Skip to main content
Log in

Molecular mechanism of salicylic acid-induced abiotic stress tolerance in higher plants

  • Review
  • Published:
Acta Physiologiae Plantarum Aims and scope Submit manuscript

Abstract

Salicylic acid (SA), a key signaling molecule in higher plants, has been found to play a role in the response to a diverse range of phytopathogens and is essential for the establishment of both local and systemic-acquired resistance. Recent studies have indicated that SA also plays an important role in abiotic stress-induced signaling, and studies on SA-modulated abiotic tolerance have mainly focused on the antioxidant capacity of plants by altering the activity of anti-oxidative enzymes. However, little information is available about the molecular mechanisms of SA-induced abiotic stress tolerance. Here, we review recent progress toward characterizing the SA-regulated genes and proteins, the SA signaling pathway, the connections and differences between SA-induced tolerances to biotic and abiotic stresses, and the interaction of SA with other plant hormones under conditions of abiotic stress. The future prospects related to molecular tolerance of SA in response to abiotic stresses are also further summarized.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1

Similar content being viewed by others

References

  • Ahsan N, Renaut J, Komatsu S (2009) Recent developments in the application of proteomics to the analysis of plant responses to heavy metals. Proteomics 9:2602–2621

    CAS  PubMed  Google Scholar 

  • Alonso-Ramírez A, Rodríguez D, Reyes D, Jiménez JA, Nicolás G, López-Climent M, Gómez-Cadenas A, Nicolás C (2009) Evidence for a role of gibberellins in salicylic acid-modulated early plant responses to abiotic stress in Arabidopsis seeds. Plant Physiol 150:1335–1344

    PubMed Central  PubMed  Google Scholar 

  • An C, Mou Z (2011) Salicylic acid and its function in plant immunity. J Integr Plant Biol 53:412–428

    CAS  PubMed  Google Scholar 

  • 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 29:162–190

    CAS  Google Scholar 

  • Bari R, Jones JDG (2009) Role of plant hormones in plant defense response. Plant Mol Biol 69:473–488

    CAS  PubMed  Google Scholar 

  • Boston RS, Viitanen PV, Vierling E (1996) Molecular chaperones and protein folding in plants. Plant Mol Biol 32:191–222

    CAS  PubMed  Google Scholar 

  • Campo S, Peris-Peris C, Montesinos L, Peñas G, Messeguer J, San Segundo B (2012) Expression of the maize ZmGF14-6 gene in rice confers tolerance to drought stress while enhancing susceptibility to pathogen infection. J Exp Bot 63:983–999

    CAS  PubMed Central  PubMed  Google Scholar 

  • Chen S, Liu Z, Cui J, Ding J, Xia X, Liu D, Yu J (2011) Alleviation of chilling-induced oxidative damage by salicylic acid pretreatment and related gene expression in eggplant seedlings. Plant Growth Regul 65:101–108

    CAS  Google Scholar 

  • Chinnusamy V, Zhu J, Zhu JK (2006) Salt stress signaling and mechanisms of plant salt tolerance. Genet Eng 27:141–177

    CAS  Google Scholar 

  • Cummins I, Cole DJ, Edwards R (1999) A role for glutathione transferases functioning as glutathione peroxidases in resistance to multiple herbicides in black-grass. Plant J 18:285–292

    CAS  PubMed  Google Scholar 

  • De las Mercedes Dana M, Pintor-Toro JA, Cubero B (2006) Transgenic tobacco plants overexpressing chitinases of fungal origin show enhanced resistance to biotic and abiotic stress agents. Plant Physiol 142:722–730

    PubMed  Google Scholar 

  • de Oliveira TM, Cidade LC, Gesteira AS, Coelho-Filho MA, Soares-Filho WS, Costa MGC (2011) Analysis of the NAC transcription factor gene family in citrus reveals a novel member involved in multiple abiotic stress responses. Tree Genet Genomes 7:1123–1134

    Google Scholar 

  • Dempsey DA, Shah J, Klessig DF (1999) Salicylic acid and disease resistance in plants. Crit Rev Plant Sci 18:547–575

    CAS  Google Scholar 

  • Ding CK, Wang CY, Gross KC (2002) Jasmonate and salicylate induce the expression of pathogenesis-related- protein genes and increase resistance to chilling injury in tomato fruit. Planta 214:895–901

    CAS  PubMed  Google Scholar 

  • Duan M, Feng HL, Wang LY, Li D, Meng QW (2012) Overexpression of thylakoidal ascorbate peroxidase shows enhanced resistance to chilling stress in tomato. J Plant Physiol 169:867–877

    CAS  PubMed  Google Scholar 

  • Durrant WE, Dong X (2004) Systemic acquired resistance. Annu Rev Phytopathol 42:185–209

    CAS  PubMed  Google Scholar 

  • Eltayeb AE, Kawano N, Badawi GH, Kaminaka H, Sanekata T, Shibahara T, Inanaga S, Tanaka K (2007) Enhanced tolerance to ozone and drought stresses in transgenic tobacco overexpressing dehydroascorbate reductase in cytosol. Planta 225:1255–1264

    CAS  PubMed  Google Scholar 

  • Fernandez DEF, Heck G, Perry SE, Patterson SE, Bleecker AB, Fang SC (2000) The embryo MADS domain factor AGL15 acts postembryonically inhibition of perianth senescence and abscission via constitutive expression. Plant Cell 12:183–198

    CAS  PubMed Central  PubMed  Google Scholar 

  • Fiorani F, Umbach AL, Siedow JN (2005) The alternative oxidase of plant mitochondria is involved in the acclimation of shoot growth at low temperature. A study of Arabidopsis AOX1a transgenic plants. Plant Physiol 139:1795–1805

    CAS  PubMed Central  PubMed  Google Scholar 

  • Fung RW, Wang CY, Smith DL, Gross KC, Tao Y, Tian M (2006) Characterization of alternative oxidase (AOX) gene expression in response to methyl salicylate and methyl jasmonate pre-treatment and low temperature in tomatoes. J Plant Physiol 163:1049–1060

    CAS  PubMed  Google Scholar 

  • Garcia AB, Engler Jde A, Claes B, Villarroel R, Van Montagu M, Gerats T, Caplan A (1998) The expression of the salt-responsive gene salt from rice is regulated by hormonal and developmental cues. Planta 207:172–180

    CAS  PubMed  Google Scholar 

  • Hanafy MS, El-Banna A, Schumacher HM, Jacobsen HJ, Hassan FS (2013) Enhanced tolerance to drought and salt stresses in transgenic faba bean (Vicia faba L.) plants by heterologous expression of the PR10a gene from potato. Plant Cell Rep 32:663–674

    CAS  PubMed  Google Scholar 

  • Hao JH, Dong CJ, Zhang ZG, Wang XL, Shang QM (2012) Insights into salicylic acid responses in cucumber (Cucumis sativus L.) cotyledons based on a comparative proteomic analysis. Plant Sci 187:69–82

    CAS  PubMed  Google Scholar 

  • Hayat Q, Hayat S, Irfan M, Ahmad A (2010) Effect of exogenous salicylic acid under changing environment: a review. Environ Exp Bot 68:14–25

    CAS  Google Scholar 

  • Holtzapffel RC, Castelli J, Finnegan PM, Millar AH, Whelan J, Day DA (2003) A tomato alternative oxidase protein with altered regulatory properties. Biochim Biophys Acta 1606:153–162

    CAS  PubMed  Google Scholar 

  • Hong JK, Hwang BK (2005a) Functional characterization of PR-1 protein, β-1,3-glucanase and chitinase genes during defense response to biotic and abiotic stresses in Capsicum annuum. Plant Pathol J 21:195–206

    Google Scholar 

  • Hong JK, Hwang BK (2005b) Induction of enhanced disease resistance and oxidative stress tolerance by overexpression of pepper basic PR-1 gene in Arabidopsis. Physiol Plant 124:267–277

    CAS  Google Scholar 

  • Horváth E, Szalai G, Janda T (2007) Induction of abiotic stress tolerance by salicylic acid signaling. J Plant Growth Regul 26:290–300

    Google Scholar 

  • Hoshida H, Tanaka Y, Hibino T, Hayashi Y, Tanaka A, Takabe T, Takabe T (2000) Enhanced tolerance to salt stress in transgenic rice that overexpresses chloroplast glutamine synthetase. Plant Mol Biol 43:103–111

    CAS  PubMed  Google Scholar 

  • Hossain MA, Munemasa S, Uraji M, Nakamura Y, Mori IC, Murata Y (2011) Involvement of endogenous abscisic acid in methyl jasmonate-induced stomatal closure in Arabidopsis. Plant Physiol 156:430–438

    CAS  PubMed Central  PubMed  Google Scholar 

  • Jain S, Kumar D, Jian M, Chaudhary P, Deswal P, Sarin NB (2012) Ectopic overexpression of a salt stress-induced pathogenesis-related class 10 protein (PR10) gene from peanut (Arachis hypogaea L.) affords broad spectrum abiotic stress tolerance in transgenic tobacco. Plant Cell Tiss Org 109:19–31

    CAS  Google Scholar 

  • Jeong MJ, Park SC, Byun MO (2001) Improvement of salt tolerance in transgenic potato plants by glyceraldehyde- 3-phosphate dehydrogenase gene transfer. Mol Cell 12:185–189

    CAS  Google Scholar 

  • Jin H, Huang F, Cheng H, Song H, Yu D (2013) Overexpression of the GmNAC2 gene, an NAC transcription factor, reduces abiotic stress tolerance in tobacco. Plant Mol Biol Rep 31:435–442

    CAS  Google Scholar 

  • Jonak C, Ökrész L, Bo¨gre L, Hirt H (2002) Complexity, cross talk and integration of plant MAP kinase signalling. Curr Opin Plant Biol 5:415–424

    CAS  PubMed  Google Scholar 

  • Kang G, Wang C, Sun G, Wang Z (2003) Salicylic acid changes activities of H2O2-metabolizing enzymes and increases the chilling tolerance of banana seedlings. Environ Exp Bot 50:9–15

    CAS  Google Scholar 

  • Kang G, Li G, Xu W, Peng X, Han Q, Zhu Y, Guo T (2012a) Proteomics reveals the effects of salicylic acid on growth and tolerance to subsequent drought stress in wheat. J Proteome Res 11:6066–6079

    CAS  PubMed  Google Scholar 

  • Kang G, Li G, Zheng B, Han Q, Wang C, Zhu Y, Guo T (2012b) Proteomic analysis on salicylic acid-induced salt tolerance in common wheat seedlings. BBA-Proteins Proteom. BBA Proteins Proteom 1824:1324–1333

    CAS  Google Scholar 

  • Kang G, Le G, Liu G, Xu W, Peng X, Wang C, Zhu Y, Guo T (2013) Exogenous salicylic acid enhances wheat drought tolerance by influence on the expression of genes related to ascorbate-glutathione cycle. Biol Plant 57:718–724

    CAS  Google Scholar 

  • Kazan K, Manners JM (2009) Linking development to defense: auxin in plant–pathogen interactions. Trends Plant Sci 14:373–382

    CAS  PubMed  Google Scholar 

  • Khan MIR, Khan NA (2013) Salicylic acid and jasmonates: approaches in abiotic stress tolerance. J Plant Biochem Physiol 1:4

    Google Scholar 

  • Khan NA, Syeed S, Masood A, Nazar R, Iqbal N (2010) Application of salicylic acid increases contents of nutrients and antioxidative metabolism in mungbean and alleviates adverse effects of salinity stress. Int J Plant Biol 15:19–21

    Google Scholar 

  • Khan MIR, Iqbal N, Masood A, Per TS, Khan NA (2013) Salicylic acid alleviates adverse effects of heat stress on photosynthesis through changes in proline production and ethylene formation. Plant Signal Behav 8:e26374

    PubMed Central  PubMed  Google Scholar 

  • Khodary S (2004) Effect of salicylic acid on the growth, photosynthesis and carbohydrate metabolism in salt-stressed maize plants. Int J Agric Biol 6:5–8

    CAS  Google Scholar 

  • Kim ST, Yu S, Kang YH, Kim SG, Kang KY (2008) The rice pathogen-related protein 10 (JIOsPR10) is induced by abiotic and biotic stresses and exhibits ribonuclease activity. Plant Cell Rep 27:593–603

    CAS  PubMed  Google Scholar 

  • Kohli A, Sreenivasulu N, Lakshmanan P, Kumar PP (2013) The phytohormone crosstalk paradigm takes center stage in understanding how plants respond to abiotic stresses. Plant Cell Rep 32:945–957

    CAS  PubMed  Google Scholar 

  • Kundu S, Chakraborty D, Pal A (2011) Proteomic analysis of salicylic acid induced resistance to Mungbean Yellow Mosaic India Virus in Vigna mungo. J Proteomics 74:337–349

    CAS  PubMed  Google Scholar 

  • Kwon Y, Kim SH, Jung MS, Kim MS, Oh JE, Ju HW, Kim KI, Vierling E, Lee H, Hong SW (2007) Arabidopsis hot2 encodes an endochitinase-like protein that is essential for tolerance to heat, salt and drought stresses. Plant J 49:184–198

    CAS  PubMed  Google Scholar 

  • Lei T, Feng H, Sun X, Dai QL, Zhang F, Liang HG, Lin HH (2010) The alternative pathway in cucumber seedlings under low temperature stress was enhanced by salicylic acid. Plant Growth Regul 60:35–42

    CAS  Google Scholar 

  • Li G, Peng X, Wei L, Kang G (2013) Salicylic acid increases the contents of glutathione and ascorbate and temporally regulates the related gene expression in salt-stressed wheat seedlings. Gene 529:321–325

    CAS  PubMed  Google Scholar 

  • Liu JJ, Ekramoddoullah AKM, Hawkins B, Shah S (2013) Overexpression of a western white pine PR10 protein enhances cold tolerance in transgenic Arabidopsis. Plant Cell Tissue Org 114:217–223

    CAS  Google Scholar 

  • Loake G, Grant M (2007) Salicylic acid in plant defence–the players and protagonists. Curr Opin Plant Biol 10:466–472

    CAS  PubMed  Google Scholar 

  • Metwally A, Finkemeier I, Georgi M, Dietz KJ (2003) Salicylic acid alleviates the cadmium toxicity in barley seedlings. Plant Physiol 132:272–281

    CAS  PubMed Central  PubMed  Google Scholar 

  • Mittler R (2002) Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci 7:405–410

    CAS  PubMed  Google Scholar 

  • Miura K, Tada Y (2014) Regulation of water, salinity, and cold stress responses by salicylic acid. Front Plant Sci 5:4

    PubMed Central  PubMed  Google Scholar 

  • 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 accumulation of reactive oxygen species in Arabidopsis. Plant J 49:79–90

    Google Scholar 

  • Nagamiya K, Motohashi T, Nakao K, Prodhan SH, Hattonri E, Hirose S, Ozawa K, Ohkawa Y, Takabe T, Takabe T, Komamine A (2007) Enhancement of salt tolerance in transgenic rice expressing an Escherichia coli catalase gene, katE. Plant Biotechnol Rep 1:49–55

    Google Scholar 

  • 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 168:807–815

    CAS  PubMed  Google Scholar 

  • Palma F, López-Gómez M, Tejera NA, Lluch C (2013) Salicylic acid improves the salinity tolerance of Medicago sativa in symbiosis with Sinorhizobium meliloti by preventing nitrogen fixation inhibition. Plant Sci 208:75–82

    CAS  PubMed  Google Scholar 

  • 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 mechanism. Plant Physiol 141:910–923

    CAS  PubMed Central  PubMed  Google Scholar 

  • Raskin I (1992) Role of salicylic acid in plants. Annu Rev Plant Physiol 43:438–463

    Google Scholar 

  • Rospert S, Dubaquie Y, Gautschi M (2002) Nascent-polypeptide-associated complex. Cell Mol Life Sci 59:1632–1639

    CAS  PubMed  Google Scholar 

  • Sarowar S, Kim YJ, Kim EN, Kim KD, Hwang BK, Islam R, Shin JS (2005) Overexpression of a pepper basic pathogenesis-related protein 1 gene in tobacco plants enhances resistance to heavy metal and pathogen stresses. Plant Cell Rep 24:216–224

    CAS  PubMed  Google Scholar 

  • Seo PJ, Lee AK, Xiang F, Park CM (2008) Molecular and functional profiling of arabidopsis pathogenesis-related genes: insights into their roles in salt response of seed germination. Plant Cell Physiol 49:334–344

    CAS  PubMed  Google Scholar 

  • Shan C, Liang Z (2010) Jasmonic acid regulates ascorbate and glutathione metabolism in Agropyron cristatum leaves under water stress. J Plant Physiol 178:130–139

    CAS  Google Scholar 

  • Shekhawat UKS, Ganapathi TR (2013) Musa WRKY71 overexpression in banana plants leads to altered abiotic and biotic stress responses. Plos One 8:75506

    Google Scholar 

  • Shukla RK, Raha S, Tripathi V, Chattopadhyay D (2006) Expression of CAP2, an APETALA2-family transcription factor from chickpea, enhances growth and tolerance to dehydration and salt stress in transgenic tobacco. Plant Physiol 142:113–123

    CAS  PubMed Central  PubMed  Google Scholar 

  • Singh B, Usha K (2003) Salicylic acid induced physiological and biochemical changes in wheat seedlings under water stress. Plant Growth Regul 39:137–141

    CAS  Google Scholar 

  • Slotkin RK, Martienssen R (2007) Transposable elements and the epigenetic regulation of the genome. Nat Rev Genet 8:272–285

    CAS  PubMed  Google Scholar 

  • Snyman M, Cronjé J (2008) Modulation of heat shock factors accompanies salicylic acid-mediated potentiation of Hsp70 in tomato seedlings. J Exp Bot 59:2125–2132

    CAS  PubMed Central  PubMed  Google Scholar 

  • Springer NM, Napoli CA, Selinger DA, Pandey R, Cone KC, Chandler VL, Kaeppler H, Kaeppler SM (2003) Comparative analysis of SET domain proteins in maize and Arabidopsis reveals multiple duplications preceding the divergence of monocots and dicots. Plant Physiol 132:907–925

    CAS  PubMed Central  PubMed  Google Scholar 

  • Sultana S, Khew CY, Morshed MM, Namasivayam P, Napis S, Ho CL (2012) Overexpression of monodehydroascorbate reductase from a mangrove plant (AeMDHAR) confers salt tolerance on rice. J Plant Physiol 169:311–318

    CAS  PubMed  Google Scholar 

  • Syeed S, Anjum NA, Nazar R, Iqbal N, Masood A, Khan NA (2011) Salicylic acid-mediated changes in photosynthesis, nutrients content and antioxidant metabolism in two mustard (Brassica juncea L.) cultivars differing in salt tolerance. Acta Physiol Plant 33:877–886

    CAS  Google Scholar 

  • Vicente MR, Plasencia J (2011) Salicylic acid beyond defence: its role in plant growth and development. J Exp Bot 62:3321–3338

    Article  Google Scholar 

  • Vlot AC, Dempsey DA, Klessig DF (2009) Salicylic acid, a multifaceted hormone to combat disease. Annu Rev Phytopathol 47:177–206

    Article  CAS  PubMed  Google Scholar 

  • Wang WX, Vinocur B, Shoseyov O, Altman A (2004) Role of plant heat-shock proteins and molecular chaperones in the abiotic stress response. Trends Plant Sci 9:244–252

    Article  CAS  PubMed  Google Scholar 

  • Wang L, Chen S, Kong W, Li S, Archbold DD (2006) Salicylic acid pretreatment alleviates chilling injury and affects the antioxidant system and heat shock proteins of peaches during cold storage. Postharvest Biol Technol 41:244–251

    Article  Google Scholar 

  • Wang DH, LiXX SuZK, Ren HX (2009) The role of salicylic acid in response of two rice cultivars to chilling stress. Biol Plant 53:545–552

    Article  CAS  Google Scholar 

  • Wang N, Xiao B, Xiong L (2011) Identification of a cluster of PR4-like genes involved in stress responses in rice. J Plant Physiol 168:2212–2224

    Article  CAS  PubMed  Google Scholar 

  • Wiedmann B, Sakai H, Davis TA, Wiedmann M (1994) A protein complex required for signal-sequence-specific sorting and translocation. Nature 370:434–440

    Article  CAS  PubMed  Google Scholar 

  • Wildermuth MC (2006) Variations on a theme: synthesis and modification of plant benzoic acids. Curr Opin Plant Biol 9:288–296

    Article  CAS  PubMed  Google Scholar 

  • Wildermuth MC, Dewdney J, Wu G, Ausubel FM (2001) Isochorismate synthase is required to synthesize salicylic acid for plant defence. Nature 414:562–565

    Article  CAS  PubMed  Google Scholar 

  • Xu D, Duan X, Wang B, Hong B, Ho THD, 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 110:249–257

    CAS  PubMed Central  PubMed  Google Scholar 

  • Yuan S, Lin HH (2008) Role of salicylic acid in plant abiotic stress. Z Naturforsch C 63:313–320

    CAS  PubMed  Google Scholar 

  • 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 11:49–67

    Article  PubMed  Google Scholar 

  • Zhang Z, Zhang Q, Wu J, Zheng X, Zheng S, Sun X, Qiu Q, Lu T (2013) Gene knockout study reveals that cytosolic ascorbate peroxidase 2(OsAPX2) plays a critical role in growth and reproduction in rice under drought, salt and cold stresses. PLos One 8:e57472

    Article  CAS  PubMed Central  PubMed  Google Scholar 

Download references

Acknowledgments

We apologize to our colleagues whose valuable works have not been cited in this paper because of our inadvertent pretermission.

Conflict of interest

The authors declare no competing financial interest.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Guozhang Kang.

Additional information

Communicated by A. K. Kononowicz.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kang, G., Li, G. & Guo, T. Molecular mechanism of salicylic acid-induced abiotic stress tolerance in higher plants. Acta Physiol Plant 36, 2287–2297 (2014). https://doi.org/10.1007/s11738-014-1603-z

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11738-014-1603-z

Keywords

Navigation