Effect of Salinity Stress on Plants and Its Tolerance Strategies: A Review PDF

Environ Sci Pollut Res (2015) 22:4056–4075 DOI 10.1007/s11356-014-3739-1 REVIEW ARTICLE Effect of salinity stress on plants and its tolerance strategies: a review Parul Parihar & Samiksha Singh & Rachana Singh & Vijay Pratap Singh & Sheo Mohan Prasad Received: 27 July 2014 / Accepted: 17 October...

Environ Sci Pollut Res DOI 10.1007/s11356-014-3739-1 REVIEW ARTICLE Effect of salinity stress on plants and its tolerance strategies: a review Parul Parihar & Samiksha Singh & Rachana Singh Vijay Pratap Singh & Sheo Mohan Prasad Received: 27 July 2014 / Accepted: 17 October 2014 # Springer-Verlag Berlin Heidelberg 2014 Abstract The environmental stress is a major area of sci- entific concern because it constraints plant as well productivity. This situation has been further worsened by anthropogenic activities. Therefore, there is a much scien- tific saddle on researchers to enhance crop productivity under environmental stress in order to cope with the in- creasing food demands. The abiotic stresses such as salin- ity, drought, cold, and heat negatively influence the surviv- al, biomass production and yield of staple food crops. According to an estimate of FAO, over 6 % of the world’s land is affected by salinity. Thus, salinity stress appears to be a major constraint to plant and crop productivity. Here, we review our understanding of salinity impact on various aspects of plant metabolism and its tolerance strategies in plants. Keywords Genomics. Metabolomics. Plant productivity. Proteomics. Salinity stress. Salinity tolerance. Transcriptomics Responsible editor: Philippe Garrigues P. Parihar : R. Singh : S. M. Prasad (*) Ranjan Plant Physiology and Biochemistry Laboratory, Department of Botany, University of Allahabad, Allahabad 211002, India e-mail: [email protected] and Na2SO4 and sometimes also contain appreciable quanti- ties of Cl− and SO4− of Ca2+and Mg2+; these soils contain sufficient neutral soluble salts to pose negative effect on growth of most crop plants, and (2) sodic soils—these soils contain Na+ salts capable of alkaline hydrolysis, mainly Na2CO3. In this review article, type and causes of salinity, impact of salinity on plants, and salt tolerance strategies of data-cfemail="77011e1d160e07051603160759160237101a161e1b5914181a">[email protected] plants are discussed. 4057 Table 1 Global estimate of secondary salinization in the world’s irrigated soils (source Ghassemi et al. 1995) Country Total land area Area irrigated Area of irrigated land cropped that is salt affected salts over Mha Mha % Mha % the soil or China 97 45 46 6.7 15 India 169 42 25 7.0 17 Soviet Union 233 21 9 3.7 18 United States 190 18 10 4.2 23 Pakistan 21 16 78 4.2 26 Iran 15 6 39 1.7 30 Thailand 20 4 20 0.4 10 Egypt 3 3 100 0.9 33 Australia 47 2 4 0.2 9 Argentina 36 2 5 0.6 34 South Africa 13 1 9 0.1 9 Subtotal 843 159 19 29.6 20 World 1,474 227 15 45.4 20 The effects of salinity on plants Salts in the soil water may inhibit plant growth for two reasons. Firstly, the presence of salt in the soil solution reduces the ability of the plant to take up water and this leads to reductions in the growth rate. This is referred to as the osmotic or water-deficit effect of salinity. Secondly, if excessive amounts of salt enter the plant in the transpiration stream, there will be injury to cells in the transpiring leaves and this may cause further reductions in growth. This is called the salt- specific or ion-excess effect of salinity (Greenway and Munns 1980). These salinity effects has threefold effects viz. it re- duces water potential and causes ion imbalance or distur- bances in ion homeostasis and toxicity; this altered water status leads to initial growth reduction and limitation of plant productivity. The detrimental effect is observed at the whole- plant level as death of plants or decrease in productivity. Salt stress affects all the major processes such as germination, growth, photosynthetic pigments and photosynthesis, water relation, nutrient imbalance, oxidative stress, and yield. These are discussed under separate headings. Germination tons of salt. Seed germination is one of the most fundamental and vital phases in the growth cycle of a plant that determines the yield. However, it has been established that salinity adversely affects the process of germination in various plants like Posidonia (Fernández-Torquemada and Sánchez-Lizaso 2013), Oryza sativa (Xu et al. 2011), Triticum aestivum (Akbarimoghaddam et al. 2011), Zea mays (Carpıcı et al. 2009; Khodarahmpour Environ Sci Pollut Res (2015) 22:4056–4075 growth response to salinity given by Munns (1993, 2005; Fig. 2). Phase 1: The first phase of the growth response results from the effect of salt outside the plant. The salt in the soil solution reduces leaf growth and to a lesser extent root growth (Munns 1993). The cellular and metabolic processes involved are in common to drought-affected plants. Neither Na+ nor Cl− builds up in growing tissues at concentrations that inhibit growth: meristematic tissues are fed largely in the phloem from which salt is effectively excluded, and rapidly elongating cells can accommodate the salt that arrives in the xylem within their expanding vacuoles. Phase 2: The second phase of the growth response results from the toxic effect of salt inside the plant. The salt taken up by the plant concentrates in old leaves: continued transport into transpiring leaves over a long period eventually results in very high Na+ and Cl−concentrations, and the leaves die. The cause of injury is probably the salt load exceeding the ability of cells to compartmentalize salts in the vacuole. Salts would then build up rapidly in the cytoplasm and inhibit enzyme activity. Alternatively, they might build up in the cell walls and dehydrate the cell. The excessive salt concentration cor- respondingly increases the osmotic potential of the soil that restricts the water uptake by plants. The Na+ and Cl− ions are the major ions that produce many physiological disorders and detrimental effects on plants. However, Na+ is the primary ion as it interferes with the uptake of potassium (K+) ion and disturbs stomatal regulation that ultimately causes water loss while the Cl− ion disturbs the chlorophyll production and causes chlorotic toxicity. But, Cl− is more dangerous than Na+ (Tavakkoli et al. 2011). Moreover, the need of Cl− in plant is essential as well and is required for the regulation of turgor pressure and pH and enzyme activities in the cyto- plasm. Dang et al. (2008), on the basis of number of field trials, concluded that Cl− concentration in the soil was more important to growth and yield reduction than Na+ and the critical level (defined as the concentration that reduces the growth or yield by 10 %) of subsoil Cl− concentration was time after sowing at Fig. 2 Overview of the two-phase growth response to salinity for plant differing in salt sensitivity (adopted from Munns 2005) 4059 highest ion accumulation was found in leaves followed by stem and root suggesting a positive relationship between Na+ and Cl− concentration. The Ca2+ content was reduced in shoots and leaves of A. griffithii plants grown at high salinity; however, being stable in roots and the K+ content was reduced with increased levels of salinity, particularly in leaves. On the other hand, Mg2+ concentration was not much affected in stems and roots but the decrease in leaf was more prominent (Khan et al 2000). Decrease in Ca2+ and Mg2+ content of leaves upon salinity stress suggests increased membrane sta- bility and decreased chlorophyll content, respectively (Parida et al. 2004). Despite the fact that most plants accumulate both Na+ and Cl− ions in high concentrations in their shoot tissues when grown in saline soils, Cl− toxicity is also an important cause of growth reduction. Tavakkoli et al. (2011) studied the extent to which specific ion toxicity of Na+ and Cl− reduces the growth of four barley genotypes grown in saline soils under varying salinity treatments. High Na+, Cl−, and NaCl separately reduced the growth of barley; however, the reduc- tions in growth and photosynthesis were greatest under NaCl stress and were mainly additives of the effects of Na+ and Cl− stress. They also reported that Na+ and Cl− exclusion among barley genotypes are independent mechanisms and different genotypes expressed different combinations of the two mech- anisms. High concentrations of Na+ reduced K+ and Ca2+ uptake and reduced photosynthesis mainly by reducing sto- matal conductance, while high Cl− concentration reduced the includes three compart- and Cl− homeostasis across the plasma membrane and tonoplast. Included are organelles (chloroplast (chlcp), mitochondrion (mitmt), and peroxi- some (perox) for which the importance of ROS-scavenging is implicated responsible for Na+ Environ Sci Pollut Res (2015) 22:4056–4075 control, the pigment contents decreased on an average by 31 % for total chlorophyll, 22 % for chlorophyll a, 45 % for chlorophyll b, 14 % for carotene, and 19 % for xanthophylls (Saha et al. 2010). In one of the studies in cucumber, it has been shown that total leaf chlorophyll contents significantly decreased with an increasing NaCl levels. The decrease in total chlorophyll contents was 12, 21, and 30 % at 2 and 3, and 5 dS m−1 of salt stress, respectively, compared to non-treated plants (Khan et al. 2013). Associated with the decline in pigment levels, there was an average 16 % loss of the intensity of chlorophyll fluorescence as well. Usually, there is domi- nance of chlorophyll “a” over chlorophyll “b” in plants but their values become closer with increasing salinity (Mane et al. 2010). The decrease in chlorophyll content under stress is a commonly reported phenomenon, and in various studies, this may be due to different reasons, one of them is related to membrane deterioration (Mane et al. 2010). Photosystem II (PS II) is a relatively sensitive component of the photosynthetic system with respect to salt stress (Allakhverdiev et al. 2000). A considerable decrease in the efficiency of PS II, electron transport chain (ETC), and assim- ilation rate of CO2 under the influence of salinity has been noticed (Piotr and Grazyna 2005). Demetriou et al. (2007) noticed alterations in photosynthetic characteristics of Scenedesmus obliquus that result into declined biomass accu- mulation. In citrus, salinity stress decreased growth by reduc- ing of net photosynthetic rate, stomatal conductance, perfor- mance of PSII, and photosynthetic efficiency (Lòpez-Climent et al. 2008). Kalaji et al. (2011) reported that salinity stress affects growth of barley by altering chlorophyll fluorescence (PS II) and function of oxygen evolving complex. Furthermore, Mittal et al. (2012) observed that salt stress affects growth of Brassica juncea by affecting photosynthetic (PS II) and electron transport rates, and D1 protein. There are some other factors that reduce photosynthetic rates under salt stress: dehydration of cell membranes which reduce their permeability to carbon dioxide, salt toxicity, enhanced senes- cence, changes in enzyme activity induced by alterations in cytoplasmic structure, and negative feedback by reduced sink activity (Iyengar and Reddy 1996). al. 2011). In Water relation Water potential is an important physiological parameter for determining the water status of the plants (Parida and Das 2005). According to Romero-Aranda et al. (2001), a increase of salt in the root medium can lead to a decrease in leaf water potential and, hence, may affect many plant processes. At very low soil water potentials, this condition interferes with plant’s ability to extract water from the soil and maintain turgor. However, at low or moderate salt concentration (higher soil water potential), plants adjust osmotically (accumulate sol- utes) and maintain a potential gradient for the influx of water. 4061 damage, and/or interact with other vital constituents of plant cells. Salt stress can lead to stomatal closure, which reduces carbon dioxide availability in the leaves and inhibits carbon fixation, exposing chloroplasts to excessive excitation energy which in turn increase the generation of ROS such as super- oxide (O2 –), hydrogen peroxide (H2O2), hydroxyl radical (OH ), and singlet oxygen (1O2; Parida and Das 2005; Ahmad and Sharma 2008; Ahmad et al. 2010a, 2011). On the other hand, as salt stress is complex and imposes a water deficit because of osmotic effects on a wide variety of meta- bolic activities (Greenway and Munns 1980; Cheeseman 1988). This water deficit leads to the formation of ROS (Halliwell and Gutteridge 1985; Elstner 1987). ROS are high- ly reactive and may cause cellular damage through oxidation of lipids, proteins, and nucleic acids (Apel and Hirt 2004; Ahmad et al. 2010a,b). In many plant studies, it was observed that production of ROS is increased under saline conditions and ROS-mediated membrane damage has been demonstrated to be a major cause of the cellular toxicity by salinity in different crop plants such as rice, tomato, citrus, pea, and mustard (Gueta-Dahan et al. 1997; Dionisio-Sese and Tobita 1998; Mittova et al. 2004; Ahmad et al. 2009, 2010b). In one of the studies, it has been shown that long-term salinity treatments (EC 5.4 and 10.6 dS m−1, 60 days) causes signif- icant increase in H2O2 and lipid peroxidation in wheat seed- lings, which was higher in salt-sensitive cultivar than salt tolerant cultivar (Sairam et al. 2002). In a recent study, in- creased lipid peroxidation and levels of H2O2 were observed with increased salinity in Brassica napus (Hasanuzzaman and Fujita 2011a) and Triticum aestivum (Hasanuzzaman and Fujita (2011b)). It has been shown that the production of ROS during environmental stresses such as salinity is one of the main causes for decreases in crop productivity (Halliwell and Gutteridge 1989; Asada 1994). Therefore, regulation of ROS is a crucial process to avoid unwanted cellular cytotox- icity and oxidative damage (Halliwell and Gutteridge 1989). Yield The above mentioned effects of salt stress on plants ultimately lead to reduction of yield of crop which is the most countable effect of salt stress in agriculture. Different yield components of Vigna radiate were significantly affected by salinity stress as reported by Nahar and Hasanuzzaman (2009). Numbers of pods per plant, seeds per pod, and seed weight were negatively correlated with salinity levels. The reproductive growth of V. radiata was also affected by salinity as the number of pods per plant substantially decreased with increasing salinity levels. An application of 250 mM NaCl reduced 77, 73, and 66 % yield in V. radiata cv. BARI mung-2, BARI mung-5, and BARI mung-6, respectively over control (Nahar and Hasanuzzaman 2009). The reduction of yield and its compo- nents under salt stress condition may be attributed to low Environ Sci Pollut Res (2015) 22:4056–4075 Genomic level Tolerant plants may possess some unique stress-responsive genes which are absent in susceptible plants (differences at genome structure level). Profiling at the genome level, when combined with systematic genetic analysis, promises to reveal much of the signaling networks that control stress tolerance. Munns (2005) reported genes which could increase salt toler- ance fall into three main functional groups as follows: (1) those that control salt uptake and transport, (2) those that have an osmotic or protective function, and (3) those that could make a plant grow more quickly in saline soil. under stress Genes that control salt uptake and transport to salt stress Several Arabidopsis salt overly sensitive (SOS) mutants, de- fective in salt tolerance, have been characterized (Zhu et al. 1998) The sos mutants are specifically hypersensitive to high external Na+ or Li+ and also unable to grow under very low external K+ concentrations (Zhu et al. 1998). Allelic tests indicated that the sos mutants define three SOS loci, i.e., SOS1, SOS2, and SOS3 (Martínez-Atienza et al. 2007). The SOS1 encodes for a plasma membrane Na+/H+ antiporter, responsible for the exclusion of sodium in the apoplast (Shi et al. 2000). The SOS2 gene encodes a serine/threonine type protein kinase, which activates SOS1 (Liu et al. 2000). The SOS3 gene encodes an EF-hand type calcium binding protein with similarities to animal neuronal calcium sensors and the yeast calcineurin B subunit (Mahajan et al. 2008). In yeast, calcineurin plays a central role in the regulation of Na+ and K+ transport. Mutations in calcineurin B lead to increased sensi- tivity of yeast cells to growth inhibition by Na+ and Li+ stresses (Mendoza et al. 1994). The SOS2 physically interacts with and is activated by SOS3 (Halfter et al. 2000). Therefore, SOS2 and SOS3 define a regulatory pathway for Na+ and K+ homeostasis and salt tolerance in plants. Besides being regu- lated by SOS2, SOS1 activity may also be regulated by SOS4. The SOS4 catalyzes the formation of pyridoxal-5- phosphate, a cofactor that may serve as a ligand for SOS1, because the latter contains a putative binding sequence for this cofactor (Shi and Zhu 2002). Quan et al. (2007) reported SOS3-like calcium-binding protein8 (SCaBP8), which along with SOS3 is required for the activation of SOS2. Lin et al. (2009)further reported that SOS2 also phosphorylates and activates down- stream SCaBP8, but not SOS3. Among the three SOS loci, SOS1 plays the greatest role in plant salt tolerance. Compared with sos2 and sos3 mutant plants, sos1 mutant plants are even more sensitive to Na+ and Li+ stresses (Zhu 2004). Double mutant analysis indicated that SOS1 functions in the same pathway as SOS2 and SOS3 (Liu et al. 2000). At the plasma membrane, a family of P-type H+-ATPases serves as the primary pump that generates a proton motive force for driving the active transport of other solutes; include K+ and Na+ (Sze 4063 proteins that protect the formation or stability of other pro- teins. There are four main classes of solutes that could have an osmotic or protective role, which are as follows: the N- containing solutes such as proline and glycine betaine; sugars such as sucrose and raffinose; straight-chain polyhydric alco- hols (polyols) such as mannitol and sorbitol; and cyclic polyhydric alcohols (cyclic polyols). Proteins with protective roles of unknown function include late-embryogenesis- abundant proteins (LEAs) and their close relatives with dehydrins. The osmolyte(s) and their corresponding gene(s) whose overexpression imparts salt tolerance in different plant species have been shown in Table 2. Genes that control cell and tissue growth rates Candidate genes controlling growth are probably involved in signaling pathways that start with a sensor and involve hormones, transcription factors, protein kinases, protein phosphatise, and other signaling molecules such as cal- modulin binding proteins. It is highly likely that such genes are common to drought stress (reviewed by Chaves et al. 2003) and are common to other stresses, such as cold, and soil conditions that reduce growth such as soil hard- ness caused by compaction or sodicity. Many are induced by treatment with abscisic acid (ABA). The sensor may be a metabolite that changes in concentration or a membrane protein that changes in configuration, as the cell shrinks in response to a salt, drought or cold stress, or a long-distance signal moving from roots to shoots in the transpiration stream. Transcriptomic level Tolerant plants reveal altered regulation of gene expression of important stress-responsive genes than susceptible plants (qualitative and quantitative differences at gene expression level). It reveals the altered regulation of stress responsive genes. A transcriptomic study done by Kumari et al. (2009) on a salt-sensitive rice line IR64 and a salt-tolerant rice Pokkali has led to the identification of a set of salinity- responsive genes including GST, LEA, V-ATPase, OSAP1 zinc finger protein, and transcription factor HB1B displaying a higher expression in Pokkali than in IR64 and possibly contributing to a higher salinity tolerance of Pokkali. The transcriptomic section has been divided in the following subheadings: Transcription factors A transcription factor (sometimes called a sequence-specific DNA-binding factor) is a protein that binds to specific DNA sequences, thereby, controlling the flow (or transcription) of genetic information from DNA to messenger RNA and is Environ Sci Pollut Res (2015) 22:4056–4075 whose overexpression imparts salt stress tolerance in different plant species studies with whole plants that resulted into increased salt tolerance Gene(s) Species Concentration Reference P5CS mod, codA, Tobacco, rice 5–60 mM Sakamoto and Alia (1998), P5CS Hong et al. (2000), Ohnishi and Murata (2006), Nounjana et al. (2012) otsA, otsB, AtTPS1, Rice 300 μM Garg et al. (2002), AtTPS2 Baea et al.(2005) sorbitol mt1D, S6PDH, Wheat, tobacco, 2–60 mM Tarczynski et al. (1993), OemaT1 persimmon Gao et al. (2001) Abebe et al. (2003), Conde et al. (2007) imt1 Tobacco 35 mM Sheveleva et al. (1997) choline oxidase, otsA trehalose-6- phosphate synthase, otsB trehalose-6-phosphate phosphatase, dehydrogenase, imt1 D-myo-inositol methyltransferase, OeMaT1 mannitol-1, MAP kinases ion Mitogen-activated protein kinase (MAPK) cascades are con- served eukaryotic signaling modules which play key regula- tory roles in development as well as in numerous stress responses. Acting early after stress perception, they serve for both amplification and transduction of the stress information. A well-studied stress-related MAPK cascade is the HOG1 pathway, which regulates the high-osmolarity response in yeast (Zi et al. 2010). Similarly, stress-related MAPK cascades have been discovered in animals (Ballif and Blenis 2001; Kyriakis and Avruch 2012) and plants (Rodriguez et al. 2010). MPK cascades consist of three sequential components, MPK kinase kinase, MPKkinase (MKK), and MPK. Various combinations of MPK cascades mediate plant tolerance to NaCl and play roles in cell wall biosynthesis and cell growth and differentiation (Colcombet and Hirt 2008). Irrespective of the organism, signaling involves a phosphor-relay mecha- nism: a MAPKKK activates its downstream MAPKK which in turn activates a target MAPK. Finally, MAPKs regulate the properties of substrate proteins through phosphorylation at serine or threonine residues adjacent to a proline (S/T-P). A kinase interaction motif (R/K-x(2–6)-I/LxI/L) found in a num- ber of plant MAPK targets has been shown to assist substrate binding (Schweighofer et al. 2007). Among the 10 MAPKKs and 20 MAPKs in Arabidopsis, MKK4/MKK5 and their direct substrates, MPK3/MPK6 in particular, are strongly associated with stress signaling. They are activated by various biotic and abiotic stimuli (Colcombet and Hirt 2008; Pitzschke et al. 2009; Rodriguez et al. 2010; Samajova et al. 2013). Both MKK4/MKK5 and MPK3/MPK6 are pairs of closely related proteins, which have highly, but not entirely, 4065 2011a). The MiR159 and 319 were upregulated following saline treatment in artichoke tissues (De Paola et al. 2012). regulating Proteomic level Proteins involved in stress response reveal an altered activity in tolerant plants than in susceptible ones (differences in protein structure and activity level). Several studies on the molecular mechanisms regulating salt stress response in plants have focused on changes in transcription (Brumós et al. 2009). However, phenotypic performance also depends on protein expression, as well as on their post-translational modifications that cannot be identified by simply analyzing transcription. Therefore, proteomic analysis may provide a powerful molec- ular tool to complement genomic and transcriptomic analysis. A mere protein differential abundance does not give much information on protein function under salinity and therefore validation of comparative proteomics should be done by pro- tein functional analysis. Therefore, other approaches (e.g., post-translational modifications, protein-protein interactions, tissue and subcellular localization, and phenotype influence on silencing or overexpressing of a gene encoding a protein of interest) have to be employed to unravel the role of the proteins in acquisition and development of salinity tolerance in plants. Several functional groups of proteins affected by salt stress including proteins involved in signaling, ion transport, energy metabolism (photosynthesis, ATP production, respira- tion), carbohydrate, protein and lipid metabolism, metabolism of osmolytes and phytohormones, stress-related proteins (ox- idative stress-ROS scavenging enzymes, pathogenesis related proteins, osmotic stress-related proteins-osmotin), cytoskele- ton and cytoskeleton-associated proteins, enzymes involved in secondary metabolism (biosynthesis of lignin, degradation of cyanate), and others (Kosová et al. 2013). Below, the main protein functional groups affected by salt stress are discussed in detail. With the help of 2DE experiments, some Ca binding pro- teins activated by salinity stress have been detected including plasma membrane protein annexin (Pang et al. 2010) and calmodulin (Cheng et al. 2009). These proteins were observed to mediate osmotic stress and ABA signal transduction (Lee et al. 2004a, b) and their levels were increased in salt-exposed shoots of Salicornia europea, one of the most tolerant salt plant species (Wang et al. 2009) and in the tobacco salt- stressed roots (Manaa et al. 2011). Other differentially abun- dant signaling proteins belonging to the Rab family of guano- sine triphosphate-binding proteins (GTPase) are also involved in stress signal transduction via regulation of endocytosis and vesicle trafficking (Wang et al. 2008a; Pang et al. 2010). A gene encoding a small GTP related to the Rab2 gene family of GTPases was induced by salt stress in Lolium temulentum (Dombrowski et al. 2008). Environ Sci Pollut Res (2015) 22:4056–4075 in Suaeda aegyptiaca (Askari et al. 2006), putative alpha1 subunit of 20S proteosome in rice panicles (Dooki et al. 2006) or 26S proteosomal subunit in foxtail millet (Veeranagamallaiah et al. 2008) and Salicornia europaea (Wang et al. 2009) indi- cates an enhanced protein degradation upon salt stress. Increased relative abundance of FtsH-like protein, an ATP-dependent metalloprotease involved in degradation of D1 core component of PSII, indicates an enhanced damage of photosystem core proteins upon salinity (Zörb et al. 2009). Salinity stress reveals profound impacts on plant energy metabolism. Due to osmotic stress, there is enhanced stomatal closure and a reduced CO2 availability; CO2 assimilation decreased in most of the plants. A reduced CO2assimilation rate is reflected by a decreased abundance of Rubisco large and small subunits, OEE proteins (components of oxygen evolving complex), carbonic anhydrase, and Rubisco activase and an enhanced degradation of Rubisco subunits observed in several glycophytic plants and crops exposed to salt (Aghaei et al. 2008; Pang et al. 2010; Sobhanian et al. 2010a; Bandehagh et al. 2011;Chattopadhyay et al. 2011). Besides activation of Rubisco, Rubisco activase also reveals a chaper- one function under stress (Kim et al. 2005; Fatehi et al. 2012). Similarly, an increased relative abundance of OEE2 protein was found in salt-treated barley (Rasoulnia et al. 2011; Fatehi et al. 2012), possibly as a compensation for stress-induced damage of PSII core. An enhanced abundance of ferredoxin NADPH reductase, 23 kDa polypeptide of PSII and the FtsH- like protein has been observed in salt-exposed maize chloro- plast fraction which may be due to adverse impacts of Na+ on photosynthetic electron transport chain (Zörb et al. 2009). Other salt-increased proteins with protective functions on photosystems include CP47 protein revealing protective ef- fects on D1 protein in RC PSII and PSI subunit IV protein (Veeranagamallaiah et al. 2008; Sengupta and Majumder 2009) and in one of the study on Porteresia enhanced accu- mulation of CP47 has been observed under salt stress (Sengupta and Majumder 2009). Enzymes associated with carbohydrate metabolism (Calvin cycle, glycolysis) have been found to increase under salt stress. As an example, fructose- 1,6-bisphosphatase (FBPase) and fructose-1,6-bisphosphatase aldolase (FBP aldolase) can be given (Kim et al. 2005). The FBPase catalyses hydrolysis of fructose-1,6-bisphosphate to fructose-6-phosphate and FBP aldolase catalyses conversion (splitting) of fructose-1,6-bisphosphate into glyceraldehyde- 3-phosphate and dihydroxyacetone phosphate. Increased rel- ative abundance of FBP aldolase together with other glyco- lytic enzymes and enzymes involved in ethanolic fermentation and glycolate metabolism in rice seedlings indicates an in- creased relative abundance of anaerobic metabolism under salt stress (Abbasi and Komatsu 2004). An increased relative abundance of alcohol dehydrogenase has been found in hy- pocotyls of salt-stressed soybean (Sobhanian et al. 2010a) and grasspea leaves (Chattopadhyay et al. 2011). Moreover, it has 4067 Kumar Swami et al. 2011). Besides activation of ROS scav- enging enzymes, other responses could be observed in salt- treated plants. An increased abundance of tocopherol cyclase, a crucial enzyme in the biosynthesis of α-tocopherol, an important compound in plant non-enzymatic ROS scavenging mechanisms, has been found in Chinese halophytic plant Puccinellia tenuiflora (Yu et al. 2011). An increased abun- dance of mitochondrial alternative oxidase (AOX), an enzyme involved in so-called “cyanide-resistant respiration,” i.e., res- piration without utilization of cytochromes leading to a re- duced ROS formation, has been observed in salt-treated wheat mitochondria (Jacoby et al. 2010). It is also known that free metal ions could act as catalysers of ROS formation. Therefore, responses leading to elimina- tion of free metal ions were observed in salt-stressed plants. In salt-exposed barley roots, a decrease in IDI2, IDS2, and IDS3 proteins has been observed (Witzel et al. 2009). The reduced relative abundance of IDI2, IDS2, and IDS3 indicates a de- crease in Fe consumption which may reflect the avoidance of metal ion-induced oxidative stress. Consistent with the aim to maintain low levels of free intracellular Fe, an increased abundance of ferritin, an Fe-binding protein, was found in salt-treated rice (Kim et al. 2005), Arabidopsis cell culture (Ndimba et al. 2005) and tomato (Chen et al. 2009) seedlings, and accumulation of triplicated transferrin-like protein was detected in Dunaliella salina (Liska et al. 2004). An elevated abundance of magnesium chelatase, an enzyme involved in incorporating magnesium into chlorophyll structure which catalyses the first unique step of the chlorophyll biosynthetic pathway, has been found in salt-treated barley (Rasoulnia et al. 2011). Salt stress also causes an augmentation of several proteins with protective functions such as chaperones from HSP90 family in tomato roots (Manaa et al. 2011) and HSP 70 family, Hsc70 (heat-shock cognate) proteins in A. thaliana (Pang et al. 2010) and P. patens (Wang et al. 2008a), DnaK protein, and others in salt-treated rice seedlings (Kim et al. 2005; Chitteti and Peng 2007) or Arabidopsis cell culture (Ndimba et al. 2005). Increased relative abundance of several small HSPs (mitochondrial small HSP, chloroplast HSP, 17.8 kDa class I small HSP, HSP20) was found in salt- treated tomato hypocotyls (Chen et al. 2009) and Aster tripolium leaves (Geissler et al. 2010). Increased relative abundance of STI1 protein, a stress-responsive protein with two heat shock chaperonin-binding motifs and three tetratri- copeptide repeats (TPR) in salt-treated rice panicles (Dooki et al. 2006) points toward a large regulatory network affected by salt stress since TPR-containing proteins have been report- ed as being involved in myriads of processes including HSP90 signaling, gibberellin signaling and protein mitochondrial transport. Other stress-responsive proteins include germin-like pro- teins (GLPs) which play an important role in plant embryo- genesis. Some GLPs display oxalate oxidase and SOD Environ Sci Pollut Res (2015) 22:4056–4075 profiling and proteomics (Wu et al. 2013). Major approaches currently being used in plant metabolomics are metabolic fingerprinting, metabolite profiling, and targeted analysis. In recent years, metabolomics analysis is being widely used to investigate abiotic stresses including salinity stress tolerance of plants (Alvarez et al. 2008; Shulaev et al. 2008; Renberg et al. 2010). Herein, we described the role of metabolomics in salt stress tolerance in plants under following subheadings: Osmolyte metabolism ive A decreased osmotic potential of water containing high con- centrations of dissolved salt ions poses an enhanced osmotic stress on plant cells. Thus, to overcome the stress, plant cells achieve osmotic adjustment by accumulation of inorganic salt ions that includes hydrophilic compounds, called osmolytes, and hydrophilic proteins with osmoprotective function. In salt-treated plants, changes in metabolism of several osmolytes, namely proline and glycine betaine (GB), have been found. An increased level of enzymes involved in proline biosynthesis, and in contrast, a decreased level of enzyme catalyzing proline hydrolysis have been found in Thellungiella under salt stress (Pang et al. 2010). An increased relative abun- dance of enzymes involved in GB biosynthesis such as S- adenosylmethioninesynthetase (SAMS), choline monooxygenase, and betaine aldehyde dehydrogenase has been found in salt-treated Suaeda aegyptiaca (Askari et al. 2006) and foxtail millet (Veeranagamallaiah et al. 2008). Hydrophilic proteins with 4069 in biosynthesis of galactosylglycerolipids (monogalactosyl diac- ylglycerol, digalactosyl diacylglycerol), the major components of chloroplast inner envelope and thylakoid system, observed in salt-treated maize chloroplasts (Zörb et al. 2009), and an in- creased relative abundance of UDP-sulfoquinovose synthase involved in biosynthesis of thylakoid membrane sulfolipids observed in creeping bent grass (Xu et al. 2010) indicate pro- found changes in chloroplast membrane structure and composi- tion in response to salt and osmotic stress. Changes in lipid- metabolism associated lipid transfer proteins and temperature- induced lipocalins have been observed in apoplastic fluid of tobacco cells (Dani et al. 2005) and tomato radicals (Chen et al. 2009), respectively, subjected to salinity stress. Lipid transfer proteins are known to be involved in plant response to patho- gens (Garcia-Olmedo et al. 1995) and lipocalins are known to display a protective role against photooxidative damage (Bugos et al. 1998). Conclusion and future perspectives with and with Crop productivity is severely affected by salinity stress. This occurs directly due to the impact of salinity on photosynthesis, respiration, nutrient assimilation, hormonal imbalance, etc. The indirect adverse effect of salinity is enhanced generation of receptor reactive oxygen species in stressed plant which subsequently cause damage to macromolecules such as lipids, proteins, and (increase in nucleic acids, and thus, constrain crop productivity. Therefore, an to engineer more salt-tolerant plants, it is important to find out under salt the key components of the plant salt-tolerance network. Recently, geneomics, transcriptomics, proteomics, and meta- bolomics have been successfully applied and given exciting outcome to unravel different components of salt tolerance in plants. These components include various genes (SOS signal- plants can ing-network), transcription factors (HLH, MYB, etc.), and namely its proteins and metabolites (osmolytes, phytohormones, lipids, etc.) which may be used to engineer plants for their increased salt tolerance. 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