Physiological and Molecular Insights into Mechanisms for Salt Tolerance in Plants

  • P. C. Sharma
  • G. Rama Prashat
  • Ashwani Kumar
  • Anita Mann


Salinity is one of the most serious factors limiting the productivity of agricultural crops, with adverse effects on germination, plant vigor, and crop yield. During the onset and development of salt stress within a plant, all the major processes such as photosynthesis, protein synthesis, energy and lipid metabolism are affected, thereby increasing or decreasing the levels of different metabolites or solutes involved in various processes. Ion homeostasis and appropriate compartmentalization are the key factors in salt tolerance mechanisms in different plants. Under high salinity, an increased intracellular Na+ level also induces Ca2+ signaling leading to an activation of Na+ active efflux from plant cells via SOS1/SOS2/SOS3 pathway. A rapid and appropriate response to stress is key to survival, and the major part of plant adaptation to abiotic stresses is regulated at the level of gene expression. A thorough understanding of plant response to abiotic stress at the molecular level is a prerequisite for its effective management, and the regulatory steps involved in accurate expression of stress-related genes need to be tailored for optimal plant performance. The universality of stress responses is probably the most salient feature in plants. The network of interactions between different inputs and signaling channels that is formed in a plant-specific way drives metabolic adjustments which include reactions that are common to all or nearly all plant species. The molecular mechanism of stress tolerance is complex and requires information at the omics level to understand it effectively. The advancement of “omics” is providing a detailed fingerprint of proteins, transcripts, or all metabolites upregulated or downregulated in plant cells during adverse environmental conditions. Although most studies have focused on either of regulatory mechanism, stress tolerance is more likely the combined actions of several mechanisms that provide a stress-specific output. This data may generate information for the dissection of the plant response to salinity including the generation of various metabolites and solutes and try to find future applications for ameliorating the impact of salinity on plants, improving the performance of species important to human health and agricultural sustainability.


Salt Stress Salt Tolerance Salinity Stress Salinity Tolerance Late Embryogenesis Abundant 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


  1. Abebe T, Guenzi AC, Martin B, Cushman JC (2003) Tolerance of mannitol-accumulating transgenic wheat to water stress and salinity. Plant Physiol 131(4):1748–1755PubMedPubMedCentralCrossRefGoogle Scholar
  2. Abogadallah GM (2010) Antioxidative defense under salt stress. Plant Signal Behav 5(4):369–374PubMedPubMedCentralCrossRefGoogle Scholar
  3. Agarwal S, Shaheen R (2007) Stimulation of antioxidant system and lipid peroxidation by abiotic stresses in leaves of Momordica charantia. Braz J Plant Physiol 19(2):149–161CrossRefGoogle Scholar
  4. Aghaei K, Ehsanpour AA, Komatsu S (2008) Proteome analysis of potato under salt stress. J Proteome Res 7:4858–4868PubMedCrossRefGoogle Scholar
  5. Agrawal GK, Rakwal R, Yonekura M, Kubo A, Saji H (2002) Proteome analysis of differentially displayed proteins as a tool for investigating ozone stress in rice (Oryza sativa L.) seedlings. Proteomics 2:947–959PubMedCrossRefGoogle Scholar
  6. 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 7:49–57CrossRefGoogle Scholar
  7. Akpinar BA, Lucas SJ, Budak H (2013) Genomics approaches for crop improvement against abiotic stress. Sci World J. Hindawi Publishing Corporation, Article ID 361921Google Scholar
  8. Alamgir ANM, Yousuf Ali M (1999) Effect of salinity on leaf pigments, sugar and protein concentrations and chloroplast ATPase activity of rice (Oryza sativa L.). Bangladesh J Bot 28(2):145–149Google Scholar
  9. Alcazar R, Cuevas JC, Patrón M, Altabella T, Tiburcio AF (2006a) Abscisic acid modulates polyamine metabolism under water stress in Arabidopsis thaliana. Plant Physiol 128:448–455CrossRefGoogle Scholar
  10. Alcazar R, Marco F, Cuevas JC (2006b) Involvement of polyamines in plant response to abiotic stress. Biotechnol Lett 28(23):1867–1876PubMedCrossRefGoogle Scholar
  11. Alcazar R, Altabella T, Marco F, Bortolotti C, Reymond M, Koncz C, Carrasco P, Tiburcio AF (2010) Polyamines: molecules with regulatory functions in plant abiotic stress tolerance. Planta 231:1237–1249PubMedCrossRefGoogle Scholar
  12. Alvarez S, Goodger JQ, Marsh EL, Chen S, Asirvatham VS, Schachtman DP (2006) Characterization of the maize xylem sap proteome. J Proteome Res 5:963–972PubMedCrossRefGoogle Scholar
  13. Alvarez S, Marsh EL, Schroeder SG, Schachtman DP (2008) Metabolomic and proteomic changes in the xylem sap of maize under drought. Plant Cell Environ 31:325–340PubMedCrossRefGoogle Scholar
  14. Aly-Salama KH, Al-Mutawa MM (2009) Glutathione-triggered mitigation in salt-induced alterations in plasmalemma of onion epidermal cells. Int J Agric Biol 11(5):639–642Google Scholar
  15. Apse MP, Aharon GS, Snedden WA, Blumwald E (1999) Salt tolerance conferred by overexpression of a vacuolar Na+/H+ Antiport in Arabidopsis. Science 285(5431):1256–1258PubMedCrossRefGoogle Scholar
  16. Arbona V, Iglesias DJ, Talón M, Gómez-Cadenas A (2009) Plant phenotype demarcation using nontargeted LC–MS and GC–MS metabolite profiling. J Agric Food Chem 57:7338–7347PubMedCrossRefGoogle Scholar
  17. Arbona V, Argamasilla R, Gómez-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 167:1342–1350PubMedCrossRefGoogle Scholar
  18. Asada K (1999) The water-water cycle in chloroplasts: scavenging of active oxygens and dissipation of excess photons. Annu Rev Plant Physiol Plant Mol Biol 50:601–639PubMedCrossRefGoogle Scholar
  19. Ashraf M (2009) Biotechnological approach of improving plant salt tolerance using antioxidants as markers. Biotechnol Adv 27:84–93PubMedCrossRefGoogle Scholar
  20. Ashraf M, Akram NA (2009) Improving salinity tolerance of plants through conventional breeding and genetic engineering: an analytical comparison. Biotechnol Adv 27:744–752PubMedCrossRefGoogle Scholar
  21. Ashraf M, Foolad MR (2007) Roles of glycine betaine and proline in improving plant abiotic stress resistance. Environ Exp Bot 59(2):206–216CrossRefGoogle Scholar
  22. Ashraf M, Harris PJC (2004) Potential biochemical indicators of salinity tolerance in plants. Plant Sci 166:3–16CrossRefGoogle Scholar
  23. Barragán V, Leidia EO, Andrésa Z, Rubiob L, Lucaa AD, Fernándezb JA, Cuberoa B, Pardo JM (2012) Ion exchangers NHX1 and NHX2 mediate active potassium uptake into vacuoles to regulate cell turgor and stomatal function in Arabidopsis. Plant Cell 24(3):1127–1142PubMedPubMedCentralCrossRefGoogle Scholar
  24. Bartels D, Sunkar R (2005) Drought and salt tolerance in plants. Crit Rev Plant Sci 24:23–58CrossRefGoogle Scholar
  25. Baxter I (2009) Ionomics: studying the social network of mineral nutrients. Curr Opin Plant Biol 12:381–386PubMedPubMedCentralCrossRefGoogle Scholar
  26. Binzel ML, Hess FD, Bressan RA, Hasegawa PM (1988) Intracellular compartmentation of ions in salt adapted tobacco cells. Plant Physiol 86:607–614PubMedPubMedCentralCrossRefGoogle Scholar
  27. Bouché N, Lacombe B, Fromm H (2003) GABA signaling: a conserved and ubiquitous mechanism. Trends Cell Biol 13(12):607–610PubMedCrossRefGoogle Scholar
  28. Brady SM, Orlando DA, Lee JY, Wang JY, Koch J, Dinneny JR, Mace D, Ohler U, Benfey PN (2007) A high-resolution root spatiotemporal map reveals dominant expression patterns. Science 318(5851):801–806PubMedCrossRefGoogle Scholar
  29. Bray EA, Bailey-Serres J, Weretilnyk E (2000) Responses to abiotic stresses. In: Gruissem W, Buchannan B, Jones R (eds) Biochemistry and molecular biology of plants. American Society of Plant Physiologists, Rockville, pp 1158–1249Google Scholar
  30. Brini F, Hanin M, Lumbreras V, Amara I, Khoudi H, Hassairi A, Pagès M, Masmoudi K (2007) Overexpression of wheat dehydrin DHN-5 enhances tolerance to salt and osmotic stress in Arabidopsis thaliana. Plant Cell Rep 26:2017–2026PubMedCrossRefGoogle Scholar
  31. Buhtz A, Kolasa A, Arlt K, Walz C, Kehr J (2004) Xylem sap protein composition is conserved among different plant species. Planta 219:610–618PubMedCrossRefGoogle Scholar
  32. Carillo P, Mastrolonardo G, Nacca F, Parisi D, Verlotta A, Fuggi A (2008) Nitrogen metabolism in durum wheat under salinity: accumulation of proline and glycine betaine. Funct Plant Biol 35(5):412–426CrossRefGoogle Scholar
  33. Carillo P, Annunziata MG, Pontecorvo G, Fuggi A, Woofrow P (2011) Salinity stress and salt tolerance. In: Shanker A, Venkateswarlu B (eds) Agricultural and biological sciences abiotic stress in plants -mechanisms and adaptation. ISBN:978-953-307-394-1 InTech doi: 10.5772/22331
  34. Chen TH, Murata N (2008) Glycinebetaine: an effective protectant against abiotic stress in plants. Trends Plant Sci 13(9):499–505PubMedCrossRefGoogle Scholar
  35. Chen L, Ren F, Zhong H, Jiang W, Li X (2010) Identification and expression analysis of genes in response to high-salinity and drought stresses in Brassica napus. Acta Biochim Biophys Sin 42(2):154–164PubMedCrossRefGoogle Scholar
  36. Chitteti BR, Peng Z (2007) Proteome and phosphoproteome differential expression under salinity stress in rice (Oryza sativa) roots. J Proteome Res 6:1718–1727PubMedCrossRefGoogle Scholar
  37. Cramer GR, Urano K, Delrot S, Pezzotti M, Shinozaki K (2011) Effects of abiotic stress on plants: a systems biology perspective. BMC Plant Biol 11:163. doi: 10.1186/1471-2229-11-163 PubMedPubMedCentralCrossRefGoogle Scholar
  38. Crawford NM (2006) Mechanisms for nitric oxide synthesis in plants. J Exp Bot 57(3):471–478PubMedCrossRefGoogle Scholar
  39. Cushman JC, Bohnert HJ (2000) Genomic approaches to plant stress tolerance. Curr Opin Plant Biol 3:117–124PubMedCrossRefGoogle Scholar
  40. Delauney AJ, Verma DPS (1993) Proline biosynthesis and osmoregulation in plants. Plant J 4:215–223CrossRefGoogle Scholar
  41. Diatloff E, Kumar R, Schachtman DP (1998) Site directed mutagenesis reduces the Na+ affinity of HKT1, a Na+ energized high affinity K+ transporter. FEBS Lett 432:31–36PubMedCrossRefGoogle Scholar
  42. Dietz KJ, Tavakoli N, Kluge C, Mimura T, Sharma SS, Harris GC, Chardonnens AN, Golldack D (2001) Significance of the V-type ATPase for the adaptation to stressful growth conditions and its regulation on the molecular and biochemical level. J Exp Bot 52(363):1969–1980PubMedCrossRefGoogle Scholar
  43. Dinneny JR, Long TA, Wang JY, Jung JW, Mace D, Pointer S, Barron C, Brady SM, Schiefelbein J, Benfey PN (2008) Cell identity mediates the response of Arabidopsis roots to abiotic stress. Science 320(5878):942–945PubMedCrossRefGoogle Scholar
  44. Dionisiosese ML, Tobita S (1998) Antioxidant response of rice seedlings to salinity stress. Plant Sci 135:1–9CrossRefGoogle Scholar
  45. Djordjevic MA, Oakes M, Li DX, Hwang CH, Hocart CH, Gresshoff PM (2007) The Glycine max xylem sap and apoplast proteome. J Proteome Res 6:3771–3779PubMedCrossRefGoogle Scholar
  46. El-Shintinawy F, El-Shourbagy MN (2001) Alleviation of changes in protein metabolism in NaCl-stressed wheat seedlings by thiamine. Biol Plant 44(4):541–545CrossRefGoogle Scholar
  47. Endler A, Kesten C, Schneider R, Zhang Y, Ivakov A, Frohlich A, Funke N, Persson S (2015) A mechanism for sustained cellulose synthesis during salt stress: proteins that help plants grow under salt stress identified. Cell 162:1353–1364. doi: 10.1016/j.cell.2015.08.028 PubMedCrossRefGoogle Scholar
  48. FAO (2009) High level expert forum—how to feed the world in 2050. Economic and Social Development, Food and Agricultural Organization of the United Nations, RomeGoogle Scholar
  49. Fiehn O (2002) Metabolomics-the link between genotypes and phenotypes. Plant Mol Biol 48:155–171PubMedCrossRefGoogle Scholar
  50. Flowers TJ (2004) Improving crop salt tolerance. J Exp Bot 55(396):307–319PubMedCrossRefGoogle Scholar
  51. Fougere F, Rudulier DL, Streeter JG (1991) Effects of salt stress on amino acid, organic acid and carbohydrate composition of roots, bacteroides, and cytosol of alfalfa (Medicago sativa L.). Plant Physiol 96:1228–1236PubMedPubMedCentralCrossRefGoogle Scholar
  52. Fukuda A, Nakamura A, Tagiri A, Tanaka H, Miyao A, Hirochika H, Tanaka Y (2004) Function, intracellular localization and the importance in salt tolerance of a vacuolar Na+/H+ antiporter from rice. Plant Cell Physiol 45(2):146–159PubMedCrossRefGoogle Scholar
  53. G’alvez FJ, Baghour M, Hao G, Cagnac O, Rodr’ıguez-Rosales MP, Venema K (2012) Expression of LeNHX isoforms in response to salt stress in salt sensitive and salt tolerant tomato species. Plant Physiol Biochem 51:109–115CrossRefGoogle Scholar
  54. Gao Z, Sagi M, Lips SH (1998) Carbohydrate metabolism in leaves and assimilate partitioning in fruits of tomato (Lycopersicon esculentum L.) as affected by salinity. Plant Sci 135(2):149–159CrossRefGoogle Scholar
  55. Garg B, Puranik S, Misra S, Tripathi BN, Prasad M (2013) Transcript profiling identifies novel transcripts with unknown functions as primary response components to osmotic stress in wheat (Triticum aestivum L.). Plant Cell Tiss Org Cult 113(1):91–101CrossRefGoogle Scholar
  56. Garratt LC, Janagoudar BS, Lowe KC, Anthony P, Power JB, Davey MR (2002) Salinity tolerance and antioxidant status in cotton cultures. Free Radic Biol Med 33:502–511PubMedCrossRefGoogle Scholar
  57. Gavaghan CL, Li JV, Hadfield ST, Hole S, Nicholson JK, Wilson ID, Howe PW, Stanley PD, Holmes E (2011) Application of NMR-based metabolomics to the investigation of salt stress in maize (Zea mays). Phytochem Anal 22:214–224PubMedCrossRefGoogle Scholar
  58. Gekko K, Timasheff SN (1981) Thermodynamic and kinetic examination of protein stabilization by glycerol. Biochemistry 20:4677–4686PubMedCrossRefGoogle Scholar
  59. Golldack D, Dietz KJ (2001) Salt-induced expression of the vacuolar H+ ATPase in the common ice plant is developmentally controlled and tissue specific. Plant Physiol 125:1643–1654PubMedPubMedCentralCrossRefGoogle Scholar
  60. Gossett DR, Millhollon EP, Lucas MC (1994) Antioxidant response to NaCl stress in salt-tolerant and salt-sensitive cultivars of cotton. Crop Sci 34:706–714CrossRefGoogle Scholar
  61. Groppa MD, Benavides MP (2008) Polyamines and abiotic stress: recent advances. Amino Acids 34(1):35–45PubMedCrossRefGoogle Scholar
  62. Gruber V, Blanchet S, Diet A, Zahaf O, Boualem A, Kakar K, Alunni B, Udvardi M, Frugier F, Crespi M (2009) Identification of transcription factors involved in root apex responses to salt stress in Medicago truncatula. Mol Genet Genomics 281:55–66PubMedCrossRefGoogle Scholar
  63. Gueta-Dahan Y, Yaniv Z, Zilinskas BA, Ben-Hayyim G (1997) Salt and oxidative stress: similar and specific responses and their relation to salt tolerance in citrus. Planta 203(460):469Google Scholar
  64. Gupta A, Huang B (2014) Mechanism of salinity tolerance in plants: physiological, biochemical, and molecular characterization. Int J Genomics. doi: 10.1155/2014/701596 PubMedPubMedCentralGoogle Scholar
  65. Gupta K, Dey A, Gupta B (2013) Plant polyamines in abiotic stress responses. Acta Physiol Plant 35(7):2015–2036CrossRefGoogle Scholar
  66. Hasanuzzaman M, Nahar K, Fujita M (2014) Regulatory roles of polyamines in growth, development and abiotic stress tolerance in plants. In: Anjum NA, Gill SS, Gill R (eds) Plant adaptation to environmental change: significance of amino acids and their derivatives. CABI Publication, Wallingford, pp 157–193Google Scholar
  67. Hasegawa PM, Bressan RA, Zhu JK, Bohnert HJ (2000) Plant cellular and molecular responses to high salinity. Annu Rev Plant Biol 51:463–499CrossRefGoogle Scholar
  68. Hauser F, Horie T (2010) A conserved primary salt tolerance mechanism mediated by HKT transporters: a mechanism for sodium exclusion and maintenance of high K+/Na+ ratio in leaves during salinity stress. Plant Cell Environ 33:552–565PubMedCrossRefGoogle Scholar
  69. Hernández JA, Olmos E, Corpas FJ, Sevilla F, Del Río FA (1995) Salt-induced oxidative stress in chloroplast of pea plants. Plant Sci 105:151–167CrossRefGoogle Scholar
  70. Horie T, Hauser F, Schroeder JI (2009) HKT transporter mediated salinity resistance mechanisms in Arabidopsis and monocot crop plants. Trends Plant Sci 14:660–668PubMedPubMedCentralCrossRefGoogle Scholar
  71. Horie T, Karahara I, Katsuhara M (2012) Salinity tolerance mechanisms in glycophytes: an overview with the central focus on rice plants. Rice 5:11. doi: 10.1186/1939-8433-5-11 PubMedCrossRefGoogle Scholar
  72. James RA, Davenport RJ, Munns R (2006) Physiological characterisation of two genes for Na+ exclusion in durum wheat: Nax1 and Nax2. Plant Physiol 142:1537–1547PubMedPubMedCentralCrossRefGoogle Scholar
  73. James RA, von Caemmerer S, Condon AG, Zwart AB, Munns R (2008) Genetic variation on tolerance to the osmotic stress component of salinity stress in durum wheat. Funct Plant Biol 35(2):111–123CrossRefGoogle Scholar
  74. James RA, Blake C, Byrt CS, Munns R (2011) Major genes for Na+ exclusion, Nax1 and Nax2 (wheat HKT1;4 and HKT1;5) decrease Na+ accumulation in bread wheat leaves under saline and waterlogged conditions. J Exp Bot 62(8):2939–2947PubMedCrossRefGoogle Scholar
  75. Jamil A, Riaz S, Ashraf M, Foolad MR (2011) Gene expression profiling of plants under salt stress. Crit Rev Plant Sci 30:435–458CrossRefGoogle Scholar
  76. Jayakannan M, Bose J, Babourina O, Rengel Z, Shabala S (2013) Salicylic acid improves salinity tolerance in Arabidopsis by restoring membrane potential and preventing salt-induced K+ loss via a GORK channel. J Exp Bot 64(8):2255–2268PubMedPubMedCentralCrossRefGoogle Scholar
  77. Jiang Y, Yang B, Harris NS, Deyholos MK (2007) Comparative proteomic analysis of NaCl stress-responsive proteins in Arabidopsis roots. J Exp Bot 58(13):3591–3607PubMedCrossRefGoogle Scholar
  78. Joseph TC, Lawrance AR, Thampuran N, James R (2010) Functional characterization of trehalose biosynthesis genes from E. coli: an osmolyte involved in stress tolerance. Mol Biotechnol 46:20–25PubMedCrossRefGoogle Scholar
  79. Kang JY, Choi HI, Im MY, Kim SY (2002) Arabidopsis basic leucine zipper proteins that mediate stress-responsive abscisic acid signaling. Plant Cell 14:343–357PubMedPubMedCentralCrossRefGoogle Scholar
  80. Kang G, Li G, Xu W, Peng X, Han Q, Zhu Y, Guo T (2012) Proteomics reveals the effects of salicylic acid on growth and tolerance to subsequent drought stress in wheat. J Proteome Res 11(12):6066–6079PubMedGoogle Scholar
  81. Kav NNV, Srivastava S, Goonewardene L, Blade SF (2004) Proteome-level changes in the roots of Pisum sativum in response to salinity. Front Mol Neurosci 145(Suppl 2):217–230Google Scholar
  82. Kawaura K, Mochida K, Ogihara Y (2008) Genome-wide analysis for identification of salt-responsive genes in common wheat. Funct Integr Genom 8:277–286CrossRefGoogle Scholar
  83. Kehr J, Buhtz A, Giavalisco P (2005) Analysis of xylem sap proteins from Brassica napus. BMC Plant Biol 5:11. doi: 10.1186/1471-2229-5-11 PubMedPubMedCentralCrossRefGoogle Scholar
  84. Kerepesi I, Galiba G (2000) Osmotic and salt stress-induced alteration in soluble carbohydrate content in wheat seedlings. Crop Sci 40(2):482–487CrossRefGoogle Scholar
  85. Kim DW, Rakwal R, Agrawal GK, Jung YH, Shibato J, Jwa NS (2005) A hydroponic rice seedling culture model system for investigating proteome of salt stress in rice leaf. Electrophoresis 26:4521–4539PubMedCrossRefGoogle Scholar
  86. Kim JK, Bamba T, Harada K, Fukusaki E, Kobayashi A (2007) Time-course metabolic profiling in Arabidopsis thaliana cell cultures after salt stress treatment. J Exp Bot 58(3):415–424PubMedCrossRefGoogle Scholar
  87. Kim DY, Hong MJ, Jang JH, Seo YW (2012) cDNA-AFLP analysis reveals differential gene expression in response to salt stress in Brachypodium distachyon. Genes Genomics 34(5):475–484CrossRefGoogle Scholar
  88. Kumar R (2009) Role of naturally occurring osmolytes on the protein folding and stability. Arch Biochem Biophys 491:1–6PubMedCrossRefGoogle Scholar
  89. Kusano T, Yamaguchi K, Berberich T, Takahashi Y (2007) The polyamine spermine rescues Arabidopsis from salinity and drought stresses (Plant Signaling and Behavior). Plant Signal Behav 2(4):251–252PubMedPubMedCentralCrossRefGoogle Scholar
  90. Lamattina L, Garcıa-Mata C, Graziano M, Pagnussat G (2003) Nitric oxide: the versatility of an extensive signal molecule. Annu Rev Plant Biol 54:109–136PubMedCrossRefGoogle Scholar
  91. LaRosa PC, Chen Z, Nelson DE, Singh NK, Hasegawa PM, Bressan RA (1992) Osmotin gene expression is post transcriptionally regulated. Plant Physiol 100:409–415PubMedPubMedCentralCrossRefGoogle Scholar
  92. Läuchli A, Epstein E (1990) Plant responses to saline and sodic conditions. In: Tanji KK (ed) Agricultural salinity assessment and management. American Society of Civil Engineers, New York, pp 113–137Google Scholar
  93. Laurie S, Feeney KA, Maathuis FJM, Heard PJ, Brown SJ, Leigh RA (2002) A role for HKT1 in sodium uptake by wheat roots. Plant J 32:139–149PubMedCrossRefGoogle Scholar
  94. Li B, He L, Guo S, Li J, Yang Y, Yan B, Sun J, Li J (2013) Proteomics reveal cucumber Spd-responses under normal condition and salt stress. Plant Physiol Biochem 67:7–14PubMedCrossRefGoogle Scholar
  95. Long TA (2011) Many needles in a haystack: cell-type specific abiotic stress responses. Curr Opin Plant Biol 14:325–331PubMedCrossRefGoogle Scholar
  96. Louis P, Galinski EA (1997) Characterization of genes for the biosynthesis of the compatible solute ectoine from Marinococcus halophilus and osmoregulated expression in E. coli. Microbiology 143:1141–1149PubMedCrossRefGoogle Scholar
  97. Lu Y, Lam H, Pi E, Zhan Q, Tsai S, Wang C, Kwan Y, Ngai S (2013) Comparative metabolomics in Glycine max and Glycine soja under salt stress to reveal the phenotypes of their offspring. J Agric Food Chem 61:8711–8721PubMedCrossRefGoogle Scholar
  98. Mahajan S, Pandey GK, Tuteja N (2008) Calcium- and salt-stress signaling in plants: shedding light on SOS pathway. Arch Biochem Biophys 471:146–158PubMedCrossRefGoogle Scholar
  99. Makihara F, Tsuzuki M, Sato K, Masuda S, Nagashima KV, Abo M, Okubo A (2005) Role of trehalose synthesis pathways in salt tolerance mechanism of Rhodobacter sphaeroides f. sp. denitrificans IL106. Arch Microbiol 184(1):56–65PubMedCrossRefGoogle Scholar
  100. Malakshah SN, Rezaei MH, Heidari M, Salekdeh GH (2007) Proteomics reveals new salt responsive proteins associated with rice plasma membrane. Biosci Biotechnol Biochem 71:2144–2154CrossRefGoogle Scholar
  101. Martin-Tanguy J (2001) Metabolism and function of polyamines in plants: recent development (new approaches). Plant Growth Regul 34(1):135–148CrossRefGoogle Scholar
  102. Mian A, Oomen R, Isayenkov S, Sentenac H, Maathuis FJM, Very AA (2011) Over-expression of an Na(+)- and K(+)-permeable HKT transporter in barley improves salt tolerance. Plant J 68:468–479PubMedCrossRefGoogle Scholar
  103. Miller G, Suzuki N, Rizhsky L, Hegie A, Koussevitzky S, Mittler R (2007) Double mutants deficient in cytosolic and thylakoid ascorbate peroxidase reveal a complex mode of interaction between reactive oxygen species, plant development and a response to abiotic stress. Plant Physiol 144:1777–1785PubMedPubMedCentralCrossRefGoogle Scholar
  104. Mostofa MG, Hossain MA, Fujita M (2015) Trehalose pre-treatment induces salt tolerance in rice (Oryza sativa L.) seedlings: oxidative damage and co-induction of antioxidant defence and glyoxalase systems. Protoplasma 252:461–475PubMedCrossRefGoogle Scholar
  105. Mott IW, Wang RRC (2007) Comparative transcriptome analysis of salt-tolerant wheat germplasm lines using wheat genome arrays. Plant Sci 173:327–339CrossRefGoogle Scholar
  106. Munir N, Aftab F (2011) Enhancement of salt tolerance in sugarcane by ascorbic acid pretreatment. Afr J Biotechnol 10(80):18362–18370Google Scholar
  107. Munns R, Tester M (2008) Mechanisms of salinity tolerance. Annu Rev Plant Biol 59:651–681PubMedCrossRefGoogle Scholar
  108. Munns R, Schachtman D, Condon A (1995) The significance of a two-phase growth response to salinity in wheat and barley. Funct Plant Biol 22(4):561–569Google Scholar
  109. Munns R, Rebetzke GJ, Husain S, James RA, Hare RA (2003) Genetic control of sodium exclusion in durum wheat. Aust J Agr Res 54(7):627–635CrossRefGoogle Scholar
  110. Muscolo AA, Junker C, Klukas K, Weigelt-Fischer DR, Altmann T (2015) Phenotypic and metabolic responses to drought and salinity of four contrasting lentil accessions. J Exp Bot. doi: 10.1093/jxb/erv208 PubMedPubMedCentralGoogle Scholar
  111. Nazar R, Iqbal N, Syeed S, Khan NA (2011) Salicylic acid alleviates decreases in photosynthesis under salt stress by enhancing nitrogen and sulfur assimilation and antioxidant metabolism differentially in two mungbean cultivars. J Plant Physiol 168(8):807–815PubMedCrossRefGoogle Scholar
  112. Otoch MDL, Menezes Sobreira AC, Farias De Aragão ME, Orellano EG, Da Guia Silva Lima M, Fernandes De Melo D (2001) Salt modulation of vacuolar H+-ATPase and H+-Pyrophosphatase activities in Vigna unguiculata. J Plant Physiol 158(5):545–551CrossRefGoogle Scholar
  113. Pasapula V, Shen G, Kuppu S, Paez-Valencia J, Mendoza M, Hou P, Chen J, Qiu X, Zhu L, Zhang X, Auld D, Blumwald E, Zhang H, Gaxiola R, Payton P (2011) Expression of an Arabidopsis vacuolar H+-pyrophosphatase gene (AVP1) in cotton improves drought- and salt tolerance and increases fibre yield in the field conditions. Plant Biotechnol J 9(1):88–99PubMedCrossRefGoogle Scholar
  114. Pattanagul W, Thitisaksakul M (2008) Effect of salinity stress on growth and carbohydrate metabolism in three rice (Oryza sativa L.) cultivars differing in salinity tolerance. Indian J Exp Biol 46:736–742PubMedGoogle Scholar
  115. Peng Z, Wang M, Li F, Lv H, Li C, Xia G (2009) A proteomic study of the response to salinity and drought stress in an introgression strain of bread wheat. Mol Cell Proteomics 8(12):2676–2686PubMedPubMedCentralCrossRefGoogle Scholar
  116. Plett DC, Moller IS (2010) Na+ transport in glycophytic plants: what we know and would like to know. Plant Cell Environ 33:612–626CrossRefGoogle Scholar
  117. Pu L, Brady S (2010) Systems biology update: cell type-specific transcriptional regulatory networks. Plant Physiol 152:411–419PubMedPubMedCentralCrossRefGoogle Scholar
  118. Qureshi MI, Israr M, Abdin MZ, Iqbal M (2005) Responses of Artemisia annua L. to lead and salt-induced oxidative stress. Environ Exp Bot 53:185–193CrossRefGoogle Scholar
  119. Rajendran K, Tester M, Roy SJ (2009) Quantifying the three main components of salinity tolerance in cereals. Plant Cell Environ 32:237–249PubMedCrossRefGoogle Scholar
  120. Rawia Eid A, Taha LS, Ibrahiem SMM (2011) Alleviation of adverse effects of salinity on growth, and chemical constituents of marigold plants by using glutathione and ascorbate. J Appl Sci Res 7:714–721Google Scholar
  121. Rep M, Dekker HL, Vossen JH, De Boer AD, Houterman PM, De Koster CG, Cornelissen BJ (2003) A tomato xylem sap protein represents a new family of small cysteine-rich proteins with structural similarity to lipid transfer proteins. Eur J Biochem 534:82–86Google Scholar
  122. Rodrıguez-Kessler M, Alpuche-Solís AG, Ruiz OA, Jiménez-Bremont JF (2006) Effect of salt stress on the regulation of maize (Zea mays L.) genes involved in polyamine biosynthesis. Plant Growth Regul 48:175–185CrossRefGoogle Scholar
  123. Rogers ED, Jackson T, Moussaieff A, Aharoni A, Benfey PN (2012) Cell type-specific transcriptional profiling: implications for metabolite profiling. Plant J 70:5–17PubMedPubMedCentralCrossRefGoogle Scholar
  124. Roy M, Wu R (2002) Overexpression of S-adenosylmethionine decarboxylase gene in rice increases polyamine level and enhances sodium chloride-stress tolerance. Plant Sci 163(5):987–992CrossRefGoogle Scholar
  125. Roy SJ, Negrao S, Tester M (2014) Salt resistant crop plants. Curr Opin Biotechnol 26:115–124PubMedCrossRefGoogle Scholar
  126. Sairam RK, Tyagi A (2004) Physiology and molecular biology of salinity stress tolerance in plants. Curr Sci 86(3):407–421Google Scholar
  127. Sakuma Y, Maruyama K, Osakabe Y, Qin F, Seki M, Shinozaki K, Yamaguchi-Shinozaki K (2006) Functional analysis of an Arabidopsis transcription factor DREB2A involved in drought-responsive gene expression. Plant Cell 18:1292–1309PubMedPubMedCentralCrossRefGoogle Scholar
  128. Sanchez DH, Pieckenstain FL, Escaray F, Erban A, Kraemer U, Udvardi MK, Kopka J (2011) Comparative ionomics and metabolomics in extremophile and glycophytic Lotus species under salt stress challenge the metabolic pre-adaptation hypothesis. Plant Cell Environ 34:605–617PubMedCrossRefGoogle Scholar
  129. Saneoka H, Nagasaka C, Hahn DT, Yang W-J, Premachandra GS, Joly RJ, Rhodes D (1995) Salt tolerance of glycine betaine-deficient and -containing maize lines. Plant Physiol 107:631–638PubMedPubMedCentralGoogle Scholar
  130. Saxena SC, Kaur H, Verma P (2013) Osmoprotectants: potential for crop improvement under adverse conditions. In: Tuteja N, Gill SS (eds) Plant acclimation to environmental stress. Springer, New York, pp 197–232CrossRefGoogle Scholar
  131. Schachtman DP (2000) Molecular insights into the structure and function of plant K+ transport mechanisms. Biochim Biophys Acta 1465:127–139PubMedCrossRefGoogle Scholar
  132. Schwacke R, Grallath S, Breitkreuz KE, Stransky E, Stransky H, Frommer WB, Rentsch D (1999) LeProT1, a transporter for proline, glycine betaine, and gamma-amino butyric acid in tomato pollen. Plant Cell 11(3):377–392PubMedPubMedCentralGoogle Scholar
  133. Sharma P, Jha AB, Dubey RS, Pessarakli M (2012) Reactive oxygen species, oxidative damage and antioxidative defense mechanism in plants under stressful conditions. J Bot:1–26, Article ID 217037. doi: 10.1155/2012/217037
  134. Shelden MC, Roessner U (2013) Advances in functional genomics for investigating salinity stress tolerance mechanisms in cereals. Front Plant Sci 4:123PubMedPubMedCentralCrossRefGoogle Scholar
  135. Shi H, Quintero FJ, Pardo JM, Zhu JK (2002) The putative plasma membrane Na+/H+ antiporter SOS1 controls long distance Na+ transport in plants. Plant Cell 14(2):465–477PubMedPubMedCentralCrossRefGoogle Scholar
  136. Shinozaki K, Yamaguchi-Shinozaki K (2000) Molecular responses to dehydration and low temperature: differences and cross-talk between two stress signaling pathways. Curr Opin Plant Biol 3:217–223PubMedCrossRefGoogle Scholar
  137. Silva PH, Gerós (2009) Regulation by salt of vacuolar H+-ATPase and H+-pyrophosphatase activities and Na+/H+ exchange. Plant Signal Behav 4(8):718–726PubMedPubMedCentralCrossRefGoogle Scholar
  138. Singh NK, Nelson DE, Kuhn D, Hasegawa PM, Bressan RA (1989) Molecular cloning of osmotin and regulation of its expression by ABA and adaptation to low water potential. Plant Physiol 90:1096–1101PubMedPubMedCentralCrossRefGoogle Scholar
  139. Sobhanian H, Motamed N, Rastgar Jazii F, Nakamura T, Komatsu S (2010) Salt stress induced differential proteome and metabolome response in the shoots of Aeluropus lagopoides (Poaceae), a halophyte C4 plant. J Proteome Res 9:2882–2897PubMedCrossRefGoogle Scholar
  140. Soda N, Wallace S, Karan R (2015) Omics study for abiotic stress responses in plants. Adv Plants Agric Res 2(1):1–7Google Scholar
  141. Spollen WG, Tao W, Valliyodan B, Chen K, Hejlek LG, Kim JJ, Lenoble ME, Zhu J, Bohnert HJ, Henderson D, Schachtman DP, Davis GE, Springer GK, Sharp RE, Nguyen HT (2008) Spatial distribution of transcript changes in the maize primary root elongation zone at low water potential. BMC Plant Biol 8:32. doi: 10.1186/1471-2229-8-32 PubMedPubMedCentralCrossRefGoogle Scholar
  142. Street TO, Bolen DW, Rose GD (2006) A molecular mechanism for osmolyte-induced protein stability. Proc Natl Acad Sci U S A 103:13997–14002PubMedPubMedCentralCrossRefGoogle Scholar
  143. Tarczynski MC, Jensen RG, Bohnert HJ (1993) Stress protection of transgenic tobacco by production of the osmolyte mannitol. Science 259:508–510PubMedCrossRefGoogle Scholar
  144. Thompson JE, Ledge RL, Barber RF (1987) The role of free radicals in senescence and wounding. New Phytol 105:317–344CrossRefGoogle Scholar
  145. Toshihiko A, Mikao S, Ryouhei N, Tadakatsu Y, Shuichi Y (2008) Nano scale proteomics revealed the presence of regulatory proteins including three FT-like proteins in phloem and xylem saps from rice. Plant Cell Physiol 49:767–790CrossRefGoogle Scholar
  146. Tugizimana F, Piater LA, Dubery IA (2013) Plant metabolomics: a new frontier in phytochemical analysis. S Afr J Sci 109:1–11CrossRefGoogle Scholar
  147. Tuteja N, Tuteja R (2004) Prokaryotic and eukaryotic DNA helicases. Eur J Biochem 271:1835–1848PubMedCrossRefGoogle Scholar
  148. Ueda A, Kathiresan A, Bennett J, Takabe T (2006) Comparative transcriptome analyses of barley and rice under salt stress. Theor Appl Genet 112:1286–1294PubMedCrossRefGoogle Scholar
  149. Umezawa T, Fujita M, Fujita Y, Yamaguchi-Shinozaki K, Shinozaki K (2006) Engineering drought tolerance in plants: discovering and tailoring genes unlock the future. Curr Opin Biotechnol 17:113–122PubMedCrossRefGoogle Scholar
  150. Varshney RK, Graner A, Sorrells ME (2005) Genomics assisted breeding for crop improvement. Trends Plant Sci 10(12):621–630PubMedCrossRefGoogle Scholar
  151. Vashisht AA, Pradhan A, Tuteja R, Tuteja N (2005) Cold- and salinity stress-induced bipolar pea DNA helicase 47 is involved in protein synthesis and stimulated by phosphorylation with protein kinase C. Plant J 44(1):76–87PubMedCrossRefGoogle Scholar
  152. Walia H, Wilson C, Condamine P, Ismail AM, Xu J, Cui XP, Close TJ (2007) Array-based genotyping and expression analysis of barley cv. Maythorpe and Golden Promise. BMC Genomics 8:87. doi: 10.1186/1471-2164-8-87 PubMedPubMedCentralCrossRefGoogle Scholar
  153. Wang B, L¨uttge U, Ratajczak R (2001) Effects of salt treatment and osmotic stress on V-ATPase and V-PPase in leaves of the halophyte Suaeda salsa. J Exp Bot 52(365):2355–2365PubMedCrossRefGoogle Scholar
  154. Wang MC, Peng ZY, Li CL, Li F, Liu C, Xia GM (2008) Proteomic analysis on a high salt tolerance introgression strain of Triticum aestivum/Thinopyrum ponticum. Proteomics 8:1470–1489PubMedCrossRefGoogle Scholar
  155. White PJ, Broadley MR, Thompson JA, McNicol JW, Crawley MJ, Poulton PR, Johnston AE (2012) Testing the distinctness of shoot ionomes of angiosperm families using the Rothamsted Park Grass Continuous Hay experiment. New Phytol 196(1):101–109PubMedCrossRefGoogle Scholar
  156. Widodo, Patterson JH, Newbigin E, Tester M, Bacic A, Roessner U (2009) Metabolic responses to salt stress of barley (Hordeum vulgare L.) cultivars, Sahara and Clipper, which differ in salinity tolerance. J Exp Bot 60(14):4089–4103PubMedPubMedCentralCrossRefGoogle Scholar
  157. Wise RR, Naylor AW (1987) Chilling-enhanced photooxidation: evidence for the role of singlet oxygen and endogenous antioxidants. Plant Physiol 83:278–282PubMedPubMedCentralCrossRefGoogle Scholar
  158. Wu D, Cai S, Chen M, Ye L, Chen Z, Zhang H, Dai F, Wu F, Zhang G (2013) Tissue metabolic responses to salt stress in wild and cultivated barley. PLoS One 8(1):e55431. doi: 10.1371/journal.pone.0055431 PubMedPubMedCentralCrossRefGoogle Scholar
  159. Xiong L, Gong Z, Rock CD, Subramanian S, Guo Y, Xu W, Galbraith D, Zhu JK (2001) Modulation of abscisic acid signal transduction and biosynthesis by an Sm-like protein in Arabidopsis. Dev Cell 1(6):771–781PubMedCrossRefGoogle Scholar
  160. Xu D, Duan X, Wang B, Hong B, Ho T, Wu R (1996) Expression of a late embryogenesis abundant protein gene, HVA1, from barley confers tolerance to water deficit and salt stress in transgenic rice. Plant Physiol 110(1):249–257PubMedPubMedCentralGoogle Scholar
  161. Xu K, Hong P, Luo L, Xia T (2009) Overexpression of NHX1, a Vacuolar Na+/H+ antiporter from Arabidopsis thaliana and Petunia hybrid enhances salt and drought tolerance. J Plant Biol 52(5):453–461CrossRefGoogle Scholar
  162. Xu C, Sibicky T, Huang B (2010) Protein profile analysis of salt-responsive proteins in leaves and roots in two cultivars of creeping bent grass differing in salinity tolerance. Plant Cell Rep 29:595–615PubMedCrossRefGoogle Scholar
  163. Xue S, Yao X, Luo W, Jha D, Tester M, Horie T, Schroeder JI (2011) AtHKT1;1 mediates nernstian sodium channel transport properties in Arabidopsis root stellar cells. PLoS One 6(9):e24725. doi: 10.1371/journal.pone.0024725 PubMedPubMedCentralCrossRefGoogle Scholar
  164. Yamaguchi M, Sharp RE (2010) Complexity and coordination of root growth at low water potentials: recent advances from transcriptomic and proteomic analyses. Plant Cell Environ 33:590–603PubMedCrossRefGoogle Scholar
  165. Yamaguchi-Shinozaki K, Kazuo S (2006) Transcriptional regulatory networks in cellular responses and tolerance to dehydration and cold stresses. Annu Rev Plant Biol 57:781–803PubMedCrossRefGoogle Scholar
  166. Yang Q, Chen ZZ, Zhou XF, Yin HB, Li X, Xin XF, Hong XH, Zhu JK, Gong Z (2009) Overexpression of SOS (Salt Overly Sensitive) genes increases salt tolerance in transgenic Arabidopsis. Mol Plant 2(1):22–31PubMedCrossRefGoogle Scholar
  167. Yang DH, Song LY, Hu J, Yin WB, Li ZG, Chen YH, Su XH, Wang RR, Hu ZM (2012) Enhanced tolerance to NaCl and LiCl stresses by over-expressing Caragana korshinskii sodium/proton exchanger 1 (CkNHX1) and the hydrophilic C terminus is required for the activity of CkNHX1 in Atsos3-1 mutant and yeast. Biochem Biophys Res Commun 417(2):732–737PubMedCrossRefGoogle Scholar
  168. Yin YG, Tominaga T, Iijima Y, Aoki K, Shibata D, Ashihara H, Nishimura S, Ezura H, Matsukura C (2010) Metabolic alterations in organic acids and gamma-aminobutyric acid in developing tomato (Solanum lycopersicum L.) fruits. Plant Cell Physiol 51(8):1300–1314PubMedCrossRefGoogle Scholar
  169. Zhang H, Blumwald E (2001) Transgenic salt-tolerant tomato plants accumulate salt in foliage but not in fruit. Nat Biotechnol 19(8):765–768PubMedCrossRefGoogle Scholar
  170. Zhang Y, Wang L, Liu Y, Zhang Q, Wei Q, Zhang W (2006) Nitric oxide enhances salt tolerance in maize seedlings through increasing activities of proton-pump and Na+/H+ antiport in the tonoplast. Planta 224(3):545–555PubMedCrossRefGoogle Scholar
  171. Zhang J, Zhang Y, Du Y, Chen S, Tang H (2011) Dynamic metabolomic responses of tobacco (Nicotiana tabacum) plants to salt stress. J Proteome Res 10:1904–1914PubMedCrossRefGoogle Scholar
  172. Zhang H, Han B, Wang T, Chen S, Li H, Zhang Y, Dai S (2012) Mechanisms of plant salt response: insights from proteomics. J Proteome Res 11:49–67PubMedCrossRefGoogle Scholar
  173. Zhao Q, Zhang H, Wang T, Chen S, Dai S (2013) Proteomics-based investigation of salt-responsive mechanisms in plant roots. J Proteomics 82:230–253PubMedCrossRefGoogle Scholar
  174. Zhao X, Wang W, Zhang F, Deng J, Li Z, Fu B (2014) Comparative metabolite profiling of two rice genotypes with contrasting salt stress tolerance at the seedling stage. PLoS One 9(9):e108020. doi: 10.1371/journal.pone.0108020 PubMedPubMedCentralCrossRefGoogle Scholar
  175. Zhou S, Sauvé RJ, Liu Z, Reddy S, Bhatti S, Hucko SD, Fish T, Thannhauser TW (2011) Identification of salt-induced changes in leaf and root proteomes of the wild tomato, Solanum chilense. J Am Soc Hortic Sci 136:288–302Google Scholar
  176. Zhu JK (2003) Regulation of ion homeostasis under salt stress. Curr Opin Plant Biol 6:441–445PubMedCrossRefGoogle Scholar
  177. Zhu J, Alvarez S, Marsh EL, Lenoble ME, Cho IJ, Sivaguru M, Chen S, Nguyen HT, Wu Y, Schachtman DP, Sharp RE (2007) Cell wall proteome in the maize primary root elongation zone. II. Region-specific changes in water soluble and lightly ionically bound proteins under water deficit. Plant Physiol 145:1533–1548PubMedPubMedCentralCrossRefGoogle Scholar
  178. Zörb C, Schmitt S, Neeb A, Karl S, Linder M, Schubert S (2004) The biochemical reaction of maize (Zea mays L.) to salt stress is characterized by a mitigation of symptoms and not by a specific adaptation. Plant Sci 167:91–100CrossRefGoogle Scholar

Copyright information

© Springer India 2016

Authors and Affiliations

  • P. C. Sharma
    • 1
  • G. Rama Prashat
    • 2
  • Ashwani Kumar
    • 1
  • Anita Mann
    • 1
  1. 1.ICAR-Central Soil Salinity Research InstituteKarnalIndia
  2. 2.ICAR-Indian Agricultural Research InstituteNew DelhiIndia

Personalised recommendations