra and Dubey (2008) found enhanced accumulation of hexoses (glucose and fructose) in Al31 (80 and 160 μM) treated O. sativa cv Malviya-36 and Pant12, which might have some role in preventing desiccation. In another experiment, Mishra and Dubey (2013) used similar plant materials with NiSO4 (200 and 400 μM) stress and found Ni induced high accumulation of reducing, nonreducing and total sugars. Similarly, excess NiSO4 (10 mM) induced Pro accumulation was also observed in the detached leaves of O. sativa cv. Taichung Native 1 (Lin and Kao, 2007). Iron exposure (0, 250, and 500 mg l21 Fe21) on two Oryza glaberrima L. cv TOG 7105 (resistant) and IRGC 104047 (sensitive) varieties were investigated. Increased Fe21 concentrations in the roots, osmotic potential, and polyamine biosynthesis were found in TOG 7105, whereas reduced soluble sugars and Pro levels were evident in sensitive IRGC 104047 (Majerus et al., 2007). Maheshwari and Dubey (2007) reported that O. sativa cv Malviya-36 and Pant-12 exposed to Ni toxicity (Ni21, 0 2500 μM), reduced ribonuclease (RNase) and protease activity along with the suppression of RNA and protein hydrolysis, where Pro was further found to protect the RNase enzyme. Similar experimental results were also evident when O. sativa cv Malviya-36 and Pant-12 were subjected to As31 toxicity (As2O3, 25 and 50 μM) (Mishra and Dubey, 2006). Sharma and Dubey (2005) again demonstrated that nitrate reductase activity decreased notably upon Al31 (160 μM) stress in O. sativa seedlings. The exogenous application of Pro, GB, and sucrose (1 mM) protected the enzyme from the damaging effects of Al31.

33.5 ENGINEERING OSMOLYTE BIOSYNTHESIS TRAITS IN CONFERRING ABIOTIC STRESS TOLERANCE IN RICE One effective strategy for salt stress tolerance is osmotic adjustment which is dependent on osmolyte synthesis and accumulation in plants. However, whether osmolyte accumulation or their homeostasis is more critical is still unclear (Kavi Kishor and Sreenivasulu, 2014). More importantly, osmoprotectants are not species-specific. For example, T. aestivum, Z. mays and H. vulgare cannot synthesize sufficient levels of GB in a natural process. Truncated transcript generation for the GB synthesizing BADH enzyme is the contributing factor behind this issue. Whereas, in O. sativa their uncommon processing brings about the expulsion of translational initiation codon, loss of functional domains, and premature stop codons (Niu et al., 2007). Moreover, O. sativa is known to be a GB nonaccumulator (Nakamura et al., 1997). In such a case, Pro and sucrose are thought to be vital osmorotectants for protecting rice plants from salt-induced osmotic stress, where P5CS and sucrose-phosphate synthase perform important roles as enzymes (Uchida et al., 2006). Considering these facts, using molecular biological approaches to transfer genes responsible for osmolyte synthesis in nonaccumulator plants might be an alternative. This may lead to the overproduction of osmolytes in salt-stressed plants. A higher expression of P5C showed a positive correlation with drought tolerance in rice subjected to 10 and 16 bar PEG (Choudhary et al., 2005). In salt-tolerant

33.5 ENGINEERING OSMOLYTE BIOSYNTHESIS TRAITS

697

rice cultivar, P5CS gene expression was higher than in the salt-sensitive one when subjected to salt stress which was positively associated with Pro content (Azzami et al., 2009). Engineering the genes responsible for osmolyte biosynthesis pathways showed that transgenic plants were able to tolerate salt, drought, and cold stress better as compared to cultivated species (Chen and Murata, 2002). However, there are few attempts reported on such approaches in the case of rice (Table 33.2; Majumder et al., 2009). Kathuria et al. (2009) produced transgenic rice with chloroplast-targeted choline oxidase encoded by the codA gene from Arthrobacter globiformis that showed enhanced physiological performance, activated antioxidant defense, and provided better protection against water stress, which was due to the activation of stress response pathways by GB as well as H2O2. Transgenic rice overexpressing p5c genes transferred from Vigna aconitifolia provided increased biomass production and root and shoot growth under both salinity and drought (Su and Wu, 2004). Transgenic plants accumulated much higher Pro than the control did. The overexpression of Tre biosynthetic genes shows stress tolerance. Li et al. (2011) revealed that OsTPS1 overexpression in rice improved salt tolerance by improving osmolyte synthesis and activating defense responsive genes. The level of raffinose accumulation was significantly higher in a

Table 33.2 Transgenic Plants OverProducing Pro and GB and Their Role in Salt and Drought Stress Tolerance Source of Gene

Observed Effects Toward Tolerance

References

Vigna aconitifolia L. P5CS gene under barley HVA22 promoter Barley peroxisomal BADH gene

Quicker salt stress recovery

Zhu et al. (1998)

Improved Chl fluorescence; reduced Na1 and Cl2 uptake and enhanced K1 uptake under salt stress Higher Tre content, enhanced plant growth, less oxidative damages, and nutrient homeostasis under salt, drought, and low temperature stresses

Kishitani et al. (2000)

Better seedling growth and PS II yield under salt, drought, and cold stresses Faster growth of shoots and roots and increased biomass production under salt and drought Better root and shoot dry weight under 150 mM salt Activated stress response pathways and provided better detoxification of ROS and higher activity of PS II which led to better growth and physiology

Jang et al. (2003)

E. coli otsA (trehalose-6-phosphate synthase) and otsB (trehalose-6-phosphate phosphatase) bi-functional fusion gene (TPSP) under the control of abscisic acid (ABA) responsive promoter or RuBisCO small subunit promoter E. coli TPSP under maize ubiquitin promoter Vigna aconitifolia p5c cDNA

A. pascens cox gene using ABA-inducible promoter Arthrobacter globiformis chloroplasttargeted choline oxidase encoded by the codA gene

Garg et al. (2002)

Su and Wu (2004)

Su et al. (2006) Kathuria et al. (2009)

Pro, Proline; GB, Glycine betaine; Tre, Trehalose, PS II, Photosystem II; ROS, Reactive oxygen species. Adapted from Majumder, A.L., Sengupta, S., Goswami, L., 2009. Osmolyte regulation in abiotic stress. In: Pareek, A., Sopory, S., Bohnert, H. (Eds.), Abiotic Stress Adaptation in Plants. Springer, Dordrecht, pp. 349 370.

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transgenic O. sativa overexpressing OsWRKY11, which promoted heat pre-treatment induced heat and desiccation tolerance (Wu et al., 2009). In O. sativa, exogenously applied betaine aldehyde significantly increased the endogenous accumulation of GB and thereby, gave some tolerance to heat stress (Shirasawa et al., 2006).

33.6 CONCLUSION To feed the increasing population of the world, especially in Asian countries rice production needs to be increased substantially. However, rice is sensitive to many abiotic stresses which are more common today due to climate change. Researchers are trying to develop an understanding of plant responses to abiotic stress and the underlying mechanisms of tolerance. One tolerance mechanisms is synthesis of osmolytes which are mainly compatible solutes like Pro, GB, Tre, and sugars. These compounds are found to be effective in maintaining osmotic balance in plants during osmotic stress. Moreover, they provided enhanced antioxidant defense and signaling. Unfortunately, rice cannot sufficiently accumulate some of these osmolytes and hence, manipulation of rice plants toward synthesis or accumulation of those compounds has been experimented on in the last few decades. Many studies have provided the notion that the exogenous application of such osmolytes provided better protection against different abiotic stresses such as salinity, drought, metal toxicity, extreme temperatures, and flooding, etc. Therefore, the transfer of osmolyte synthesizing genes to sensitive plants has been done by many researchers. However, the actual signaling role of osmolytes and their interaction with other molecules still needs to be thoroughly explored. Considering the exogenous use of osmolytes many scientists have revealed a vast variation in suitable doses for improved protection. Therefore, fine tuning of such doses of osmolytes and suitable application methods in field crops need to be perfected in order to be useable for farmers.

ACKNOWLEDGEMENT The author acknowledges Springer (Nahar et al., 2016a) for providing permission to reuse three figures to develop some content of the current chapter in its proper sequence. We thank Mrs. Khursheda Parvin, Department of Horticulture, Sher-e-Bangla Agricultural University, Dhaka, Bangladesh for her critical reading and formatting of the manuscript.

REFERENCES Abdallah, M.M.S., Abdelgawad, Z.A., El-Bassiouny, H.M.S., 2016. Alleviation of the adverse effects of salinity stress using trehalose in two rice varieties. S. Afr. J. Bot. 103, 275 282. Abdelgawad, Z.A., Hathout, T.A., El-Khallal, S.M., Said, E.M., Al-Mokadem, A.Z., 2014. Accumulation of trehalose mediates salt adaptation in rice seedlings. Am. Eurasian J. Agric. Environ. Sci. 14, 1450 1463. Abebe, T., Guenzi, A.C., Martin, B., Cushman, J.C., 2003. Tolerance of mannitol-accumulating transgenic wheat to water stress and salinity. Plant Physiol. 131, 1748 1755. Acquaah, G., 2007. Principles of Plant Genetics and Breeding. Blackwell, Oxford.

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FURTHER READING Pilon-Smits, E.A.H., Terry, N., Sears, T., Kim, H., Zayed, A., Hwang, S., et al., 1998. Trehalose-producing transgenic tobacco plants show improved growth performance under drought stress. J. Plant Physiol. 152, 525 532.