Plant Growth Regulation

, Volume 76, Issue 1, pp 25–40 | Cite as

Salicylic acid in plant salinity stress signalling and tolerance

  • Maheswari Jayakannan
  • Jayakumar Bose
  • Olga Babourina
  • Zed Rengel
  • Sergey Shabala
Original paper


Soil salinity is one of the major environmental stresses affecting crop production worldwide, costing over $27Bln per year in lost opportunities to agricultural sector and making improved salinity tolerance of crops a critical step for sustainable food production. Salicylic acid (SA) is a signalling molecule known to participate in defence responses against variety of environmental stresses including salinity. However, the specific knowledge on how SA signalling propagates and promotes salt tolerance in plants remains largely unknown. This review focuses on the role of SA in regulation of ion transport processes during salt stress. In doing this, we briefly summarise a current knowledge on SA biosynthesis and metabolism, and then discuss molecular and physiological mechanisms mediating SA intracellular and long distance transport. We then discuss mechanisms of SA sensing and interaction with other plant hormones and signalling molecules such as ROS, and how this signalling affects activity of sodium and potassium transporters during salt stress. We argue that NPR1-mediated SA signalling is pivotal for (1) controlling Na+ entry into roots and the subsequent long-distance transport into shoots, (2) enhancing H+-ATPase activity in roots, (3) preventing stress-induced K+ leakage from roots via depolarisation-activated potassium outward-rectifying channel (KOR) and ROS-activated non-selective cation channels, and (4) increasing K+ concentration in shoots during salt stress. Future work should focus on how SA can regulate Na+ exclusion and sequestration mechanisms in plants.


Sodium Potassium Reactive oxygen species Intracellular ionic homeostasis Stomatal regulation H+-ATPase Membrane transporters Voltage gating 



Abscisic acid


ABA biosynthesis mutant3-1


Accelerated cell death


Aberrant growth and death2


Encoding poly (A)-specific ribonuclease




Constitutive expresser of PR (pathogenesis related protein)


Defence no death


Enhanced disease susceptibility 5


Glutamate receptor channels


Guard cells Outward-Rectifying depolarisation-activated K+ channel


High-affinity K+ transporter


Isochorismate synthase


Isochorismate pyruvate lyase


Lesions simulating disease1


Methyl salicylic acid O-β-glucose


Methyl salicylate


Naphthalene hydroxylase G


Non-expresser of pathogenesis related protein 1


Non-selective cation channels


Nudix hydrolase7


Phenylalanine ammonia-lyase


SA-binding protein 2


Salicylic acid O-β-glucoside


SA glycosyltransferase


Systemic acquired resistance


Salicylic acid


Salicyloyl glucose ester




Small ubiquitin-like modifier E3 ligase1


Suppressor of npr1-1 consitutive1


Salt overly sensitive1


Small ubiquitin-related modifier


  1. Acharya BR, Assmann SM (2009) Hormone interactions in stomatal function. Plant Mol Biol 69:451–462PubMedCrossRefGoogle Scholar
  2. Alonso-Ramirez A, Rodriguez D, Reyes D, Jimenez JA, Nicolas G, Lopez-Climent M, Gomez-Cadenas A, Nicolas C (2009) Evidence for a role of gibberellins in salicylic acid-modulated early plant responses to abiotic stress in Arabidopsis seeds. Plant Physiol 150:1335–1344PubMedCentralPubMedCrossRefGoogle Scholar
  3. Amtmann A, Sanders D (1999) Mechanisms of Na+ uptake by plant cells. Adv Bot Res 29:75–112CrossRefGoogle Scholar
  4. Anschutz U, Becker D, Shabala S (2014) Going beyond nutrition: regulation of potassium homoeostasis as a common denominator of plant adaptive responses to environment. J Plant Physiol 171:670–687Google Scholar
  5. Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol 55:373–399PubMedCrossRefGoogle Scholar
  6. Apse MP, Blumwald E (2007) Na+ transport in plants. FEBS Lett 581:2247–2254PubMedCrossRefGoogle Scholar
  7. Apse MP, Aharon GS, Snedden WA, Blumwald E (1999) Salt tolerance conferred by overexpression of a vacuolar Na+/H+ antiport in Arabidopsis. Science 285:1256–1258PubMedCrossRefGoogle Scholar
  8. Apse MP, Sottosanto JB, Blumwald E (2003) Vacuolar cation/H+ exchange, ion homeostasis, and leaf development are altered in a T-DNA insertional mutant of AtNHX1, the Arabidopsis vacuolar Na+/H+ antiporter. Plant J 36:229–239PubMedCrossRefGoogle Scholar
  9. Asensi-Fabado M, Munné-Bosch S (2011) The aba3-1 mutant of Arabidopsis thaliana withstands moderate doses of salt stress by modulating leaf growth and salicylic acid levels. J Plant Growth Regul 30:456–466CrossRefGoogle Scholar
  10. Ashraf M, Akram NA, Arteca RN, Foolad MR (2010) The physiological, biochemical and molecular roles of brassinosteroids and salicylic acid in plant processes and salt tolerance. Crit Rev Plant Sci 29:162–190CrossRefGoogle Scholar
  11. Attaran E, He SY (2012) The long-sought-after salicylic acid receptors. Mol Plant 5:971–973PubMedCentralPubMedCrossRefGoogle Scholar
  12. Barragán V, Leidi EO, Andrés Z, Rubio L, De Luca A, Fernández JA, Cubero 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 24:1127–1142PubMedCentralPubMedCrossRefGoogle Scholar
  13. Bassil E, Tajima H, Liang Y-C, Ohto M-A, Ushijima K, Nakano R, Esumi T, Coku A, Belmonte M, Blumwald E (2011) The Arabidopsis Na+/H+ antiporters NHX1 and NHX2 control vacuolar pH and K+ homeostasis to regulate growth, flower development, and reproduction. Plant Cell 23:3482–3497PubMedCentralPubMedCrossRefGoogle Scholar
  14. Berteli F, Corrales E, Guerrero C, Ariza MJ, Pliego F, Valpuesta V (1995) Salt stress increases ferredoxin-dependent glutamate synthase activity and protein level in the leaves of tomato. Physiol Plant 93:259–264CrossRefGoogle Scholar
  15. Blanco F, Salinas P, Cecchini N, Jordana X, Hummelen P, Alvarez M, Holuigue L (2009) Early genomic responses to salicylic acid in Arabidopsis. Plant Mol Biol 70:79–102PubMedCrossRefGoogle Scholar
  16. Borsani O, Valpuesta V, Botella MA (2001) Evidence for a role of salicylic acid in the oxidative damage generated by NaCl and osmotic stress in Arabidopsis seedlings. Plant Physiol 126:1024–1030PubMedCentralPubMedCrossRefGoogle Scholar
  17. Bose J, Xie Y, Shen W, Shabala S (2013) Haem oxygenase modifies salinity tolerance in Arabidopsis by controlling K+ retention via regulation of the plasma membrane H+-ATPase and by altering SOS1 transcript levels in roots. J Exp Bot 64:471–481PubMedCentralPubMedCrossRefGoogle Scholar
  18. Bose J, Rodrigo-Moreno A, Shabala S (2014a) ROS homeostasis in halophytes in the context of salinity stress tolerance. J Exp Bot 65:1241–1257PubMedCrossRefGoogle Scholar
  19. Bose J, Rodrigo-Moreno A, Lai D, Xie Y, Shen W, Shabala S (2014b) Rapid regulation of the plasma membrane H+-ATPase activity is essential to salinity tolerance in two halophyte species, Atriplex lentiformis and Chenopodium quinoa. Ann Bot (in press). doi:10.1093/aob/mcu219
  20. Cao H, Bowling SA, Gordon AS, Dong X (1994) Characterization of an Arabidopsis mutant that is nonresponsive to inducers of systemic acquired resistance. Plant Cell 6:1583–1592PubMedCentralPubMedCrossRefGoogle Scholar
  21. Cao Y, Zhang ZW, Xue LW, Du JB, Shang J, Xu F, Yuan S, Lin HH (2009) Lack of salicylic acid in Arabidopsis protects plants against moderate salt stress. Z Naturforsch C J Biosci 64:231–238Google Scholar
  22. Chang-Qing Z, Shunsaku N, Shenkui L, Tetsuo T (2008) Characterization of two plasma membrane protein 3 genes (PutPMP3) from the alkali grass, Puccinellia tenuiflora, and functional comparison of the rice homologues, OsLti6a/b from rice. Biochem Mol Biol Rep 41:448–454Google Scholar
  23. Chen H-J (1999) Ca2+-dependent excretion of salicylic acid in tobacco cell suspension culture. Bot Bull Acad Sin 40:267–273Google Scholar
  24. Chen H-J, Hou W-C, Kuc J, Lin Y-H (2001) Ca2+ dependent and Ca2+ independent excretion modes of salicylic acid in tobacco cell suspension culture. J Exp Bot 52:1219–1226PubMedCrossRefGoogle Scholar
  25. Chen Z, Newman I, Zhou M, Mendham N, Zhang G, Shabala S (2005) Screening plants for salt tolerance by measuring K+ flux: a case study for barley. Plant Cell Environ 28:1230–1246CrossRefGoogle Scholar
  26. Chen Z, Cuin TA, Zhou M, Twomey A, Naidu BP, Shabala S (2007a) Compatible solute accumulation and stress-mitigating effects in barley genotypes contrasting in their salt tolerance. J Exp Bot 58:4245–4255PubMedCrossRefGoogle Scholar
  27. Chen Z, Pottosin II, Cuin TA, Fuglsang AT, Tester M, Jha D, Zepeda-Jazo I, Zhou M, Palmgren MG, Newman IA, Shabala S (2007b) Root plasma membrane transporters controlling K+/Na+ homeostasis in salt-stressed barley. Plant Physiol 145:1714–1725PubMedCentralPubMedCrossRefGoogle Scholar
  28. Chung JS, Zhu JK, Bressan RA, Hasegawa PM, Shi H (2008) Reactive oxygen species mediate Na+-induced SOS1 mRNA stability in Arabidopsis. Plant J 53:554–565PubMedCentralPubMedCrossRefGoogle Scholar
  29. Cuin TA, Shabala S (2005) Exogenously supplied compatible solutes rapidly ameliorate NaCl-induced potassium efflux from barley roots. Plant Cell Physiol 46:1924–1933PubMedCrossRefGoogle Scholar
  30. Cuin T, Shabala S (2007) Amino acids regulate salinity-induced potassium efflux in barley root epidermis. Planta 225:753–761PubMedCrossRefGoogle Scholar
  31. Cuin TA, Betts SA, Chalmandrier R, Shabala S (2008) A root’s ability to retain K+ correlates with salt tolerance in wheat. J Exp Bot 59:2697–2706PubMedCentralPubMedCrossRefGoogle Scholar
  32. Davenport RJ, Tester M (2000) A weakly voltage-dependent, nonselective cation channel mediates toxic sodium influx in wheat. Plant Physiol 122:823–834PubMedCentralPubMedCrossRefGoogle Scholar
  33. Dean JV, Delaney SP (2008) Metabolism of salicylic acid in wild-type, ugt74f1 and ugt74f2 glucosyltransferase mutants of Arabidopsis thaliana. Physiol Plant 132:417–425PubMedCrossRefGoogle Scholar
  34. Dean JV, Mills JD (2004) Uptake of salicylic acid 2-O-β-d-glucose into soybean tonoplast vesicles by an ATP-binding cassette transporter-type mechanism. Physiol Plant 120:603–612PubMedCrossRefGoogle Scholar
  35. Dean JV, Shah RP, Mohammed LA (2003) Formation and vacuolar localization of salicylic acid glucose conjugates in soybean cell suspension cultures. Physiol Plant 118:328–336CrossRefGoogle Scholar
  36. Dean JV, Mohammed LA, Fitzpatrick T (2005) The formation, vacuolar localization, and tonoplast transport of salicylic acid glucose conjugates in tobacco cell suspension cultures. Planta 221:287–296PubMedCrossRefGoogle Scholar
  37. Delaney TP, Friedrich L, Ryals JA (1995) Arabidopsis signal transduction mutant defective in chemically and biologically induced disease resistance. Proc Natl Acad Sci 92:6602–6606PubMedCentralPubMedCrossRefGoogle Scholar
  38. Demidchik V, Cuin TA, Svistunenko D, Smith SJ, Miller AJ, Shabala S, Sokolik A, Yurin V (2010) Arabidopsis root K+-efflux conductance activated by hydroxyl radicals: single-channel properties, genetic basis and involvement in stress-induced cell death. J Cell Sci 123:1468–1479PubMedCrossRefGoogle Scholar
  39. Dempsey DA, Klessig DF (1995) Signals in plant disease resistance. Bulletin de Inst Pasteur 93:167–186CrossRefGoogle Scholar
  40. Dempsey DMA, Vlot AC, Wildermuth CM, Klessig FD (2011) Salicylic acid biosynthesis and metabolism. The Arabidopsis Book 9: e0156. doi:10.1199/tab.0156
  41. Dewdney J, Reuber TL, Wildermuth MC, Devoto A, Cui J, Stutius LM, Drummond EP, Ausubel FM (2001) Three unique mutants of Arabidopsis identify eds loci required for limiting growth of a biotrophic fungal pathogen. Plant J 24:205–218CrossRefGoogle Scholar
  42. Dodd AN, Kudla J, Sanders D (2010) The language of calcium signaling. Annu Rev Plant Biol 61:593–620PubMedCrossRefGoogle Scholar
  43. Dong X (2004) NPR1, all things considered. Curr Opin Plant Biol 7:547–552PubMedCrossRefGoogle Scholar
  44. Durner J, Klessig DF (1995) Inhibition of ascorbate peroxidase by salicylic acid and 2, 6-dichloroisonicotinic acid, two inducers of plant defense responses. Proc Natl Acad Sci 92:11312–11316PubMedCentralPubMedCrossRefGoogle Scholar
  45. El-Tayeb MA (2005) Response of barley grains to the interactive effect of salinity and salicylic acid. Plant Growth Regul 45:215–224CrossRefGoogle Scholar
  46. Eraslan F, Inal A, Pilbeam DJ, Gunes A (2008) Interactive effects of salicylic acid and silicon on oxidative damage and antioxidant activity in spinach (Spinacia oleracea L. cv. Matador) grown under boron toxicity and salinity. Plant Growth Regul 55:207–219CrossRefGoogle Scholar
  47. Forouhar F, Yang Y, Kumar D, Chen Y, Fridman E, Park SW, Chiang Y, Acton TB, Montelione GT, Pichersky E (2005) Structural and biochemical studies identify tobacco SABP2 as a methyl salicylate esterase and implicate it in plant innate immunity. Proc Natl Acad Sci 102:1773–1778PubMedCentralPubMedCrossRefGoogle Scholar
  48. Fu ZQ, Yan S, Saleh A, Wang W, Ruble J, Oka N, Mohan R, Spoel SH, Tada Y, Zheng N (2012) NPR3 and NPR4 are receptors for the immune signal salicylic acid in plants. Nature 486:228–232PubMedCentralPubMedGoogle Scholar
  49. Gaffney T, Friedrich L, Vernooij B, Negrotto D, Nye G, Uknes S, Ward E, Kessmann H, Ryals J (1993) Requirement of salicylic acid for the induction of systemic acquired resistance. Science 261:754–756PubMedCrossRefGoogle Scholar
  50. Garciadeblas B, Senn ME, Banuelos MA, Rodriguez-Navarro A (2003) Sodium transport and HKT transporters: the rice model. Plant J 34:788–801PubMedCrossRefGoogle Scholar
  51. Garcion C, Lohmann A, Lamodiere E, Catinot J, Buchala A, Doermann P, Metraux J-P (2008) Characterization and biological function of the ISOCHORISMATE SYNTHASE2 gene of Arabidopsis. Plant Physiol 147:1279–1287PubMedCentralPubMedCrossRefGoogle Scholar
  52. Gassmann W, Rubio F, Schroeder JI (1996) Alkali cation selectivity of the wheat root high-affinity potassium transporter HKT1. Plant J 10:869–882CrossRefGoogle Scholar
  53. Gaxiola RA, Rao R, Sherman A, Grisafi P, Alper SL, Fink GR (1999) The Arabidopsis thaliana proton transporters, AtNhx1 and Avp1, can function in cation detoxification in yeast. Proc Natl Acad Sci 96:1480–1485PubMedCentralPubMedCrossRefGoogle Scholar
  54. Gill SS, Tuteja N (2010) Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol Biochem 48:909–930PubMedCrossRefGoogle Scholar
  55. Guan L, Scandalios JG (1995) Developmentally related responses of maize catalase genes to salicylic acid. Proc Natl Acad Sci 92:5930–5934PubMedCentralPubMedCrossRefGoogle Scholar
  56. Guan B, Hu Y, Zeng Y, Wang Y, Zhang F (2011) Molecular characterization and functional analysis of a vacuolar Na+/H+ antiporter gene (HcNHX1) from Halostachys caspica. Mol Biol Rep 38:1889–1899PubMedCrossRefGoogle Scholar
  57. Gunes A, Inal A, Alpaslan M, Cicek N, Guneri E, Eraslan F, Guzelordu T (2005) Effects of exogenously applied salicylic acid on the induction of multiple stress tolerance and mineral nutrition in maize (Zea mays L.). Arch Agron Soil Sci 51:687–695CrossRefGoogle Scholar
  58. Gunes A, Inal A, Alpaslan M, Eraslan F, Bagci EG, Cicek N (2007) Salicylic acid induced changes on some physiological parameters symptomatic for oxidative stress and mineral nutrition in maize (Zea mays L.) grown under salinity. J Plant Physiol 164:728–736PubMedCrossRefGoogle Scholar
  59. Hao L, Zhao Y, Jin D, Zhang L, Bi X, Chen H, Xu Q, Ma C, Li G (2012) Salicylic acid-altering Arabidopsis mutants response to salt stress. Plant Soil 354:81–95CrossRefGoogle Scholar
  60. Harfouche AL, Rugini E, Mencarelli F, Botondi R, Muleo R (2008) Salicylic acid induces H2O2 production and endochitinase gene expression but not ethylene biosynthesis in Castanea sativa in vitro model system. J Plant Physiol 165:734–744PubMedCrossRefGoogle Scholar
  61. Haro R, Banuelos MA, Rodriguez-Navarro A (2010) High affinity sodium uptake in land plants. Plant Cell Physiol 51:68–79Google Scholar
  62. Hasegawa PM, Bressan RA, Zhu JK, Bohnert HJ (2000) Plant cellular and molecular responses to high salinity. Annu Rev Plant Physiol Plant Mol Biol 51:463–499PubMedCrossRefGoogle Scholar
  63. Hayat Q, Hayat S, Irfan M, Ahmad A (2010) Effect of exogenous salicylic acid under changing environment: a review. Environ Exp Bot 68:14–25CrossRefGoogle Scholar
  64. He Y, Zhu Z (2008) Exogenous salicylic acid alleviates NaCl toxicity and increases antioxidative enzyme activity in Lycopersicon esculentum. Biol Plant 52:792–795CrossRefGoogle Scholar
  65. Hennig J, Malamy J, Grynkiewicz G, Indulski J, Klessig DF (1993) Interconversion of the salicylic acid signal and its glucoside in tobacco. Plant J 4:593–600PubMedCrossRefGoogle Scholar
  66. Lee H-I, Raskin I (1998) Glucosylation of salicylic acid in Nicotiana tabacum Cv. Xanthi-nc. Phytopathology 88:692–697PubMedCrossRefGoogle Scholar
  67. Horie T, Schroeder JI (2004) Sodium transporters in plants. Diverse genes and physiological functions. Plant Physiol 136:2457–2462PubMedCentralPubMedCrossRefGoogle Scholar
  68. Horie T, Yoshida K, Nakayama H, Yamada K, Oiki S, Shinmyo A (2001) Two types of HKT transporters with different properties of Na+ and K+ transport in Oryza sativa. Plant J 27:129–138PubMedCrossRefGoogle Scholar
  69. Horie T, Horie R, Chan WY, Leung HY, Schroeder JI (2006) Calcium regulation of sodium hypersensitivities of sos3 and athkt1 mutants. Plant Cell Physiol 47:622–633PubMedCrossRefGoogle Scholar
  70. Horváth E, Janda T, Szalai G, Páldi E (2002) In vitro salicylic acid inhibition of catalase activity in maize: differences between the isozymes and a possible role in the induction of chilling tolerance. Plant Sci 163:1129–1135CrossRefGoogle Scholar
  71. Horváth E, Szalai G, Janda T (2007) Induction of abiotic stress tolerance by salicylic acid signaling. J Plant Growth Regul 26:290–300CrossRefGoogle Scholar
  72. Inada M, Ueda A, Shi W, Takabe T (2005) A stress-inducible plasma membrane protein 3 (AcPMP3) in a monocotyledonous halophyte, Aneurolepidium chinense, regulates cellular Na+ and K+ accumulation under salt stress. Planta 220:395–402PubMedCrossRefGoogle Scholar
  73. Jain A, Srivastava HS (1981) Effect of salicylic acid on nitrite reductase and glutamate dehydrogenase activities in maize roots. Physiol Plant 53:285–288CrossRefGoogle Scholar
  74. Jayakannan M, Babourina O, Rengel Z (2011) Improved measurements of Na+ fluxes in plants using calixarene-based microelectrodes. J Plant Physiol 168:1045–1051PubMedCrossRefGoogle Scholar
  75. 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 64:2255–2268PubMedCentralPubMedCrossRefGoogle Scholar
  76. Jayakannan M, Bose J, Babourina O, Shabala S, Massart A, Poschenrieder C, Rengel Z (2015) NPR1-dependent salicylic acid signalling pathway is pivotal for enhanced salt and oxidative stress tolerance in Arabidopsis. J Exp Bot. doi:10.1093/jxb/eru528
  77. Durner JR, Klessig DF (1996) Salicylic acid is a modulator of tobacco and mammalian catalases. J Biol Chem 271:28492–28501PubMedCrossRefGoogle Scholar
  78. Kawano T, Furuichi T, Muto S (2004) Controlled salicylic acid levels and corresponding signaling mechanisms in plants. Plant Biotechnol 21:319–335CrossRefGoogle Scholar
  79. Kazemi N, Khavari-Nejad RA, Fahimi H, Saadatmand S, Nejad-Sattari T (2010) Effects of exogenous salicylic acid and nitric oxide on lipid peroxidation and antioxidant enzyme activities in leaves of Brassica napus L. under nickel stress. Sci Hortic 126:402–407CrossRefGoogle Scholar
  80. Kerkeb L, Donaire JP, Rodríguez-Rosales MP (2001) Plasma membrane H+-ATPase activity is involved in adaptation of tomato calli to NaCl. Physiol Plant 111:483–490PubMedCrossRefGoogle Scholar
  81. Khan MIR, Asgher M, Khan NA (2014) Alleviation of salt-induced photosynthesis and growth inhibition by salicylic acid involves glycinebetaine and ethylene in mungbean (Vigna radiata L.). Plant Physiol Biochem 80:67–74PubMedCrossRefGoogle Scholar
  82. Kumar D, Klessig DF (2003) High-affinity salicylic acid-binding protein 2 is required for plant innate immunity and has salicylic acid-stimulated lipase activity. Sci Signal 100:16101Google Scholar
  83. Kusumi K, Yaeno T, Kojo K, Hirayama M, Hirokawa D, Yara A, Iba K (2006) The role of salicylic acid in the glutathione-mediated protection against photooxidative stress in rice. Physiol Plant 128:651–661CrossRefGoogle Scholar
  84. Lee J, Nam J, Park HC, Na G, Miura K, Jin JB, Yoo CY, Baek D, Kim DH, Jeong JC (2006) Salicylic acid-mediated innate immunity in Arabidopsis is regulated by SIZ1 SUMO E3 ligase. Plant J 49:79–90PubMedCrossRefGoogle Scholar
  85. Lee S, Kim SG, Park CM (2010) Salicylic acid promotes seed germination under high salinity by modulating antioxidant activity in Arabidopsis. New Phytol 188:626–637PubMedCrossRefGoogle Scholar
  86. Li J, Besseau S, Törönen P, Sipari N, Kollist H, Holm L, Palva ET (2013) Defense-related transcription factors WRKY70 and WRKY54 modulate osmotic stress tolerance by regulating stomatal aperture in Arabidopsis. New Phytol 200:457–472PubMedCentralPubMedCrossRefGoogle Scholar
  87. Liu Y, Zhang J, Liu H, Huang W (2008) Salicylic acid or heat acclimation pre-treatment enhances the plasma membrane-associated ATPase activities in young grape plants under heat shock. Sci Hortic 119:21–27CrossRefGoogle Scholar
  88. Liu Y, Liu H, Pan Q, Yang H, Zhan J, Huang W (2009) The plasma membrane H+-ATPase is related to the development of salicylic acid-induced thermotolerance in pea leaves. Planta 229:1087–1098PubMedCrossRefGoogle Scholar
  89. Love AJ, Milner JJ, Sadanandom A (2008) Timing is everything: regulatory overlap in plant cell death. Trends Plant Sci 13:589–595PubMedCrossRefGoogle Scholar
  90. Maathuis FJM, Amtmann A (1999) K+ nutrition and Na+ toxicity: the basis of cellular K+/Na+ ratios. Ann Bot 84:123–133CrossRefGoogle Scholar
  91. Manosalva PM, Park S-W, Forouhar F, Tong L, Fry WE, Klessig DF (2010) Methyl esterase 1 (StMES1) is required for systemic acquired resistance in potato. Mol Plant Microbe Interact 23:1151–1163PubMedCrossRefGoogle Scholar
  92. Mateo A, Mühlenbock P, Rustérucci C, Chang CC-C, Miszalski Z, Karpinska B, Parker JE, Mullineaux PM, Karpinski S (2004) LESION SIMULATING DISEASE 1 is required for acclimation to conditions that promote excess excitation energy. Plant Physiol 136:2818–2830PubMedCentralPubMedCrossRefGoogle Scholar
  93. Melotto M, Underwood W, Koczan J, Nomura K, He SY (2006) Plant stomata function in innate immunity against bacterial invasion. Cell 126:969–980PubMedCrossRefGoogle Scholar
  94. Melotto M, Underwood W, He SY (2008) Role of stomata in plant innate immunity and foliar bacterial diseases. Annu Rev Phytopathol 46:101PubMedCentralPubMedCrossRefGoogle Scholar
  95. Miller G, Suzuki N, Ciftci-Yilmaz S, Mittler R (2009) Reactive oxygen species homeostasis and signalling during drought and salinity stresses. Plant Cell Environ 33:453–467PubMedCrossRefGoogle Scholar
  96. Mitsuya S, Taniguchi M, Miyake H, Takabe T (2005) Disruption of RCI2A leads to over-accumulation of Na+ and increased salt sensitivity in Arabidopsis thaliana plants. Planta 222:1001–1009PubMedCrossRefGoogle Scholar
  97. Miura K, Tada Y (2014) Regulation of water, salinity, and cold stress responses by salicylic acid. Front plant sci. doi:10.3389/fpls.2014.00004 PubMedCentralPubMedGoogle Scholar
  98. Miura K, Lee J, Jin JB, Yoo CY, Miura T, Hasegawa PM (2009) Sumoylation of ABI5 by the Arabidopsis SUMO E3 ligase SIZ1 negatively regulates abscisic acid signaling. Proc Natl Acad Sci 106:5418–5423PubMedCentralPubMedCrossRefGoogle Scholar
  99. Miura K, Sato A, Ohta M, Furukawa J (2011) Increased tolerance to salt stress in the phosphate-accumulating Arabidopsis mutants siz1 and pho2. Planta 234:1191–1199PubMedCrossRefGoogle Scholar
  100. Miura K, Okamoto H, Okuma E, Shiba H, Kamada H, Hasegawa PM, Murata Y (2013) SIZ1 deficiency causes reduced stomatal aperture and enhanced drought tolerance via controlling salicylic acid-induced ROS accumulation in Arabidopsis. Plant J 73:91–104PubMedCrossRefGoogle Scholar
  101. Moharekar S, Lokhande S, Hara T, Tanaka R, Tanaka A, Chavan P (2003) Effect of salicylic acid on chlorophyll and carotenoid contents of wheat and moong seedlings. Photosynthetica 41:315–317CrossRefGoogle Scholar
  102. Molders W, Buchala A, Metraux J-P (1996) Transport of salicylic acid in tobacco necrosis virus-infected cucumber plants. Plant Physiol 112:787–792PubMedCentralPubMedGoogle Scholar
  103. Munns R (2005) Genes and salt tolerance: bringing them together. New Phytol 167:645–663PubMedCrossRefGoogle Scholar
  104. Munns R, Tester M (2008) Mechanisms of salinity tolerance. Annu Rev Plant Biol 59:651–681PubMedCrossRefGoogle Scholar
  105. Munns R, James RA, Xu B, Athman A, Conn SJ, Jordans C, Byrt CS, Hare RA, Tyerman SD, Tester M, Plett D, Gilliham M (2012) Wheat grain yield on saline soils is improved by an ancestral Na+ transporter gene. Nat Biotechnol 30:360–364PubMedCrossRefGoogle Scholar
  106. Mustafa NR, Kim HK, Choi YH, Erkelens C, Lefeber AWM, Spijksma G, Heijden RVD, Verpoorte R (2009) Biosynthesis of salicylic acid in fungus elicited Catharanthus roseus cells. Phytochemistry 70:532–539PubMedCrossRefGoogle Scholar
  107. Nawrath C, Metraux J-P (1999) Salicylic acid inductional deficient mutants of Arabidopsis express PR-2 and PR-5 and accumulate high levels of camalexin after pathogen inoculation. Plant Cell 11:1393–1404PubMedCentralPubMedGoogle Scholar
  108. 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 168:807–815PubMedCrossRefGoogle Scholar
  109. Nemeth M, Janda T, Horvath E, Paldi E, Szalai G (2002) Exogenous salicylic acid increases polyamine content but may decrease drought tolerance in maize. Plant Sci 162:569–574CrossRefGoogle Scholar
  110. Niederl S, Kirsch T, Riederer M, Schreiber L (1998) Co-permeability of 3H-labeled water and 14C-labeled organic acids across isolated plant cuticles investigating cuticular paths of diffusion and predicting cuticular transpiration. Plant Physiol 116:117–123PubMedCentralCrossRefGoogle Scholar
  111. Nishimura N, Kitahata N, Seki M, Narusaka Y, Narusaka M, Kuromori T, Asami T, Shinozaki K, Hirayama T (2005) Analysis of ABA hypersensitive germination2 revealed the pivotal functions of PARN in stress response in Arabidopsis. Plant J 44:972–984PubMedCrossRefGoogle Scholar
  112. Ogawa D, Nakajima N, Sano T, Tamaoki M, Aono M, Kubo A, Kanna M, Ioki M, Kamada H, Saji H (2005) Salicylic acid accumulation under O3 exposure is regulated by ethylene in tobacco plants. Plant Cell Physiol 46:1062–1072PubMedCrossRefGoogle Scholar
  113. Ohashi Y, Murakami T, Mitsuhara I, Seo S (2004) Rapid down and upward translocation of salicylic acid in tobacco plants. Plant Biotechnol 21:95–101CrossRefGoogle Scholar
  114. Ondrasek G, Rengel Z, Veres S (2011) Soil salinisation and salt stress in crop production. In: Shanker A, Venkateswarlu B (eds) Abiotic stress in plants—mechanisms and adaptations. InTech ISBN: 978-953-307-394-1, pp 171–190. doi:10.5772/22248
  115. Palmgren M, Nissen P (2010) P-type ATPases. Ann Rev Biophys 40:243–266CrossRefGoogle Scholar
  116. Pancheva TV, Popova LV (1997) Effect of salicylic acid on the synthesis of ribulose-1,5-bisphosphate carboxylase/oxygenase in barley leaves. J Plant Physiol 220:381–386Google Scholar
  117. Pandolfi C, Pottosin I, Cuin T, Mancuso S, Shabala S (2010) Specificity of polyamine effects on NaCl-induced ion flux kinetics and salt stress amelioration in plants. Plant Cell Physiol 51:422–434PubMedCrossRefGoogle Scholar
  118. Parida AK, Das AB (2005) Salt tolerance and salinity effects on plants: a review. Ecotoxicol Environ Saf 60:324–349PubMedCrossRefGoogle Scholar
  119. Park SW, Kaimoyo E, Kumar D, Mosher S, Klessig DF (2007) Methyl salicylate is a critical mobile signal for plant systemic acquired resistance. Science 318:113–116PubMedCrossRefGoogle Scholar
  120. Park SW, Liu PP, Forouhar F, Vlot AC, Tong L, Tietjen K, Klessig DF (2009) Use of a synthetic salicylic acid analog to investigate the roles of methyl salicylate and its esterases in plant disease resistance. J Biol Chem 284:7307–7317PubMedCentralPubMedCrossRefGoogle Scholar
  121. Poór P, Gémes K, Horváth F, Szepesi Á, Simon ML, Tari I (2011a) Salicylic acid treatment via the rooting medium interferes with stomatal response, CO2 fixation rate and carbohydrate metabolism in tomato, and decreases harmful effects of subsequent salt stress. Plant Biol 13:105–114PubMedCrossRefGoogle Scholar
  122. Poór P, Szopkó D, Tari I (2011b) Ionic homeostasis disturbance is involved in tomato cell death induced by NaCl and salicylic acid. In Vitro Cell Dev Biol Plant 48:377–382CrossRefGoogle Scholar
  123. Qadir M, Quillérou E, Nangia V, Murtaza G, Singh M, Thomas RJ, Drechsel P, Noble AD (2014) Economics of salt-induced land degradation and restoration. Nat Res Forum. doi:10.1111/1477-8947.12054 Google Scholar
  124. Qi Y, Tsuda K, Joe A, Sato M, Nguyen LV, Glazebrook J, Alfano JR, Cohen JD, Katagiri F (2010) A putative RNA-binding protein positively regulates salicylic acid-mediated immunity in Arabidopsis. Mol Plant Microbe Interact 23:1573–1583PubMedCrossRefGoogle Scholar
  125. Quan LJ, Zhang B, Shi WW, Li HY (2008) Hydrogen peroxide in plants: a versatile molecule of the reactive oxygen species network. J Integr Plant Biol 50:2–18PubMedCrossRefGoogle Scholar
  126. Rai V, Sharma S, Sharma S (1986) Reversal of ABA-induced stomatal closure by phenolic compounds. J Exp Bot 37:129–134CrossRefGoogle Scholar
  127. Rajjou L, Belghazi M, Huguet R, Robin C, Moreau A, Job C, Job D (2006) Proteomic investigation of the effect of salicylic acid on Arabidopsis seed germination and establishment of early defense mechanisms. Plant Physiol 141:910–923PubMedCentralPubMedCrossRefGoogle Scholar
  128. Rao MV, Davis KR (1999) Ozone-induced cell death occurs via two distinct mechanisms in Arabidopsis: the role of salicylic acid. Plant J 17:603–614PubMedCrossRefGoogle Scholar
  129. Rivas-San Vicente M, Plasencia J (2011) Salicylic acid beyond defence: its role in plant growth and development. J Exp Bot 62:3321–3338PubMedCrossRefGoogle Scholar
  130. Rodríguez-Rosales MP, Gálvez FJ, Huertas R, Aranda MN, Baghour M, Cagnac O, Venema K (2009) Plant NHX cation/proton antiporters. Plant Signal Behav 4:265–276Google Scholar
  131. Rodríguez-Rosales MP, Jiang XJ, Gálvez FJ, Aranda MN, Cubero B, Venema K (2008) Overexpression of the tomato K+/H+ antiporter LeNHX2 confers salt tolerance by improving potassium compartmentalization. New Phytol 179:366–377Google Scholar
  132. Ross JR, Nam KH, D’Auria JC, Pichersky E (1999) S-adenosyl-l-methionine: salicylic acid carboxyl methyltransferase, an enzyme involved in floral scent production and plant defense, represents a new class of plant methyltransferases. Arch Biochem Biophys 367:9–16PubMedCrossRefGoogle Scholar
  133. Rubio F, Gassmann W, Schroeder JI (1995) Sodium driven potassium uptake by the plant potassium transporter hkt1 and mutations conferring salt tolerance. Science 270:1660–1663PubMedCrossRefGoogle Scholar
  134. Sahu BB, Shaw BP (2009) Salt-inducible isoform of plasma membrane H+-ATPase gene in rice remains constitutively expressed in natural halophyte, Suaeda maritima. J Plant Physiol 166:1077–1089PubMedCrossRefGoogle Scholar
  135. Sanders D (2000) Plant biology: the salty tale of Arabidopsis. Curr Biol 10:R486–R488PubMedCrossRefGoogle Scholar
  136. Sawada H, Shim I-S, Usui K (2006) Induction of benzoic acid 2-hydroxylase and salicylic acid biosynthesis-modulation by salt stress in rice seedlings. Plant Sci 171:263–270CrossRefGoogle Scholar
  137. Seskar M, Shulaev V, Raskin I (1998) Endogenous methyl salicylate in pathogen-inoculated tobacco plants. Plant Physiol 116:387–392PubMedCentralCrossRefGoogle Scholar
  138. Shabala S (2009) Salinity and programmed cell death: unravelling mechanisms for ion specific signalling. J Exp Bot 60:709–712PubMedCrossRefGoogle Scholar
  139. Shabala S (2013) Learning from halophytes: physiological basis and strategies to improve abiotic stress tolerance in crops. Ann Bot 112:1209–1221PubMedCentralPubMedCrossRefGoogle Scholar
  140. Shabala S, Cuin TA (2008) Potassium transport and plant salt tolerance. Physiol Plant 133:651–669PubMedCrossRefGoogle Scholar
  141. Shabala S, Mackay A (2011) Ion transport in halophytes. In: Turkan I (ed) Plant Responses to Drought and Salinity Stress: Developments in a Post-Genomic Era. Elsevier, Academic Press, pp 151–199Google Scholar
  142. Shabala S, Pottosin I (2014) Regulation of potassium transport in plants under hostile conditions: implications for abiotic and biotic stress tolerance. Physiol Plant 151:257–279Google Scholar
  143. Shabala S, Shabala L, Van Volkenburgh E (2003) Effect of calcium on root development and root ion fluxes in salinised barley seedlings. Funct Plant Biol 30:507–514CrossRefGoogle Scholar
  144. Shabala L, Cuin TA, Newman IA, Shabala S (2005) Salinity-induced ion flux patterns from the excised roots of Arabidopsis sos mutants. Planta 222:1041–1050PubMedCrossRefGoogle Scholar
  145. Shabala S, Demidchik V, Shabala L, Cuin TA, Smith SJ, Miller AJ, Davies JM, Newman IA (2006) Extracellular Ca2+ ameliorates NaCl-induced K+ loss from Arabidopsis root and leaf cells by controlling plasma membrane K+-permeable channels. Plant Physiol 141:1653–1665PubMedCentralPubMedCrossRefGoogle Scholar
  146. Shabala S, Cuin TA, Prismall L, Nemchinov LG (2007) Expression of animal CED-9 anti-apoptotic gene in tobacco modifies plasma membrane ion fluxes in response to salinity and oxidative stress. Planta 227:189–197PubMedCrossRefGoogle Scholar
  147. Shakirova FM (2003) Changes in the hormonal status of wheat seedlings induced by salicylic acid and salinity. Plant Sci 164:317–322CrossRefGoogle Scholar
  148. Shi HZ, Ishitani M, Kim CS, Zhu JK (2000) The Arabidopsis thaliana salt tolerance gene SOS1 encodes a putative Na+/H+ antiporter. Proc Natl Acad Sci 97:6896–6901PubMedCentralPubMedCrossRefGoogle Scholar
  149. Shirasu K, Nakajima H, Rajasekhar VK, Dixon RA, Lamb C (1997) Salicylic acid potentiates an agonist-dependent gain control that amplifies pathogen signals in the activation of defense mechanisms. Plant Cell 9:261–270PubMedCentralPubMedCrossRefGoogle Scholar
  150. Shulaev V, Silverman P, Raskin I (1997) Airborne signalling by methyl salicylate in plant pathogen resistance. Nature 385:718–721CrossRefGoogle Scholar
  151. Smethurst CF, Rix K, Garnett T, Auricht G, Bayart A, Lane P, Wilson SJ, Shabala S (2008) Multiple traits associated with salt tolerance in lucerne: revealing the underlying cellular mechanisms. Funct Plant Biol 35:640–650CrossRefGoogle Scholar
  152. Song JT (2006) Induction of a salicylic acid glucosyltransferase, AtSGT1, is an early disease response in Arabidopsis thaliana. Mol Cells 22:233–238PubMedGoogle Scholar
  153. Song JT, Koo YJ, Seo HS, Kim MC, Choi YD, Kim JH (2008) Overexpression of AtSGT1, an Arabidopsis salicylic acid glucosyltransferase, leads to increased susceptibility to Pseudomonas syringae. Phytochemistry 69:1128–1134PubMedCrossRefGoogle Scholar
  154. Stevens J, Senaratna T, Sivasithamparam K (2006) Salicylic acid induces salinity tolerance in tomato (Lycopersicon esculentum cv. Roma): associated changes in gas exchange, water relations and membrane stabilisation. Plant Growth Regul 49:77–83Google Scholar
  155. Strawn MA, Marr SK, Inoue K, Inada N, Zubieta C, Wildermuth MC (2007) Arabidopsis isochorismate synthase functional in pathogen-induced salicylate biosynthesis exhibits properties consistent with a role in diverse stress responses. J Biol Chem 282:5919–5933PubMedCrossRefGoogle Scholar
  156. Sun W, Xu X, Zhu H, Liu A, Liu L, Li J, Hua X (2010) Comparative transcriptomic profiling of a salt-tolerant wild tomato species and a salt-sensitive tomato cultivar. Plant Cell Physiol 51:997–1006PubMedCrossRefGoogle Scholar
  157. Szepesi A, Poór P, Gémes K, Horváth E, Tari I (2008) Influence of exogenous salicylic acid on antioxidant enzyme activities in the roots of salt stressed tomato plants. Acta Biologica Szeged 52:199–200Google Scholar
  158. Szepesi A, Csiszar J, Gemes K, Horvath E, Horvath F, Simon ML, Tari I (2009) Salicylic acid improves acclimation to salt stress by stimulating abscisic aldehyde oxidase activity and abscisic acid accumulation, and increases Na+ content in leaves without toxicity symptoms in Solanum lycopersicum L. J Plant Physiol 166:914–925PubMedCrossRefGoogle Scholar
  159. Tester M, Davenport R (2003) Na+ tolerance and Na+ transport in higher plants. Ann Bot 91:503–527PubMedCentralPubMedCrossRefGoogle Scholar
  160. Tester M, Langridge P (2010) Breeding technologies to increase crop production in a changing world. Science 327:818–822PubMedCrossRefGoogle Scholar
  161. Tyerman SD (2002) Nonselective cation channels. Multiple functions and commonalities. Plant Physiol 128:327–328PubMedCentralCrossRefGoogle Scholar
  162. Tyerman SD, Skerrett IM (1999) Root ion channels and salinity. Sci Hortic 78:175–235CrossRefGoogle Scholar
  163. Tyerman SD, Skerrett M, Garrill A, Findlay GP, Leigh RA (1997) Pathways for the permeation of Na+ and Cl into protoplasts derived from the cortex of wheat roots. J Exp Bot 48:459–480PubMedCrossRefGoogle Scholar
  164. Uzunova A, Popova L (2000) Effect of salicylic acid on leaf anatomy and chloroplast ultrastructure of barley plants. Photosynthetica 38:243–250CrossRefGoogle Scholar
  165. Verberne MC, Verpoorte R, Bol JF, Mercado-Blanco J, Linthorst HJM (2000) Overproduction of salicylic acid in plants by bacterial transgenes enhances pathogen resistance. Nat Biotechnol 18:779–783PubMedCrossRefGoogle Scholar
  166. Vidhyasekaran P (2015) Salicylic Acid Signaling in Plant Innate Immunity. Plant hormone signaling systems in plant innate immunity, vol 2. Springer, Netherlands, pp 27–122Google Scholar
  167. Vlot AC, Liu P-P, Cameron RK, Park S-W, Yang Y, Kumar D, Zhou F, Padukkavidana T, Gustafsson C, Pichersky E, Klessig DF (2008) Identification of likely orthologs of tobacco salicylic acid-binding protein 2 and their role in systemic acquired resistance in Arabidopsis thaliana. Plant J 56:445–456PubMedCrossRefGoogle Scholar
  168. Vlot AC, Dempsey DMA, Klessig DF (2009) Salicylic acid, a multifaceted hormone to combat disease. Annu Rev Phytopathol 47:177–206PubMedCrossRefGoogle Scholar
  169. Wildermuth MC, Dewdney J, Wu G, Ausubel FM (2001) Isochorismate synthase is required to synthesize salicylic acid for plant defence. Nature 414:562–565PubMedCrossRefGoogle Scholar
  170. Wu C-A, Yang G-D, Meng Q-W, Zheng C-C (2004) The cotton GhNHX1 gene encoding a novel putative tonoplast Na+/H+ antiporter plays an important role in salt stress. Plant Cell Physiol 45:600–607PubMedCrossRefGoogle Scholar
  171. Wu Y, Zhang D, Chu JY, Boyle P, Wang Y, Brindle ID, De Luca V, Després C (2012) The Arabidopsis NPR1 protein is a receptor for the plant defense hormone salicylic acid. Cell Rep 1:639–647PubMedCrossRefGoogle Scholar
  172. Xia J, Zhao H, Liu W, Li L, He Y (2009) Role of cytokinin and salicylic acid in plant growth at low temperatures. Plant Growth Regul 57:211–221CrossRefGoogle Scholar
  173. Xie Z, Zhang Z-L, Hanzlik S, Cook E, Shen QJ (2007) Salicylic acid inhibits gibberellin-induced alpha-amylase expression and seed germination via a pathway involving an abscisic-acid-inducible WRKY gene. Plant Mol Biol 64:293–303PubMedCrossRefGoogle Scholar
  174. Yalpani N, Silverman P, Wilson TM, Kleier DA, Raskin I (1991) Salicylic acid is a systemic signal and an inducer of pathogenesis-related proteins in virus-infected tobacco. Plant Cell 3:809–818PubMedCentralPubMedCrossRefGoogle Scholar
  175. Yang YN, Qi M, Mei CS (2004) Endogenous salicylic acid protects rice plants from oxidative damage caused by aging as well as biotic and abiotic stress. Plant J 40:909–919PubMedCrossRefGoogle Scholar
  176. Yasuda M, Ishikawa A, Jikumaru Y, Seki M, Umezawa T, Asami T, Maruyama-Nakashita A, Kudo T, Shinozaki K, Yoshida S (2008) Antagonistic interaction between systemic acquired resistance and the abscisic acid-mediated abiotic stress response in Arabidopsis. Plant Cell 20:1678–1692PubMedCentralPubMedCrossRefGoogle Scholar
  177. Yildirim E, Turan M, Guvenc I (2008) Effect of foliar salicylic acid applications on growth, chlorophyll, and mineral content of cucumber grown under salt stress. J Plant Nutr 31:593–612CrossRefGoogle Scholar
  178. Zhang HX, Blumwald E (2001) Transgenic salt-tolerant tomato plants accumulate salt in foliage but not in fruit. Nat Biotechnol 19:765–768PubMedCrossRefGoogle Scholar
  179. Zhang HX, Hodson JN, Williams JP, Blumwald E (2001) Engineering salt-tolerant Brassica plants: characterization of yield and seed oil quality in transgenic plants with increased vacuolar sodium accumulation. Proc Natl Acad Sci 98:12832–12836PubMedCentralPubMedCrossRefGoogle Scholar
  180. Zhang X, Chen S, Mou Z (2010) Nuclear localization of NPR1 is required for regulation of salicylate tolerance, isochorismate synthase 1 expression and salicylate accumulation in Arabidopsis. J Plant Physiol 167:144–148PubMedCrossRefGoogle Scholar
  181. Zhu JK (2002) Salt and drought stress signal transduction in plants. Annu Rev Plant Biol 53:247–273PubMedCentralPubMedCrossRefGoogle Scholar
  182. Zhu JK (2003) Regulation of ion homeostasis under salt stress. Curr Opin Plant Biol 6:441–445PubMedCrossRefGoogle Scholar
  183. Zörb C, Noll A, Karl S, Leib K, Yan F, Schubert S (2005) Molecular characterization of Na+/H+ antiporters (ZmNHX) of maize (Zea mays L.) and their expression under salt stress. J Plant Physiol 162:55–66PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2015

Authors and Affiliations

  • Maheswari Jayakannan
    • 1
    • 2
    • 3
  • Jayakumar Bose
    • 2
  • Olga Babourina
    • 1
  • Zed Rengel
    • 1
  • Sergey Shabala
    • 2
  1. 1.School of Earth and EnvironmentUniversity of Western AustraliaPerthAustralia
  2. 2.School of Land and Food and Tasmanian Institute for AgricultureUniversity of TasmaniaHobartAustralia
  3. 3.School of Biological ScienceUniversity of TasmaniaHobartAustralia

Personalised recommendations