Abstract
Plants are delimited by variety of environmental stresses which affect them throughout their life cycle. These stresses particularly salt, cold, and drought hamper their development, productivity resulting in great loss in crop yield across globe. To overcome environmental stresses, plants have acquired wide range of defensive response including altered gene expression, change in cellular metabolism in terms of accumulation of low-molecular-weight compounds. These metabolites include amino acids, sugars, sugar alcohols, and quaternary amines that protect proteins and membranes against damage. This chapter is intended to give an overview of osmoprotective compounds with an emphasis on recent advances describing their function, significance in adaptation, and their potential to perk up stress tolerance.
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1 Introduction
Environmental conditions determine plant growth and development. Optimal growth of plants is adversely affected by abiotic stresses such as drought and salt stress (Kintisch 2009). Soil salinity and drought stress result in crop loss affecting about 40 % of the arable lands across the globe (Wang et al. 2003). During last decade, increase in environmental stresses and global warming result in the necessity of developing new crop cultivars that are stress tolerant. Developing tolerant lines for salt and drought stress was more important and convenient owing to their already elaborated tolerance mechanisms reported in various plants (Gregory et al. 2005). Physiological responses to drought, cold, and salt stress are similar resulting in impaired plant growth, altered photosynthetic activity via reduction in the dark reaction of photosynthesis, accumulation of reactive oxygen species (ROS), alterations in ion transport and compartmentalization, faults in the osmotic responses of the cell (Schulze et al. 2002) and changes in metabolite profiles (Shulaev et al. 2008). Low-molecular-weight organic compounds are considered to have protective functions and are accumulated as a consequence of osmotic stress without any metabolic alterations (Bartels and Sunkar 2005). Compatible solutes include organic compounds that serve as tools for osmotic adjustment and protect membranes and proteins from denaturation which reduce impacts of drought stress on plants. They also alleviate ion toxicity resulting from salt stress and maintain ion imbalance. This chapter will focus on importance of osmoprotective compounds for the acclimation to extreme environmental conditions and their role in impeding deleterious effects of environmental stresses.
2 Osmolytes
Osmolytes are considered as compatible solutes which contribute to cell turgor, protect cellular structures, and alleviate ion toxicity. These solutes mediate osmotic adjustment under drought stress by stabilizing internal potential and maintain osmotic balance (Parida and Das 2005). These protective compounds comprise mainly of amino acids (Pro), quaternary amino acid compounds (alanine betaine, glycine betaine, and proline betaine), amines (polyamines), sugars (glucose, fructose, sucrose, trehalose, raffinose, and fructans), sugar alcohols (mannitol, glycerol, and sorbitol), and sulfonium compounds (choline-O-sulfate, dimethylsulfoniopropionate) (Parida and Das 2005; Shulaev et al. 2008; Ahmad and Sharma 2008; Koyro et al. 2012; Dedemo et al. 2013). However, there are contradictory reports suggesting that osmolytes may have alternative protective functions. However, lower concentrations of organic osmolytes in several halophytes indicate that these compounds might not be important for osmotic adjustment (Gagneul et al. 2007). This statement is supported by transgenic tobacco which produces proline at high rates but does not make any osmotic adjustment compared to control tobacco plants, under salt and drought stress (Kishor et al. 1995). In addition, osmoprotectants may also serve in stabilization of redox balance, maintenance of proper protein folding and signaling (Rosgen 2007).
High salinity or dehydration can alter structure of proteins and modify the proteins followed by their denaturation and finally accelerated degradation. However, osmolytes can protect proteins from aggregation or degradation by preserving their native conformations, folding of proteins, and improve their thermodynamic stability so that they can function under stress conditions (Bolen and Baskakov 2001; Street et al. 2006). In addition, osmoprotective compounds have roles in the adaptation process to extreme environmental conditions (Rontein et al. 2002). For instance, high levels of sugars or polyols, quaternary amino acid compounds such as GB, alanine betaine, and proline are produced by halophyte species (Arbona et al. 2010; Lugan et al. 2010). Salt tolerance of halophytic Limonium species are related to accumulation of high level of quaternary ammonium compounds such as choline-O-sulfate, GB, and alanine betaine (Hanson et al. 1991). Composition and concentration of these solutes in plants can vary considerably, depending on species and type of the environmental stress (Yancey 2005; Sanchez et al. 2008; Dedemo et al. 2013). For instance, GB is dominant in Plumbaginaceae species adapted to dry environments, alanine betaine is apparently more typical in species growing on saline soils, and proline betaine has been detected in plants adapted to arid environments (Hanson et al. 1994; Majumder et al. 2010).
Osmoprotectants are significant for salt and drought stress tolerance in cereals (Garcia et al. 1997; Reguera et al. 2012). High levels of proline and sugar in drought and salt tolerant rice varieties suggest that these protective compounds can contribute to stress tolerance of rice (Roychoudhury et al. 2008). Similarly, glucose, fructose, sucrose, fructan, proline and quaternary ammonium compounds are accumulated in wheat under drought conditions (Bowne et al. 2012; Maevskaya and Nikolaeva 2013). It has been shown that the accumulation is well correlated with drought tolerance of wheat (Kerepesi et al. 1998; Bajji et al. 2001). Increase in both proline and GB levels of sorghum have been recorded upon water deficit and high salt concentration (Wood et al. 1996; Chen and Murata 2011). However, an accumulation of proline in tolerant sorghum does not contribute to its drought tolerance (Premachandra et al. 1995). Like other extremophile plants, halophytic wild rice Porteresia coarctata Roxb. is known to synthesize and accumulate myo-inositol and pinitol for combating saline stress (Sengupta and Majumder 2009; Krasensky and Jonak 2012). Strong correlation between pinitol accumulation and drought tolerance in response to low water potential has been addressed in several tropical legume species (Ford 1984). Several classes of osmolytes such as amines, amino acids, and carbohydrates having roles in salt and drought tolerance of plants will be covenanted individually in the following part.
2.1 Amines
2.1.1 Polyamines
Polyamines (PAs) are low-molecular-weight polycations found in all living organisms and known to be essential for their growth and development. PA levels can be changed by abiotic stresses, such as drought, salinity, and cold (Ahmad et al. 2012a). In addition, a positive correlation between high PA levels and stress tolerance has been recorded (Kovacs et al. 2010; Quinet et al. 2010; Alcazar et al. 2011).
Putrescine (Put), spermidine (Spd), and spermine (Spm) are the most common PAs in higher plants (Ahmad et al. 2012a). PAs are synthesized from arginine and ornithine by arginine decarboxylase (ADC) and ornithine decarboxylase (ODC). Putrescine is formed by conversion of agmatine, synthesized from arginine. Spermidine and spermine are synthesized from putrescine by the transfer of aminoporply groups from decarboxylated S-adenosylmethionine (dSAM) via Spd and Spm synthases. dSAM is formed by conversion of SAM via a reaction catalyzed by SAM decarboxylase. On the other hand, diamine oxidases (DAO) and polyamine oxidases (PAO) are main PA catabolic enzymes. DOA catalyzes the oxidation of Put to 4-aminobutanal, NH3, and H2O2, while PAO oxidize only higher PAs, such as Spd and Spm.
Protection of membranes and alleviation in oxidative stress are the two functions of PAs (Alcazar et al. 2011; Hussain et al. 2011; Ahmad et al. 2012a) but their functions in stress tolerance are not well understood. Positive role of PAs in stress tolerance has been shown by studies in transgenic plants and various mutant varieties. Putrescine levels of ADC1 or ADC2-deficit mutants which are hypersensitive to stress are lower than wild type (Urano et al. 2004; Cuevas et al. 2008), whereas putrescine levels under drought and freezing tolerance enhance by ADC overexpression (Capell et al. 2004; Alcazar et al. 2010; Alet et al. 2011). Similarly, drought, salt, and cold tolerance of Arabidopsis plants increase due to enhanced spermidine content resulting from Spd synthase overexpression (Kasukabe et al. 2004). Furthermore, tolerance of tobacco plants to salt stress and polyamine levels has been increased by introduction of ODC gene from mouse (Kumriaa and Rajam 2002). In addition, plants turn out to be very sensitive to salinity stress because of Spm synthase deficiency (Yamaguchi et al. 2006).
The application of polyamines (PAs) is also an effective approach for enhancing stress tolerance in plants (Shi et al. 2010). Exogenous application of 0.4 M Spm to soybean plants ameliorates osmotic stress effects by increasing catalase, superoxide dismutase, peroxidase, and polyphenol oxidase activities and modulating levels of plant hormones, ABA and jasmonic acid (Radhakrishnan and Lee 2013). Shu et al. (2013) have examined effects of Spm on chlorophyll fluorescence, antioxidant system, and ultrastructure of chloroplasts in Cucumis sativus L. under salt stress. They have found that Spm has reversed effects of salt stress on photosynthetic apparatus. In addition, application of Spm significantly increases superoxide dismutase, peroxidase, and ascorbate peroxidase activities in the chloroplasts thriving under saline conditions. Hence, salt stress in C. sativus plants has been mitigated by Spm application.
Exogenous spermidine (Spd) applied to tomato (Solanum lycopersicum) cultivars decreases growth and induces increase in free amino acids, ammonium (NH4 +) contents, and NADH-dependent glutamate dehydrogenase (NADH-GDH) activities. They have suggested that exogenous Spd treatment alleviates disturbances in nitrogen metabolism resulted from salinity-alkalinity stress (Zhang et al. 2013).
2.1.2 Glycine Betaine
Glycine betaine (GB) is the quaternary ammonium compound and methylated derivative of glycine. Along with other quaternary ammonium compounds like -alanine betaine, proline betaine, choline-O-sulfate, hydroxyproline betaine, and pipecolate betaine they function as effective compatible osmolytes in halophytes (Ashraf and Harris 2004; Chen and Murata 2008, 2011). Different stress conditions such as osmotic stress (Hanson and Nelsen 1978), salinity (Hanson et al. 1991), and drought (Guo et al. 2009) can induce GB accumulation in plants. The beneficial effects of GB accumulation regarding salt and osmotic stress tolerance have been demonstrated in a number of engineered GB-accumulating plants, including tobacco (Zhang et al. 2008), tomato (Park et al. 2004, 2007), and rice (Chen and Murata 2008). These compounds confer resistance mainly by protecting photosynthetic activity through the maintenance of Rubisco activity and PSII activity (Yang et al. 2008).
Plants are usually very sensitive to environmental stress during reproduction. GB was shown to have a particularly important protective effect on reproductive organs, such as inflorescence apices and flowers during drought and cold stress (Chen and Murata 2008; Sakamoto and Murata 2000). Engineering of GB accumulation has reduced chilling damage on tomato flowers, leading to a 10–30 % increase in fruit production (Park et al. 2004). He et al. (2013) have introduced two genes, glycine sarcosine methyltransferase gene (ApGSMT2) and dimethylglycine methyltransferase gene (ApDMT2), from the bacterium Aphanothece halophytica to maize so that the engineered plants synthesize more GB than control plants. Thus transgenic maize could be drought tolerant by co-expression of ApGSMT2 and ApDMT2. These data confirm that GB is an osmoprotective compound, which can therefore be explored to improve tolerance to salinity and probably to drought and cold stress.
Activation and protection of the ROS detoxification system is another key component of stress tolerance (Moradi and Ismail 2007). Osmoprotective compounds can scavenge ROS directly, or contribute to the protection of the enzymes involved in the antioxidant system. Increase in antioxidant enzymes activities and alleviation of oxidative damages due to abiotic stresses have been reported in different plant species subjected to exogenous applications of GB (Nawaz and Ashraf 2010; Ahmad et al. 2013). For instance, after exogenous GB applications to Carapa guianensis plants, ascorbate peroxidase and catalase activities increase whereas lipid peroxidation has been prevented under water stress (Cruz et al. 2013). Foliar application of 50 mM GB to maize plants reduces adverse effects of salt stress by improving proline, Ca2+, and K+ levels and maintaining membrane permeability (Kaya et al. 2013).
2.2 Amino Acids
2.2.1 Proline
The imino acid proline, a common denominator of many stress responses, is accumulated during diverse abiotic and biotic stresses (Kavi Kishor et al. 2005; Koca et al. 2007; Ahmad and Sharma 2008; Ahmad et al. 2012b) such as high salinity (Ben Hassine et al. 2008), drought (Choudhary et al. 2005), oxidative stress (Yang et al. 2009), and intense irradiation (Jan et al. 2012a, b). In plants, proline is synthesized from glutamate in the cytosol and probably also in the chloroplast by delta-1-pyrroline-5-carboxylate synthetase (P5CS) and P5C reductase (P5CR). P5CS produces glutamate semialdehyde, which is unstable and is immediately converted to pyrroline-5-carboxylate (P5C). P5CR reduces P5C to proline, a reaction that takes place in the cytosol and according to biochemical data also in the chloroplast (Szabados and Savoure 2010; Koyro et al. 2012).
Proline catabolism occurs in the inner-mitochondrial membrane of all eukaryotes. Proline degradation provides electrons and glutamate for mitochondrial usage. Proline dehydrogenase (ProDH), an FAD enzyme localized to the inner-mitochondrial membrane, catalyzes the first oxidizing step of proline to P5C and meanwhile delivers electrons to the mitochondrial electron transport chain (Kiyosue et al. 1996). P5C is further oxidized to glutamate or transported back to the cytosol for proline re-synthesis by the proline cycle (Deuschle et al. 2004; Miller et al. 2009). Proline accumulation during stress protects cellular structures and stabilizes enzymes owing to its antioxidant potential (Kavi Kishor et al. 2005; Mishra and Dubey 2006; Sharma and Dubey 2005). Proline also maintains redox balance, preserve energy source for the stress recovery and functions as protein precursor (Hoque et al. 2008; Islam et al. 2009; Szekely et al. 2008). In addition, proline synthesis in the chloroplast may allow an efficient oxidation of photosynthetically produced NADPH, which is required for quenching free electrons and nascent oxygen that could otherwise lead to ROS generation (Hare and Cress 1997; Szabados and Savoure 2010).
Studies about mutants and transgenic plants have showed the protective function of proline. Hypersensitive mutant of Arabidopsis thaliana with p5cs1 insertion has confirmed importance of proline in stress tolerance. Proline content of Arabidopsis mutant is 90 % lower than the wild type and produces more ROS and lipid peroxidation products (Szekely et al. 2008). However, proline accumulation increases salt and drought tolerance in P5CS-overexpressed tobacco, rice, and soybean (Kishor et al. 1995; De Ronde et al. 2004; Kumar et al. 2010). Similarly, Swingle citrumelo plants have been transformed with Vigna aconitifolia P5CS gene (VaP5CSF129A) that improved proline levels and lead to differential expression levels of antioxidant enzymes (de Carvalho et al. 2013). Transgenic plants exhibit improved mRNA levels of ascorbate peroxidase, superoxide dismutase, and glutathione reductase isoenzymes that produce high proline level than non-transgenic plants. de Carvalho et al. (2013) have claimed that high proline level might have a regulatory role on antioxidant enzymes.
Exogenous proline is also effective in stress liberation of plants. Leaves of wild almond (Prunus spp.) species exposed to H2O2-mediated oxidative stress displayed high levels of proline (Sorkheh et al. 2012). Improved proline levels have decreased lipid peroxidation, membrane electrolyte leakage, and endogenous H2O2 content by modulating antioxidant enzymes such as peroxidase, ascorbate peroxidase, and non-enzymatic antioxidant like ascorbic acid that prevented almond species from oxidative stress injury. Similarly, exogenous proline treatment has alleviated salt stress effects by inducing catalase and ascorbate peroxide activities and decreasing endogenous H2O2 content in salt-stressed rice plants (Nounjan and Theerakulpisut 2012).
2.2.2 GABA
Adverse environmental conditions cause rapid accumulation of the non-protein amino acid like γ-aminobutyric acid (GABA) to high levels (Kaplan and Guy 2004; Kempa et al. 2008; Renault et al. 2010). Glutamate decarboxylase (GAD) convert glutamate to GABA in the cytosol, then GABA is transported to the mitochondria. Succinate is formed by GABA transaminase (GABA-T) and succinic semialdehyde dehydrogenase (SSADH) and involved in the TCA cycle (Shelp et al. 1999; Fait et al. 2008). GABA is closely related with ROS scavenging and carbon–nitrogen balance (Bouche and Fromm 2004; Song et al. 2010; Liu et al. 2011). Enzymes having role in GABA metabolism are induced by salt stress (Renault et al. 2010). Adverse effects of ionic stress increase in GABA-T-deficient Arabidopsis mutants. Levels of amino acids (including GABA) increased, while carbohydrate levels have been decreased in these mutants (Renault et al. 2010). Expression levels of genes, which are related to sucrose and starch catabolism increase under salt stress conditions with simultaneous loss of GABA-T function. Furthermore, compared with wild type, sugar concentration is twofold reduced in gaba-t/pop2-1 mutant roots. Based on this information, Renault et al. (2013) provide evidence for the implication of GABA in central carbon metabolism regulation in roots under salt stress conditions.
2.3 Carbohydrates
2.3.1 Fructans
When energy demands increase and energy supplies are reduced, plants accumulate carbohydrates as storage substances. These substances are preferred to be rapidly mobilized sugars such as starch and fructans. Main storage carbohydrate of the most plant species is starch, while fructans can be accumulated by several angiosperms grown in the areas with dry periods and seasonal cold (Hendry 1993; Valluru and Van den Ende 2008). High water solubility, resistance to crystallization under freezing temperatures, and fructan synthesis at low temperatures add compensation in accumulation of fructans (Vijn and Smeekens 1999; Livingston et al. 2009). In addition, during freezing and dehydration, fructans can contribute to osmotic adjustment (Spollen and Nelson 1994; Olien and Clark 1995) and stabilize membranes (Valluru and Van den Ende 2008).
Transferring fructose from sucrose to growing fructan chain, fructosyltransferases, 1-SST, and 6-SFT synthesize fructans in vacuole (Vijn and Smeekens 1999; Livingston et al. 2009). Increased fructosyltransferases in transgenic tobacco and rice plants improve levels of fructans that enhance tolerance to drought and low-temperature stress (Pilonsmits et al. 1995; Li et al. 2007; Kawakami et al. 2008). In addition, increases in 1-fructosyltransferase (1-FFT) and fructan 1-exohydrolase (1-FEH) activity in water-stressed Vernonia herbacea (Vell.) Rusby plants accumulate about 80 % of fructans in the underground reserve organs, depicting the potential of fructans in maintenance of water content and drought tolerance by osmotic adjustment (Garcia et al. 2011).
2.3.2 Starch, Mono and Disaccharides
Starch, a glucose polymer, serves as a source of soluble sugars and main carbohydrate storage for most of the plants. Environmental changes easily affect starch metabolism. Starch levels are very sensitive to salt and drought stress generally. These stresses cause decrease in starch content and lead to enhancement in soluble sugars in leaves (Todaka et al. 2000; Kaplan and Guy 2004; Basu et al. 2007; Kempa et al. 2008). Under stress conditions, sugars accumulate and function as osmolytes to maintain cell turgour, protect membranes and proteins from stress injury (Madden et al. 1985; Kaplan and Guy 2004). Starch degradation is included by glucan-water dikinase (GWD) and phosphoglucan-water dikinase (PWD), which catalyze phosphorylation of starch granules. Maltose synthesized from glucans by β-amylases is converted to glucose followed by formation of fructose and sucrose in cytosol (Tetlow et al. 2004; Kotting et al. 2010).
Starch hydrolysis in the leaves under stressed conditions may be related to β-amolytic pathway of starch hydrolysis under normal growth conditions. Decrease in the freeze tolerance of Arabidopsis sex1 (starch excess 1) mutants, disable to show GWD activity, is an evidence for the relation between β-amolytic pathway of starch hydrolysis and stress conditions (Yano et al. 2005). In addition, during osmotic stress total β-amylase activity has increased, while it has reduced in light-stimulated starch accumulation in wild-type Arabidopsis. On the other hand, Arabidopsis β-amylase mutant bam1 (bmy7) is hypersensitive to osmotic stress (Valerio et al. 2011). Similarly, a reduction in low stress tolerance of photosystem II has been shown in BMY8 (BAM3) antisense plants, which accumulate high starch levels, have not induced maltose, glucose, fructose, and sucrose accumulation (Kaplan and Guy 2005). Zeeman et al. (2004) have suggested a role of the phosphorolytic starch degradation pathway during stress. After salt and low air humidity exposures to Arabidopsis plants deficient in plastidial α-glucan phosphorylase, lesions formation increase in the regions surrounded by cells with high starch levels.
2.3.3 Trehalose
Some desiccation tolerant plants, for example, Myrothamnus flabellifolius can accumulate trehalose, the non-reducing disaccharide to high amounts (Bianchi et al. 1993; Drennan et al. 1993). Later, trehalose accumulation has been detected in numerous other plants under different stress conditions such as drought, cold, and high salinity (Pramanik and Imai 2005; Lopez et al. 2008). Stabilization of proteins and membranes can be done by trehalose, which can function as an osmoprotective compound at sufficient levels (Paul et al. 2008). However, trehalose levels of most angiosperms can be increased by abiotic stresses but to moderate level only (Rizhsky et al. 2004; Guy et al. 2008; Kempa et al. 2008).
Trehalose biosynthesis is a two-step pathway in which trehalose-6-phosphate is produced from UDP glucose and glucose-6-phosphate by trehalose phosphate synthase, which is converted to trehalose by the enzyme trehalose phosphate phosphatase (Vogel et al. 1998, 2001). Trehalose is catabolized by trehalase, which converts it to glucose (Goddijn et al. 1997; Brodmann et al. 2002). The importance of trehalose in stress responses has been demonstrated by engineering the trehalose biosynthetic pathway in transgenic plants. Trehalose level has been enhanced by overexpression of bacterial trehalose biosynthetic genes like otsA and otsB in rice which improve its salt and drought tolerance (Garg et al. 2002). Several other transgenic plants that accumulate trehalose at high levels have been produced. The idea about regulation of stress tolerance can be done by inducing trehalose metabolism and has been proven via studies on genetically modified plants (Ge et al. 2008; Stiller et al. 2008). On the other hand, in another study, modification of trehalase which is responsible for conversion of trehalose to glucose has showed that trehalase plays a role in the regulation of stomatal closure in plants under drought stress. During water-deficit stress, AtTRE1 overexpression in A. thaliana plants that have low level of trehalose exhibits better resistance to water deficit than Attre1 mutants that has elevated trehalose contents. High sensitivity of AtTRE1 stomata to ABA maintains leaf water content by closing more stomata than the mutants (Van Houtte et al. 2013). Exogenous applications of trehalose provide plants with improved tolerance to drought and salt stresses. Trehalose treatments cause increases in transcription of antioxidant enzyme genes such as superoxide dismutase, ascorbate peroxidase, peroxidase, and catalase in salt-stressed rice plants. Trehalose-treated plants recover immediately compared to non-treated plants (Nounjan et al. 2012).
Trehalose is suggested to function as chemical chaperon and has been shown to stabilize membranes and protect proteins in tissues under drought stress (Crowe et al. 1984; Crowe 2007). Trehalose can act as a signal molecule below 1 mg/g fresh weight instead of being a compatible solute (Garg et al. 2002). Therefore, the signaling function of trehalose and trehalose-6P could be more important than the previously suggested chaperone or osmolyte function, although in some tissues such a protective role cannot be excluded (Fernandez et al. 2010).
2.3.4 Polyols
One other class of osmoprotective compounds is polyols or sugar alcohols, which are chemically, reduced forms of aldose or ketose sugars. Water-like hydroxyl groups of polyols forming a sphere of hydration around macromolecules allow them to act as osmoprotectants under low osmotic potential. Polyols have functions as molecular chaperons stabilizing macromolecules. They also prevent membranes and enzymes from oxidative damage by scavenging ROS (Smirnoff and Cumbes 1989; Shen et al. 1997). Compared to sorbitol and galactitol, mannitol is the most common sugar alcohol and is an important photosynthetic product in a number of plant species (Loescher et al. 1992; Rumpho et al. 1983). In some plant species, there has been a correlation between stress tolerance and accumulation of mannitol and sorbitol (Stoop et al. 1996). Increase in tolerance to salinity or water deficit has been observed in Arabidopsis, tobacco, poplar, and wheat, which have been introduced mannitol-1-phosphate dehydrogenase (mtlD) from E. coli, that converts fructose-6-phosphate to mannitol-1-phosphate (Abebe et al. 2003; Chen et al. 2005; Sengupta et al. 2008). Similarly, targeted expression of mt1D in tobacco chloroplasts causes an increase in cytoplasmic mannitol concentration in transgenic tobacco plants, this increase, in turn, results in resistance to methyl viologen-induced oxidative stress (Shen et al. 1997). Overexpression of celery M6PR is an alternative way to enhance mannitol biosynthesis and has been shown to be an efficient way to improve salt tolerance of Arabidopsis (Zhifang and Loescher 2003). In a halophyte Prosopis strombulifera, leaf mannitol content increases during NaCl stress whereas sorbitol content increases after Na2SO4 treatment. According to increase in mannitol content during NaCl stress, it has been concluded that P. strombulifera prefer mannitol for osmotic adjustment, however, sorbitol synthesis during Na2SO4 might be related to problems in carbon metabolism due to toxicity of sulfate (Llanes et al. 2013).
Myo-inositol is an essential polyalcohol in plants and eukaryotes for being an important precursor of some lipid signaling molecules and it has potential role in signaling during stress, cell wall biosynthesis, cell death, and plant hormone synthesis. Biosynthesis of myo-inositol starts from d-glucose-6P, which is converted to myo-inositol-1P by myo-inositol-1P synthase (MIPS) (Johnson and Sussex 1995; Majumder et al. 1997). Myo-inositol is produced from myo-inositol-1P by dephosphorylation and is used for the subsequent biosynthesis of all inositol-containing compounds, including phospholipids. MIPS genes were shown to be salt-induced, leading to accumulation of myo-inositol in the halophyte ice plant, but not in the glycophyte Arabidopsis (Ishitani et al. 1996). MIPS genes can be regulated by several environmental stress factors such as drought, heat and cold stress, high light and controlled by ABA signals (Yoshida et al. 1999, 2002; Abreu and Aragao 2007; Wei et al. 2010a, b). Phosphorylated derivatives of myo-inositol are important signaling compounds in responses to biotic and abiotic stresses which are involved in numerous regulatory pathway and control diverse aspects of plant development (Nelson et al. 1999). Improved tolerance to salt stress during germination, seedling growth and development has been observed in Arabidopsis thaliana that overexpress myo-inositol 1-phosphate synthase gene (SaINO1) in halophytic grass, Spartina alterniflora (Joshi et al. 2013).
As an important osmoprotectant, a six-carbon alcohol sorbitol is the most preferable accumulated carbon source in some fruit trees of Rosaceae family (Tari et al. 2010; Feng et al. 2011; Li et al. 2012). Sorbitol confers tolerance against abiotic and biotic stresses by participating in osmotic adjustment during stress. Sorbitol is synthetized from hexose phosphates like sucrose. Sorbitol-6-phosphate dehydrogenase (S6PDH) is a regulatory enzyme in sorbitol biosynthesis, which catalyzes conversion of glucose-6-phophate to sorbitol-6-phosphate then in turn, sorbitol-6-phosphate is dephosphorylated to form sorbitol by sorbitol-6-phosphate phosphatase (Kanamaru et al. 2004; Liang et al. 2012).
Sorbitol transporter genes are induced by subjecting plants to stress so that plants can accumulate sorbitol. Sour berry, apple, and Arabidopsis plants have been scanned for the transporter genes and the genes have been identified in these plants (Gao et al. 2005; Fan et al. 2009). Differential regulation of sugar regulators is maintained through sugar transporters induced in response to varied abiotic and biotic stress (Wormit et al. 2006). Sorbitol accumulation in salt-stressed Plantago major has been detected by Pommerrenig et al. (2007). In addition, up-regulation of three sorbitol transporters in apple plants has improved drought tolerance in vegetative tissues with subsequent increment in sorbitol concentration as confirmed by HPLC analysis of leaves, roots, and phloem tissues (Li et al. 2012).
Pinitol is a methylated inositol, which is synthetized from myo-inositol by inositol-o-methyltransferase (IMT1) and ononitolepimerase (OEP1) (Bohnert et al. 1995; Rammesmayer et al. 1995; Sengupta et al. 2008). Pinitol increase has been correlated with improved tolerance of some plants subjected to drought or heat stress. Increase in the drought resistance of pine seedlings that accumulate pinitol has been determined. The cultivars that acquire higher pinitol content are resistant to drought stress than the low pinitol-producing cultivars (N’Guyen and Lamant 1988). Many studies confirm sucrose as the well-known low-molecular-weight carbohydrate that is accumulated in soybean plants under stress (Yamada and Fukutoku 1985; Fellows et al. 1987). Ford (1984) has reported inadequate increase in sucrose contents and significant accumulation of pinitol in soybean plants under water-stressed conditions. Pinitol accumulation is a characteristic feature of a number of halophytic plants in saline environment and occurs in several glycophytic plants grown under osmotic stress conditions (N’Guyen and Lamant 1988; Gorham et al. 1981; Popp 1984; Paul and Cockburn 1989; Sengupta et al. 2008). Unlike native rice cultivars, pinitol hyperaccumulation has been found in Porteresia coarctata, a halophytic wild relative of rice. This pinitol accumulation is controlled by inositol methyl transferase 1 (PcIMT1) gene, an essential metabolic response for salt stress (Sengupta et al. 2008). Increased salt tolerance was shown in transgenic tobacco displaying P. coarctata, MIPS overexpression, and M. crystallinum IMT1 gene insertion. These transgenic tobacco plants accumulate more inositol and pinitol that confer improved growth, higher photosynthetic activity, and lower oxidative damage during salt stress (Patra et al. 2010).
3 Conclusions and Future Perspective
Plants being sessile are subjected to diverse environmental stresses that impede their growth and development. Therefore, metabolic adjustment to cope with environmental stress conditions is important considerably for plants. However, this adjustment is brought at different levels in diverse ways making tolerance mechanism even more complex. As each organism, even its varieties exhibit assorted response to array of external stimuli. For instance, changes in cellular metabolism during development and acclimation under adverse conditions are closely related to the developmental stage of a plant. Therefore, there is great necessity to study state of vulnerability at particular developmental stage and metabolic adjustment in stress conditions.
Osmoprotective compounds like sugars and proline could function as metabolic signals and therefore have broader influence on physiological responses and metabolic adjustment to stress conditions. Despite there are many studies about signaling networks, however there is paucity regarding reports about how a metabolic response is induced by an environmental change and what are the roles of osmolytes in stress signaling. Engineering of crop plants via genetic transformation is a promising tool to study the significance of osmoprotective compounds in stress responses and to improve the performance of crop plants under suboptimal conditions. Enhanced accumulation of a metabolite can be achieved via activation of the biosynthetic pathway or inhibition of the catabolic pathway. Furthermore, novel pathways can be established in plants, by introducing genes from other species. Combining advanced approaches like genomics, proteomics, and metabolomics could increase our understanding of plant stress responses on a global scale and will put forth metabolic bases of adaptation to drought, salinity, or extreme temperatures.
References
Abebe T, Guenzi AC, Martin B, Cushman JC (2003) Tolerance of mannitol-accumulating transgenic wheat to water stress and salinity. Plant Physiol 131:1748–1755
Abreu EF, Aragao FJ (2007) Isolation and characterization of a myoinositol-1-phosphate synthase gene from yellow passion fruit (Passiflora edulis f. flavicarpa) expressed during seed development and environmental stress. Ann Bot 99:285–292
Ahmad P, Sharma S (2008) Salt stress and phytobiochemical responses of plants. Plant Soil Environ 54:89–99
Ahmad P, Kumar A, Gupta A, Hu X, Hakeem KR, Azooz MM, Sharma S (2012a) Polyamines: role in plants under abiotic stress. In: Ashraf M, Öztürk M, Ahmad MSA, Aksoy A (eds) Crop production for agricultural improvement. Springer Science and Business Media, Netherlands, pp 491–512
Ahmad P, Hakeem KR, Kumar A, Ashraf M, Akram NA (2012b) Salt-induced changes in photosynthetic activity and oxidative defense system of three cultivars of mustard (Brassica juncea L.). Afr J Biotechnol 11:2694–2703
Ahmad R, Lim CJ, Kwon SY (2013) Glycine betaine: a versatile compound with great potential for gene pyramiding to improve crop plant performance against environmental stresses. Plant Biotechnol Rep 7:49–57
Alcazar R, Planas J, Saxena T, Zarza X, Bortolotti C, Cuevas J, Bitrian M, Tiburcio AF, Altabella T (2010) Putrescine accumulation confers drought tolerance in transgenic Arabidopsis plants overexpressing the homologous arginine decarboxylase 2 gene. Plant Physiol Biochem 48:547–552
Alcazar R, Cuevas J, Planas J, Zarza X, Bortolotti C, Carrasco P, Salinas J, Tiburcio AF, Altabella T (2011) Integration of polyamines in the cold acclimation response. Plant Sci 180:31–38
Alet AI, Sanchez DH, Cuevas JC, Del Valle S, Altabella T, Tubircio AF, Marco F, Fernando A, Espasandin FD, Gonzales ME, Ruiz OA, Carrascp P (2011) Putrescine accumulation in Arabidopsis thaliana transgenic lines enhances tolerance to dehydration and freezing stress. Plant Signal Behav 6:278–286
Arbona V, Argamasilla R, Gomez-Cadenas A (2010) Common and divergent physiological, hormonal and metabolic responses of Arabidopsis thaliana and Thellungiella halophila to water and salt stress. J Plant Physiol 167:1342–1350
Ashraf M, Harris PJC (2004) Potential biochemical indicators of salinity tolerance in plants. Plant Sci 166:3–16
Bajji M, Lutts S, Kinet J (2001) Water deficit effects on solute contribution to osmotic adjustment as a function of leaf ageing in three durum wheat (Triticum durum Desf.) cultivars performing differently in arid conditions. Plant Sci 160:669–681
Bartels D, Sunkar R (2005) Drought and salt tolerance in plants. Cr Rev Plant Sci 24:23–58
Basu PS, Ali M, Chaturvedi SK (2007) Osmotic adjustment increases water uptake, remobilization of assimilates and maintains photosynthesis in chickpea under drought. Indian J Exp Biol 45:261–267
Ben Hassine A, Ghanem ME, Bouzid S, Lutts S (2008) An inland and a coastal population of the Mediterranean xero-halophyte species Atriplex halimus L. differ in their ability to accumulate proline and glycinebetaine in response to salinity and water stress. J Exp Bot 59:1315–1326
Bianchi G, Gamba A, Limiroli R, Pozzi N, Elster R, Salamini F, Bartels D (1993) The unusual sugar composition in leaves of the resurrection plant Myrothamnus flabellifolia. Physiol Plant 87:223–226
Bohnert HJ, Nelson DE, Jensen RG (1995) Adaptations to environmental stresses. Plant Cell 7:1099–1111
Bolen DW, Baskakov IV (2001) The osmophobic effect: natural selection of a thermodynamic force in protein folding. J Mol Biol 310:955–963
Bouche N, Fromm H (2004) GABA in plants: just a metabolite? Trends Plant Sci 9:110–115
Bowne JB, Erwin TA, Juttner J, Schnurbusch T, Langridge P, Bacic A, Roessner U (2012) Drought responses of leaf tissues from wheat cultivars of differing drought tolerance at the metabolite level. Mol Plant 5:418–429
Brodmann A, Schuller A, Ludwig-Müller J, Aeschbacher RA, Wiemken A, Boller T, Wingler A (2002) Induction of trehalase in Arabidopsis plants infected with the trehalose-producing pathogen Plasmodiophora brassicae. Mol Plant Microbe Interact 15:693–700
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 U S A 101:9909–9914
Chen TH, Murata N (2008) Glycinebetaine: an effective protectant against abiotic stress in plants. Trends Plant Sci 13:499–505
Chen TH, Murata N (2011) Glycinebetaine protects plants against abiotic stress: mechanisms and biotechnological applications. Plant Cell Environ 34:1–20
Chen XM, Hu L, Lu H, Liu QL, Jiang XN (2005) Overexpression of mtlD gene in transgenic Populus tomentosa improves salt tolerance through accumulation of mannitol. Tree Physiol 25:1273–1281
Choudhary NL, Sairam RK, Tyagi A (2005) Expression of delta1-pyrroline- 5-carboxylate synthetase gene during drought in rice (Oryza sativa L.). Indian J Biochem Biophys 42:366–370
Crowe JH (2007) Trehalose as a “chemical chaperone”: fact and fantasy. Adv Exp Med Biol 594:143–158
Crowe JH, Crowe LM, Chapman D (1984) Preservation of membranes in anhydrobiotic organisms: the role of trehalose. Science 223:701–703
Cruz FJR, Castro GLS, Silva Júnior DD, Festucci-Buselli RA, Pinheiro HA (2013) Exogenous glycine betaine modulates ascorbate peroxidase and catalase activities and prevent lipid peroxidation in mild water-stressed Carapa guianensis plants. Photosynthetica 51:102–108
Cuevas JC, Lopez-Cobollo R, Alcazar R, Zarza X, Koncz C, Altabella T, Salinas J, Tiburcio AF, Ferrando A (2008) Putrescine is involved in Arabidopsis freezing tolerance and cold acclimation by regulating abscisic acid levels in response to low temperature. Plant Physiol 148:1094–1105
de Carvalho K, de Campos MKF, Domingues DS, Pereira LFP, Vieira LGE (2013) The accumulation of endogenous proline induces changes in gene expression of several antioxidant enzymes in leaves of transgenic Swingle citrumelo. Mol Biol Rep 40:3269–3279
De Ronde JA, Cress WA, Kruger GHJ, Strasser RJ, Van Staden J (2004) Photosynthetic response of transgenic soybean plants, containing an Arabidopsis P5CR gene, during heat and drought stress. J Plant Physiol 161:1211–1224
Dedemo GC, Rodrigues FA, Roberto PG, Neto CB, de Castro FS, Zingaretti SM (2013) Osmoprotection in sugarcane under water deficit conditions. Plant Stress 7:1–7
Deuschle K, Funck D, Forlani G, Stransky H, Biehl A, Leister D, van der Graaff E, Kunze R, Frommer WB (2004) The role of [Delta]1-pyrroline-5-carboxylate dehydrogenase in proline degradation. Plant Cell 16:3413–3425
Drennan PM, Smith MT, Goldsworthy D, van Staden J (1993) The occurrence of trehalose in the leaves of the desiccation-tolerant angiosperm Myrothamnus flabellifolius Welw. J Plant Physiol 142:493–496
Fait A, Fromm H, Walter D, Galili G, Fernie AR (2008) Highway or byway: the metabolic role of the GABA shunt in plants. Trends Plant Sci 13:14–19
Fan RC, Peng CC, Xu YH, Wang XF, Li Y, Shang Y, Du SY, Zhao R, Zhang XY, Zhang LY, Zhang DP (2009) Apple sucrose transporter SUT1 and sorbitol transporter SOT6 interact with Cytochrome b5 to regulate their affinity for substrate sugars. Plant Physiol 150:1880–1901
Fellows RJ, Patterson RP, Raper CD Jr, Harris D (1987) Nodule activity and allocation of photosynthate of soybean during recovery from water stress. Plant Physiol 84:45–60
Feng X, Zhao P, Hao J, Hu J, Kang D, Wang H (2011) Effects of sorbitol on expression of genes involved in regeneration of upland rice (Oryza sativa L.). Plant Cell Tissue Organ Cult 106:455–463
Fernandez O, Bethencourt L, Quero A, Sangwan RS, Clement C (2010) Trehalose and plant stress responses: friend or foe? Trends Plant Sci 15:409–417
Ford CW (1984) Accumulation of low molecular weight solutes in water-stressed tropical legumes. Phytochemistry 23:1007–1015
Gagneul D, Aiouche A, Duhaze C, Lugan R, Larher FR, Bouchereau A (2007) A reassessment of the function of the so-called compatible solutes in the halophytic Plumbaginaceae Limonium latifolium. Plant Physiol 144:1598–1611
Gao Z, Jayanty S, Beaudry R, Loescher W (2005) Sorbitol transporter expression in apple sink tissues: implications for fruit sugar accumulation and watercore development. J Am Soc Hortic Sci 130:261–268
Garcia AB, JdA E, Iyer S, Gerats T, Van Montagu M, Caplan AB (1997) Effects of osmoprotectants upon NaCl stress in rice. Plant Physiol 115:159–169
Garcia PMA, Asega AF, Silva EA, Carvalho MAM (2011) Effect of drought and re-watering on fructan metabolism in Vernonia herbacea (Vell.) Rusby. Plant Physiol Biochem 49:664–670
Garg AK, Kim JK, Owens TG, Ranwala AP, Choi YD, Kochian LV, Wu RJ (2002) Trehalose accumulation in rice plants confers high tolerance levels to different abiotic stresses. Proc Natl Acad Sci U S A 99:15898–15903
Ge LF, Chao DY, Shi M, Zhu M-Z, Gao JP, Lin H-X (2008) Overexpression of the trehalose-6-phosphate phosphatase gene OsTPP1 confers stress tolerance in rice and results in the activation of stress responsive genes. Planta 228:191–201
Goddijn OJ, Verwoerd TC, Voogd E, Krutwagen RW, de Graaf PT, van Dun K, Poels J, Ponstein AS, Damm B, Pen J (1997) Inhibition of trehalase activity enhances trehalose accumulation in transgenic plants. Plant Physiol 113:181–190
Gorham J, Hughes L, Wyn-Jones RG (1981) Low-molecularweight carbohydrates in some salt-stressed plants. Physiol Plant 53:27–33
Gregory PJ, Ingram JS, Brklacich M (2005) Climate change and food security. Philos T Roy Soc B 360:2139–2148
Guo P, Baum M, Grando S, Salvatore C, Guihua B, Li R, Maria VK, Varshney RK, Andreas G, Valkoun J (2009) Differentially expressed genes between drought-tolerant and drought-sensitive barley genotypes in response to drought stress during the reproductive stage. J Exp Bot 60:3531–3544
Guy C, Kaplan F, Kopka J, Selbig J, Hincha DK (2008) Metabolomics of temperature stress. Physiol Plant 132:220–235
Hanson AD, Nelsen CE (1978) Betaine accumulation and [C]formate metabolism in water-stressed barley leaves. Plant Physiol 62:305–312
Hanson AD, Rathinasabapathi B, Chamberlin B, Gage DA (1991) Comparative physiological evidence that beta-Alanine Betaine and Choline-O-Sulfate act as compatible osmolytes in halophytic Limonium species. Plant Physiol 97:1199–1205
Hanson AD, Rathinasabapathi B, Rivoal J, Burnet M, Dillon MO, Gage DA (1994) Osmoprotective compounds in the Plumbaginaceae: a natural experiment in metabolic engineering of stress tolerance. Proc Natl Acad Sci U S A 91:306–310
Hare P, Cress W (1997) Metabolic implications of stress induced proline accumulation in plants. Plant Growth Regul 21:79–102
He C, He Y, Liu Q, Liu T, Liu C, Wang L, Zhang J (2013) Co-expression of genes ApGSMT2 and ApDMT2 for glycine betaine synthesis in maize enhances the drought tolerance of plants. Mol Breed 31:559–573
Hendry GAF (1993) Evolutionary origins and natural functions of fructans: a climatological, biogeography and mechanistic appraisal. New Phytol 123:3–14
Hoque MA, Banu NA, Nakamura Y, Shimoishi Y, Murata Y (2008) Proline and glycinebetaine enhance antioxidant defense and methylglyoxal detoxification systems and reduce NaCl-induced damage in cultured tobacco cells. J Plant Physiol 165:813–824
Hussain SS, Ali M, Ahmad M, Siddique KH (2011) Polyamines: natural and engineered abiotic and biotic stress tolerance in plants. Biotechnol Adv 29:300–311
Ishitani M, Majumder AL, Bornhouser A, Michalowski CB, Jensen RG, Bohnert HJ (1996) Coordinate transcriptional induction of myo-inositol metabolism during environmental stress. Plant J 9:537–548
Islam MM, Hoque MA, Okuma E, Banu NA, Shimoishi Y, Nakamura Y, Murata Y (2009) Exogenous proline and glycinebetaine increase antioxidant enzyme activities and confer tolerance to cadmium stress in cultured tobacco cells. J Plant Physiol 166:1587–1597
Jan S, Parween T, Siddiqi TO, Mahmooduzzafar X (2012a) Effect of gamma radiation on morphological, biochemical and physiological aspects of plants and plant products. Environ Rev 20:17–39
Jan S, Parween T, Siddiqi TO, Mahmooduzzafar X (2012b) Anti-oxidant modulation in response to gamma radiation induced oxidative stress in developing seedlings of Psoralea corylifolia L. J Environ Radioact 113:142–149
Johnson MD, Sussex IM (1995) 1 L-myo-inositol 1-phosphate synthase from Arabidopsis thaliana. Plant Physiol 107:613–619
Joshi R, Ramanarao MV, Baisakh N (2013) Arabidopsis plants constitutively overexpressing a myo-inositol 1-phosphate synthase gene (SaINO1) from the halophyte smooth cordgrass exhibits enhanced level of tolerance to salt stress. Plant Physiol Biochem 65:61–66
Kanamaru N, Ito Y, Komori S, Saito M, Kato H, Takahashi S, Omura M, Soejima J, Shiratake K, Yamada K, Yamaki S (2004) Transgenic apple transformed by sorbitol-6-phosphate dehydrogenase cDNA switch between sorbitol and sucrose supply due to its gene expression. Plant Sci 167:55–61
Kaplan F, Guy CL (2004) β-Amylase induction and the protective role of maltose during temperature shock. Plant Physiol 135:1674–1684
Kaplan F, Guy CL (2005) RNA interference of Arabidopsis beta amylase8 prevents maltose accumulation upon cold shock and increases sensitivity of PSII photochemical efficiency to freezing stress. Plant J 44:730–743
Kasukabe Y, He L, Nada K, Misawa S, Ihara I, Tachibana S (2004) Overexpression of spermidine synthase enhances tolerance to multiple environmental stresses and up-regulates the expression of various stress-regulated genes in transgenic Arabidopsis thaliana. Plant Cell Physiol 45:712–722
Kavi Kishor PB, Sangam S, Amrutha RN, Sri Laxmi P, Naidu KR, Rao KRSS, Rao S, Reddy KJ, Theriappan P, Sreenivasulu N (2005) Regulation of proline biosynthesis, degradation, uptake and transport in higher plants: its implications in plant growth and abiotic stress tolerance. Curr Sci 88:424–438
Kawakami A, Sato Y, Yoshida M (2008) Genetic engineering of rice capable of synthesizing fructans and enhancing chilling tolerance. J Exp Bot 59:793–802
Kaya C, Sönmez O, Aydemir S, Dikilitaş M (2013) Mitigation effects of glycine betaine on oxidative stress and some key growth parameters of maize exposed to salt stress. Turk J Agric For 37:188–194
Kempa S, Krasensky J, Dal Santo S, Kopka J, Jonak C (2008) A central role of abscisic acid in stress-regulated carbohydrate metabolism. PLoS One 3:e3935
Kerepesi I, Galiba G, Banyai E (1998) Osmotic and salt stresses induced differential alteration in water-soluble carbohydrate content in wheat seedlings. J Agric Food Chem 46:5347–5354
Kintisch E (2009) Global warming: projections of climate change go from bad to worse, scientists report. Science 323:1546–1547
Kishor P, Hong Z, Miao GH, Hu CAA, Verma DPS (1995) Overexpression of [delta]-pyrroline-5-carboxylate synthetase increases proline production and confers osmotolerance in transgenic plants. Plant Physiol 108:1387–1394
Kiyosue T, Yoshiba Y, Yamaguchi-Shinozaki K, Shinozaki K (1996) A nuclear gene encoding mitochondrial proline dehydrogenase, an enzyme involved in proline metabolism, is upregulated by proline but downregulated by dehydration in Arabidopsis. Plant Cell 8:1323–1335
Koca M, Bor M, Ozdemir F, Turkan I (2007) The effect of salt stress on lipid peroxidation, antioxidative enzymes and proline content of sesame cultivars. Environ Exp Bot 60:344–351
Kotting O, Kossmann J, Zeeman SC, Lloyd JR (2010) Regulation of starch metabolism: the age of enlightenment? Curr Opin Plant Biol 13:321–329
Kovacs Z, Simon-Sarkadi L, Szucs A, Kocsy G (2010) Differential effects of cold, osmotic stress and abscisic acid on polyamine accumulation in wheat. Amino Acids 38:623–631
Koyro HW, Ahmad P, Geissler N (2012) Abiotic stress responses in plants: an overview. In: Ahmad P, Prasad MNV (eds) Environmental adaptations and stress tolerance of plants in the era of climate change. Springer Science and Business Media, Germany, pp 1–28
Krasensky J, Jonak C (2012) Drought, salt, and temperature stress-induced metabolic rearrangements and regulatory networks. J Exp Bot 63:1593–1608
Kumar V, Shriram V, Kishor PBK, Jawali N, Shitole MG (2010) Enhanced proline accumulation and salt stress tolerance of transgenic indica rice by over-expressing P5CSF129A gene. Plant Biotechnol Rep 4:37–48
Kumriaa R, Rajam MV (2002) Ornithine decarboxylase transgene in tobacco affects polyamines, in vitro-morphogenesis and response to salt stress. J Plant Physiol 159:933–990
Li HJ, Yang AF, Zhang XC, Gao F, Zhang JR (2007) Improving freezing tolerance of transgenic tobacco expressing sucrose: sucrose 1-fructosyltransferase gene from Lactuca sativa. Cell Tisssue Organ Cult 89:37–48
Li F, Lei H, Zhao X, Tian R, Li T (2012) Characterization of three sorbitol transporter genes in micropropagated apple plants grown under drought stress. Plant Mol Biol Rep 30:123–130
Liang D, Cui M, Wu S, Ma FW (2012) Genomic structure, sub-cellular localization, and promoter analysis of the gene encoding sorbitol-6–phosphate dehydrogenase from apple. Plant Mol Biol Rep 30:904–914
Liu C, Zhao L, Yu G (2011) The dominant glutamic acid metabolic flux to produce gamma-amino butyric acid over proline in Nicotiana tabacum leaves under water stress relates to its significant role in antioxidant activity. J Integr Plant Biol 53:608–618
Livingston DP, Hincha DK, Heyer AG (2009) Fructan and its relationship to abiotic stress tolerance in plants. Cell Mol Life Sci 66:2007–2023
Llanes A, Bertazza G, Palacio G, Luna V (2013) Different sodium salts cause different solute accumulation in the halophyte Prosopis strombulifera. Plant Biol 15:118–125
Loescher WH, Tyson RH, Everard JD, Redgwell RJ, Bieleski RL (1992) Mannitol synthesis in higher plants: evidence for the role and characterization of a NADPH-dependent mannose 6-phosphate reductase. Plant Physiol 98:1396–1402
Lopez M, Tejera NA, Iribarne C, Lluch C, Herrera-Cervera JA (2008) Trehalose and trehalase in root nodules of Medicago truncatula and Phaseolus vulgaris in response to salt stress. Physiol Plant 134:575–582
Lugan R, Niogret MF, Leport L, Guegan JP, Larher F, Savoure A, Kopka J, Bouchereau A (2010) Metabolome and water homeostasis analysis of Thellungiella salsuginea suggests that dehydration tolerance is a key response to osmotic stress in this halophyte. Plant J 64:215–229
Madden TD, Bally MB, Hope MJ, Cullis PR, Schieren HP, Janoff AS (1985) Protection of large unilamellar vesicles by trehalose during dehydration: retention of vesicle contents. Biochim Biophys Acta 817:67–74
Maevskaya SN, Nikolaeva MK (2013) Response of antioxidant and osmoprotective systems of wheat seedlings to drought and rehydration. Russ J Plant Physiol 60:343–350
Majumder AL, Johnson MD, Henry SA (1997) 1L-myo-inositol-1-phosphate synthase. Biochim Biophys Acta 1348:245–256
Majumder AL, Sengupta S, Goswami S (2010) Osmolyte regulation in abiotic stress. In: Pareek A, Sopory SK, Bohnert HJ, Govindjee (eds) Abiotic stress adaptation in plants: physiological, molecular and genomic foundation. Springer Science Business Media BV, Germany, pp 349–370
Miller G, Honig A, Stein H, Suzuki N, Mittler R, Zilberstein A (2009) Unraveling delta1-pyrroline-5-carboxylate-proline cycle in plants by uncoupled expression of proline oxidation enzymes. J Biol Chem 284:26482–26492
Mishra S, Dubey RS (2006) Inhibition of ribonuclease and protease activities in arsenic exposed rice seedlings: role of proline as enzyme protectant. J Plant Physiol 163:927–936
Moradi F, Ismail AM (2007) Responses of photosynthesis, chlorophyll fluorescence and ROS-scavenging systems to salt stress during seedling and reproductive stages in rice. Ann Bot 99:1161–1173
N’Guyen A, Lamant A (1988) Pinitol and myo-inositol accumulation in waterstressed seedling of maritime pine. Phytochemistry 27:3423–3427
Nawaz K, Ashraf M (2010) Exogenous application of glycine betaine modulates activities of antioxidants in maize plants subject to salt stress. J Agron Crop Sci 196:28–37
Nelson DE, Koukoumanos M, Bohnert HJ (1999) Myo-inositol-dependent sodium uptake in ice plant. Plant Physiol 119:165–172
Nounjan N, Theerakulpisut P (2012) Effects of exogenous proline and trehalose on physiological responses in rice seedlings during salt-stress and after recovery. Plant Soil Environ 58:309–315
Nounjan N, Nghia PT, Theerakulpisut P (2012) Exogenous proline and trehalose promote recovery of rice seedlings from salt-stress and differentially modulate antioxidant enzymes and expression of related genes. J Plant Physiol 169:596–604
Olien CR, Clark JL (1995) Freeze-induced changes in carbohydrates associated with hardiness of barley and rye. Crop Sci 35:496–502
Parida AK, Das AB (2005) Salt tolerance and salinity effects on plants: a review. Ecotoxicol Environ Safe 60:324–349
Park EJ, Jeknic Z, Sakamoto A, DeNoma J, Yuwansiri R, Murata N, Chen TH (2004) Genetic engineering of glycinebetaine synthesis in tomato protects seeds, plants, and flowers from chilling damage. Plant J 40:474–487
Park EJ, Jeknic Z, Chen TH, Murata N (2007) The codA transgene for glycinebetaine synthesis increases the size of flowers and fruits in tomato. Plant Biotechnol J 5:422–430
Patra B, Ray S, Richter A, Majumder AL (2010) Enhanced salt tolerance of transgenic tobacco plants by coexpression of PcINO1 and McIMT1 is accompanied by increased level of myo-inositol and methylated inositol. Protoplasma 245:143–152
Paul MJ, Cockburn W (1989) Pinitol, a compatible solute in Mesembryanthemum crystallinum L.? J Exp Bot 40:1093–1098
Paul MJ, Primavesi LF, Jhurreea D, Zhang Y (2008) Trehalose metabolism and signaling. Annu Rev Plant Biol 59:417–441
Pilonsmits EAH, Ebskamp MJM, Paul MJ, Jeuken MJW, Weisbeek PJ, Smeekens SCM (1995) Improved performance of transgenic fructan-accumulating tobacco under drought stress. Plant Physiol 107:125–130
Pommerrenig B, Papini-Terzi FS, Sauer N (2007) Differential regulation of sorbitol and sucrose loading into the phloem of Plantago major in response to salt stress. Plant Physiol 144:1029–1038
Popp M (1984) Chemical composition of Australian mangroves. II. Low molecular weight carbohydrates. Z Pflanzenphysiol 113:411–421
Pramanik MH, Imai R (2005) Functional identification of a trehalose 6-phosphate phosphatase gene that is involved in transient induction of trehalose biosynthesis during chilling stress in rice. Plant Mol Biol 58:751–762
Premachandra GS, Hahn GT, Rhodes D, Joly RJ (1995) Leaf water relations and solute accumulation in two grain sorghum lines exhibiting contrasting drought tolerance. J Exp Bot 46:1833–1841
Quinet M, Ndayiragije A, Lefevre I, Lambillotte B, Dupont-Gillain CC, Lutts S (2010) Putrescine differently influences the effect of salt stress on polyamine metabolism and ethylene synthesis in rice cultivars differing in salt resistance. J Exp Bot 61:2719–2733
Radhakrishnan R, Lee IJ (2013) Spermine promotes acclimation to osmotic stress by modifying antioxidant, abscisic acid, and jasmonic acid signals in Soybean. J Plant Growth Regul 32:22–30
Rammesmayer G, Pichorner H, Adams P, Jensen RG, Bohnert HJ (1995) Characterization of IMT1, myo-inositol-O-methyltransferase, from Mesembryanthemum crystallinum. Arch Biochem Biophys 322:183–188
Reguera M, Peleg Z, Blumwald E (2012) Targeting metabolic pathways for genetic engineering abiotic stress-tolerance in crops. Biochim Biophys Acta 1819:186–194
Renault H, Roussel V, El Amrani A, Arzel M, Renault D, Bouchereau A, Deleu C (2010) The Arabidopsis pop2-1 mutant reveals the involvement of GABA transaminase in salt stress tolerance. BMC Plant Biol 10:20
Renault H, El Amrani A, Berger A, Mouille G, Soubigou-Taconnat L, Bouchereau A, Deleu C (2013) γ-Aminobutyric acid transaminase deficiency impairs central carbon metabolism and leads to cell wall defects during salt stress in Arabidopsis roots. Plant Cell Environ 36:1009–1018
Rizhsky L, Liang HJ, Shuman J, Shulaev V, Davletova S, Mittler R (2004) When defense pathways collide. The response of Arabidopsis to a combination of drought and heat stress. Plant Physiol 134:1683–1696
Rontein D, Basset G, Hanson AD (2002) Metabolic engineering of osmoprotectant accumulation in plants. Metab Eng 4:49–56
Rosgen J (2007) Molecular basis of osmolyte effects on protein and metabolites. Methods Enzymol 428:459–486
Roychoudhury A, Basu S, Sarkar S, Sengupta D (2008) Comparative physiological and molecular responses of a common aromatic indica rice cultivar to high salinity with non-aromatic indica rice cultivars. Plant Cell Rep 27:1395–1410
Rumpho ME, Edwards GE, Loescher WH (1983) A pathway for photosynthetic carbon flow to mannitol in celery leaves: activity and localization of key enzymes. Plant Physiol 73:869–873
Sakamoto A, Murata N (2000) Genetic engineering of glycinebetaine synthesis in plants: current status and implications for enhancement of stress tolerance. J Exp Bot 51:81–88
Sanchez DH, Siahpoosh MR, Roessner U, Udvardi M, Kopka J (2008) Plant metabolomics reveals conserved and divergent metabolic responses to salinity. Plant Physiol 132:209–219
Schulze ED, Beck E, Müller-Hohenstein K (2002) Pflanzenökologie. Spektrum Akademischer, Heidelberg
Sengupta S, Majumder AL (2009) Insight into the salt tolerance factors of a wild halophytic rice, Porteresia coarctata: a physiological and proteomic approach. Planta 229:911–929
Sengupta S, Patra B, Ray S, Majumder AL (2008) Inositol methyl tranferase from a halophytic wild rice, Porteresia coarctata Roxb. (Tateoka): regulation of pinitol synthesis under abiotic stress. Plant Cell Environ 31:1442–1459
Sharma P, Dubey RS (2005) Modulation of nitrate reductase activity in rice seedlings under aluminium toxicity and water stress: role of osmolytes as enzyme protectant. J Plant Physiol 162:854–864
Shelp BJ, Bown AW, McLean MD (1999) Metabolism and functions of gamma-aminobutyric acid. Trends Plant Sci 4:446–452
Shen B, Jensen RG, Bohnert HJ (1997) Increased resistance to oxidative stress in transgenic plants by targeting mannitol biosynthesis to chloroplasts. Plant Physiol 113:1177–1183
Shi J, Fu X, Peng T, Huang X, Fan Q, Liu J (2010) Spermine pretreatment confers dehydration tolerance of citrus in vitro plants via modulation of antioxidative capacity and stomatal response. Tree Physiol 30:914–922
Shu S, Yuan LY, Guo SR, Sun J, Yuan YH (2013) Effects of exogenous spermine on chlorophyll fluorescence, antioxidant system and ultrastructure of chloroplasts in Cucumis sativus L. under salt stress. Plant Physiol Biochem 63:209–216
Shulaev V, Cortes D, Miller G, Mittler R (2008) Metabolomics for plant stress response. Plant Physiol 132:199–208
Smirnoff N, Cumbes QJ (1989) Hydroxyl radical scavenging activity of compatible solutes. Phytochemistry 28:1057–1060
Song HM, Xu XB, Wang H, Wang HZ, Tao YZ (2010) Exogenous gamma-aminobutyric acid alleviates oxidative damage caused by aluminium and proton stresses on barley seedlings. J Sci Food Agric 90:1410–1416
Sorkheh K, Shiran B, Khodambashi M, Rouhi V, Mosavei S, Sofo A (2012) Exogenous proline alleviates the effects of H2O2 induced oxidative stress in wild almond species. Russ J Plant Physiol 59:788–798
Spollen WG, Nelson CJ (1994) Response of fructan to water-deficit in growing leaves of tall fescue. Plant Physiol 106:329–336
Stiller I, Dulai S, Kondrák M, Tarnai R, Szabó L, Toldi O, Bánfalvi Z (2008) Effects of drought on water content and photosynthetic parameters in potato plants expressing the trehalose-6-phosphate synthase gene of Saccharomyces cerevisiae. Planta 227:299–308
Stoop JHM, Williamson JD, Pharr DM (1996) Mannitol metabolism in plants: a method for coping with stress. Trends Plant Sci 1:139–144
Street TO, Bolen DW, Rose GD (2006) A molecular mechanism for osmolyte-induced protein stability. Proc Natl Acad Sci U S A 103:13997–14002
Szabados L, Savoure A (2010) Proline: a multifunctional amino acid. Trends Plant Sci 15:89–97
Szekely G, Abraham E, Cseplo A, Rigo G, Zsigmond L, Csiszar J, Ayaydin F, Strizhov N, Jasik J, Schmelzer E, Koncz C, Szabados L (2008) Duplicated P5CS genes of Arabidopsis play distinct roles in stress regulation and developmental control of proline biosynthesis. Plant J 53:11–28
Tari I, Kiss G, Deér AK, Csiszár J, Erdei L, Gallé A, Gémes K, Horváth F, Poór P, Szepesi Á, Simon L (2010) Salicylic acid increased aldose reductase activity and sorbitol accumulation in tomato plants under salt stress. Biol Plant 54:677–683
Tetlow IJ, Morell MK, Emes MJ (2004) Recent developments in understanding the regulation of starch metabolism in higher plants. J Exp Bot 55:2131–2145
Todaka D, Matsushima H, Morohashi Y (2000) Water stress enhances beta-amylase activity in cucumber cotyledons. J Exp Bot 51:739–745
Urano K, Yoshiba Y, Nanjo T, Ito T, Yamaguchi-Shinozaki K, Shinozaki K (2004) Arabidopsis stress-inducible gene for arginine decarboxylase AtADC2 is required for accumulation of putrescine in salt tolerance. Biochem Biophys Res Commun 313:369–375
Valerio C, Costa A, Marri L, Issakidis-Bourguet E, Pupillo P, Trost P, Sparla F (2011) Thioredoxin-regulated beta-amylase (BAM1) triggers diurnal starch degradation in guard cells, and in mesophyll cells under osmotic stress. J Exp Bot 62:545–555
Valluru R, Van den Ende W (2008) Plant fructans in stress environments: emerging concepts and future prospects. J Exp Bot 59:2905–2916
Van Houtte H, Vandesteene L, Lopez-Galvis L, Lemmens L, Kissel E, Carpentier S, Feil R, Avonce N, Beeckman T, Lunn JE, Van Dijck P (2013) Overexpression of the trehalase gene AtTRE1 leads to increased drought stress tolerance in Arabidopsis and is involved in abscisic acid-induced stomatal closure. Plant Physiol 161:1158–1171
Vijn I, Smeekens S (1999) Fructan: more than a reserve carbohydrate? Plant Physiol 120:351–359
Vogel G, Aeschbacher RA, Muller J, Boller T, Wiemken A (1998) Trehalose-6-phosphate phosphatases from Arabidopsis thaliana: identification by functional complementation of the yeast tps2 mutant. Plant J 13:673–683
Vogel G, Fiehn O, Jean-Richard-dit-Bressel L, Boller T, Wiemken A, Aeschbacher RA, Wingler A (2001) Trehalose metabolism in Arabidopsis: occurrence of trehalose and molecular cloning and characterization of trehalose-6-phosphate synthase homologues. J Exp Bot 52:1817–1826
Wang W, Vinocur B, Altman A (2003) Plant responses to drought, salinity and extreme temperatures: towards genetic engineering for stress tolerance. Planta 218:1–14
Wei W, Dai X, Wang Y, Chuan Y, Gou CB, Chen F (2010a) Cloning and expression analysis of 1 L-myo-inositol-1-phosphate synthase gene from Ricinus communis L. Z Naturforsch C 65:501–507
Wei A, He CM, Li B, Li N, Zhang JR (2010b) The pyramid of transgenes TsVP and BetA effectively enhances the drought tolerance of maize plants. Plant Biotechnol J 9:216–229
Wood AJ, Saneoka H, Rhodes D, Joly RJ, Goldsbrough PB (1996) Betaine aldehyde dehydrogenase in sorghum. Plant Physiol 110:1301–1308
Wormit A, Trentmann O, Feifer I, Lohr C, Tjaden J, Meyer S, Schmidt U, Martinoia E, Neuhaus HE (2006) molecular identification and physiological characterization of a novel monosaccharide transporter from Arabidopsis involved in vacuolar sugar transport. Plant Cell 18:3476–3490
Yamada Y, Fukutoku Y (1985) Effect of water stress on soybean metabolism. In: Shanmugasundaram S, Sulzberger EW, Mclean BJ (eds) Soybean in tropical and subtropical cropping systems. Asian Vegetation Research and Development Center, Shanhua, Taiwan, pp 373–382
Yamaguchi K, Takahashi Y, Berberich T, Imai A, Miyazaki A, Takahashi T, Michael A, Kusano T (2006) The polyamine spermine protects against high salt stress in Arabidopsis thaliana. FEBS Lett 580:6783–6788
Yancey PH (2005) Organic osmolytes as compatible, metabolic and counteracting cytoprotectants in high osmolarity and other stresses. J Exp Biol 208:2819–2830
Yang X, Liang Z, Wen X, Lu C (2008) Genetic engineering of the biosynthesis of glycinebetaine leads to increased tolerance of photosynthesis to salt stress in transgenic tobacco plants. Plant Mol Biol 66:73–86
Yang SL, Lan SS, Gong M (2009) Hydrogen peroxide-induced proline and metabolic pathway of its accumulation in maize seedlings. J Plant Physiol 166:1694–1699
Yano R, Nakamura M, Yoneyama T, Nishida I (2005) Starch related alpha-glucan/water dikinase is involved in the cold-induced development of freezing tolerance in Arabidopsis. Plant Physiol 138:837–846
Yoshida KT, Wada T, Koyama H, Mizobuchi-Fukuoka R, Naito S (1999) Temporal and spatial patterns of accumulation of the transcript of Myo-inositol-1-phosphate synthase and phytin-containing particles during seed development in rice. Plant Physiol 119:65–72
Yoshida KT, Fujiwara T, Naito S (2002) The synergistic effects of sugar and abscisic acid on myo-inositol-1-phosphate synthase expression. Physiol Plant 114:581–587
Zeeman SC, Thorneycroft D, Schupp N, Chapple A, Weck M, Dunstan H, Haldimann P, Bechtold N, Smith AM, Smith SM (2004) Plastidial alpha-glucan phosphorylase is not required for starch degradation in Arabidopsis leaves but has a role in the tolerance of abiotic stress. Plant Physiol 135:849–858
Zhang J, Ta W, Yang XH, Zhang HX (2008) Plastid-expressed choline monooxygenase gene improves salt and drought tolerance through accumulation of glycine betaine in tobacco. Plant Cell Rep 27:1113–1124
Zhang Y, Hu XH, Shi Y, Zou ZR, Yan F, Zhao YY, Zhang H, Zhao JZ (2013) Beneficial role of exogenous spermidine on nitrogen metabolism in tomato seedlings exposed to saline-alkaline stress. J Am Soc Hortic Sci 138:38–49
Zhifang G, Loescher WH (2003) Expression of a celery mannose 6-phosphate reductase in Arabidopsis thaliana enhances salt tolerance and indices biosynthesis of both mannitol and a glucosyl-mannitol dimer. Plant Cell Environ 26:275–283
Acknowledgements
The authors would like to thank Prof. Laszlo SZABADOS (Institute of Plant Biology, Biological Research Center, Szeged, Hungary) for his precious help.
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Sağlam, A., Jan, S. (2014). Importance of Protective Compounds in Stress Tolerance. In: Ahmad, P., Wani, M. (eds) Physiological Mechanisms and Adaptation Strategies in Plants Under Changing Environment. Springer, New York, NY. https://doi.org/10.1007/978-1-4614-8600-8_9
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