Molecular basis of salicylic acid–phytohormone crosstalk in regulating stress tolerance in plants

Puja Ghosh1, Aryadeep Roychoudhury2
1Department of Biotechnology, St. Xavier’s College (Autonomous), 30, Mother Teresa Sarani, Kolkata, West Bengal, 700016, India
2Discipline of Life Sciences, School of Sciences, Indira Gandhi National Open University, Maidan Garhi, New Delhi 110068, India

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Achuo EA, Prinsen E, Höfte M (2006) Influence of drought, salt stress and abscisic acid on the resistance of tomato to Botrytis cinerea and Oidium neolycopersici. Plant Pathol 55:178–186

Ahmed W, Imran M, Yaseen M, Haq TU, Jamshaid MU, Rukh S, Ikram RM, Ali M, Ali A, Maqbool M et al (2020) Role of salicylic acid in regulating ethylene and physiological characteristics for alleviating salinity stress on germination, growth and yield of sweet pepper. Peer J 8:e8475

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

Anderson JP, Badruzsaufari E, Schenk PM, Manners JM, Desmond OJ, Ehlert C, Maclean DJ, Ebert PR, Kazan K (2004) Antagonistic interaction between abscisic acid and jasmonate-ethylene signaling pathways modulates defense gene expression and disease resistance in Arabidopsis. Plant Cell 16:3460–3479

Antoniw JF, White RF (1980) The effects of aspirin and polyacrylic-acid on soluble leaf proteins and resistance to virus-infection in 5 cultivars of tobacco. J Phytopathol 98:331–341

Arnao MB, Hernández-Ruiz J (2018) Melatonin and its relationship to plant hormones. Ann Bot 121:195–207

Arnao MB, Hernández-Ruiz J (2019) Melatonin: a new plant hormone and/or a plant master regulator? Trends Plant Sci 24:38–48

Bailey T, Zhou X, Chen J, Yang Y (2009) Role of ethylene, abscisic acid and map kinase pathways in rice blast resistance. Advances in genetics, genomics and control of rice blast disease. Springer, The Netherlands, pp 185–190

Baltacıer G, Donat S, Acar O (2023) The effects of exogenous salicylic acid and strigolactone applications on seedling growth and antioxidant activity in tomato seedlings under short-term drought stress. J Inst Sci Technol 13:89–101

Bandurska H, Stroinski A (2005) The effect of salicylic acid on barley response to water deficit. Acta Physiol Plant 27:379–386

Bari R, Jones JD (2009) Role of plant hormones in plant defence responses. Plant Mol Biol 69:473–488

Bazinet Q, Tang L, Bede JC (2022) Impact of future elevated carbon dioxide on C(3) plant resistance to biotic stresses. Mol Plant Microbe Interact 35:527–539

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 126:1024–1030

Chen H, Bullock DA Jr, Alonso JM, Stepanova AN (2021) To fight or to grow: the balancing role of ethylene in plant abiotic stress responses. Plants 11:33

Choi J, Huh SU, Kojima M, Sakakibara H, Paek KH, Hwang I (2010) The cytokinin-activated transcription factor ARR2 promotes plant immunity via TGA3/NPR1-dependent salicylic acid signaling in Arabidopsis. Dev Cell 19:284–295

Clouse SD (2011) Brassinosteroid signal transduction: from receptor kinase activation to transcriptional networks regulating plant development. Plant Cell 23:1219–1230

de Torres ZM, Bennett MH, Truman WH, Grant MR (2009) Antagonism between salicylic and abscisic acid reflects early host-pathogen conflict and moulds plant defence responses. Plant J 59:375–386

Delaney TP, Uknes S, Vernooij B, Friedrich L, Weymann K, Negrotto D et al (1994) A central role of salicylic-acid in plant-disease resistance. Science 266:1247–1250

Dempsey DA, Klessig DF (2017) How does the multifaceted plant hormone salicylic acid combat disease in plants and are similar mechanisms utilized in humans? BMC Biol 15:1–11

Du Z, Zhou X, Ling Y, Zhang Z, Su Z (2010) Agrigo: a go analysis toolkit for the agricultural community. Nucleic Acids Res 38:W64–W70

Duan L, Liu H, Li X, Xiao J, Wang S (2014) Multiple phytohormones and phytoalexins are involved in disease resistance to Magnaporthe oryzae invaded from roots in rice. Physiol Plant 152:486–500

Dubey S, Misra P, Dwivedi S, Chatterjee S, Bag SK, Mantri S, Asif MH, Rai A, Kumar S, Shri M, Tripathi P (2010) Transcriptomic and metabolomic shifts in rice roots in response to Cr (VI) stress. BMC Genom 11:648

El-Sherif NA (2022) Salicylic acid and its crosstalk with other plant hormones under stressful environments. In: managing plant stress using salicylic acid: physiological and molecular aspects, pp 304–317

Emamverdian A, Ding Y, Mokhberdoran F (2020) The role of salicylic acid and gibberellin signaling in plant responses to abiotic stress with an emphasis on heavy metals. Plant Signal Behav 15:1777372

Erpen L, Devi HS, Grosser JW, Dutt M (2018) Potential use of the DREB/ERF, MYB, NAC and WRKY transcription factors to improve abiotic and biotic stress in transgenic plants. Plant Cell Tissue Organ Cult 132:1–25

Esmaeili S, Sharifi M, Ghanati F, Soltani BM, Samari E, Sagharyan M (2023) Exogenous melatonin induces phenolic compounds production in Linum album cells by altering nitric oxide and salicylic acid. Sci Rep 13:4158

Falkowska M, Pietryczuk A, Piotrowska A, Bajguz A, Grygoruk A, Czerpak R (2011) The effect of gibberellic acid (GA3) on growth, metal biosorption and metabolism of the green algae Chlorella vulgaris (chlorophyceae) beijerinck exposed to cadmium and lead stress. Pol J Environ Stud 20:53–59

Fan J, Hill L, Crooks C, Doerner P, Lamb C (2009) Abscisic acid has a key role in modulating diverse plant–pathogen interactions. Plant Physiol 150:1750–1761

Faraz A, Faizan M, Sami F et al (2020) Supplementation of salicylic acid and citric acid for alleviation of cadmium toxicity to Brassica juncea. J Plant Growth Regul 39:641–655

Flors V, Ton J, van Doorn R, Jakab G, Garcia-Agustin P, Mauch-Mani B (2008) Interplay between JA, SA and ABA signaling during basal and induced resistance against Pseudomonas syringae and Alternaria brassicicola. Plant J 54:81–92

Foyer CH, Noctor G (2020) Redox homeostasis and signaling in a higher CO2 world. Annu Rev Plant Biol 71:157–182

Fragniere C, Serrano M, Abou-Mansour E, Metraux JP, L’Haridon F (2011) Salicylic acid and its location in response to biotic and abiotic stress. FEBS Lett 585:1847–1852

Friedrich L, Vernooij B, Gaffney T, Morse A, Ryals J (1995) Characterization of tobacco plants expressing a bacterial salicylate hydroxylase gene. Plant Mol Biol 29:959–968

Ghosh P, Banerjee A, Roychoudhury A (2023) Dissecting the biochemical and molecular-genetic regulation of diverse metabolic pathways governing aroma formation in indigenous aromatic Indica rice varieties. Mol Biol Rep 50:2479–2500

Gull A, Ahmad Lone A, Ul Islam Wani N (2019) Biotic and abiotic stresses in plants. Intech Open, p 85832

Gupta A, Bhardwaj M, Tran LP (2020) Jasmonic acid at the crossroads of plant immunity and Pseudomonas syringae virulence. Int J Mol Sci 21(20):7482

Hao Y, Huang B, Jia D, Mann T, Jiang X, Qiu Y, Niitsu M, Berberich T, Kusano T, Liu T (2018) Identification of seven polyamine oxidase genes in tomato (Solanum lycopersicum L.) and their expression profiles under physiological and various stress conditions. J Plant Physiol 228:1–11

He X, Jiang JS, Wang CQ, Dehesh K (2017) ORA59 and EIN3 interaction couples jasmonate-ethylene synergistic action to antagonistic salicylic acid regulation of PDF expression. J Integr Plant Biol 59:275–287

He M-W, Wang Y, Wu J-Q, Shu S, Sun J, Guo S-R (2019) Isolation and characterization of S-Adenosylmethionine synthase gene from cucumber and responsive to abiotic stress. Plant Physiol Biochem 141:431–445

Hernández-Ruiz J, Arnao BM (2018) Relationship of melatonin and salicylic acid in biotic/abiotic plant stress responses. Agronomy 8:33

Hu Y, Dong Q, Yu D (2012) Arabidopsis WRKY46 coordinates with WRKY70 and WRKY53 in basal resistance against pathogen Pseudomonas syringae. Plant Sci 185–186:288–297

Hu Y, Jiang Y, Han X et al (2017) Jasmonate regulates leaf senescence and tolerance to cold stress: crosstalk with other phytohormones. J Exp Bot 68:1361–1369

IPCC Climate Change (2022) Impacts, adaptation and vulnerability. Working group II contribution to the IPCC sixth assessment report. IPCC, Cambridge, UK; New York, NY, USA

Jammes F, Song C, Shin D, Munemasa S, Takeda K, Gu D, Cho D, Lee S, Giordo R, Sritubtim S, Leonhardt N, Ellis BE, Murata Y, Kwak JM (2009) MAP kinases MPK9 and MPK12 are preferentially expressed in guard cells and positively regulate ROS-mediated ABA signaling. Proc Natl Acad Sci USA 106:20520–20525

Janda T, Szalai G, Tari I et al (1999) Hydroponic treatment with salicylic acid decreases the effects of chilling injury in maize (Zea mays L.) plants. Planta 208:175–180

Javid MG, Sorooshzadeh A, Moradi F, Sanavy SAMM, Allahdadi I (2011) The role of phytohormones in alleviating salt stress in crop plants. Aust J Crop Sci 5:726–734

Jiang CJ, Shimono M, Sugano S, Kojima M, Yazawa K, Yoshida R, Inoue H, Hayashi N, Sakakibara H, Takatsuji H (2010) Abscisic acid interacts antagonistically with salicylic acid signaling pathway in rice-Magnaporthe grisea interaction. Mol Plant Microbe Interact 23:791–798

Jiang CJ, Shimono M, Sugano S, Kojima M, Liu X, Inoue H, Sakakibara H, Takatsuji H (2013) Cytokinins act synergistically with salicylic acid to activate defense gene expression in rice. Mol Plant Microbe Interact 26:287–296

Jones JD, Dangl JL (2006) The plant immune system. Nature 444:323–329

Kaya C, Ugurlar F, Ashraf M, Ahmad P (2023) Salicylic acid interacts with other plant growth regulators and signal molecules in response to stressful environments in plants. Plant Physiol Biochem 196:431–443

Kazan K (2018) Plant-biotic interactions under elevated CO2: a molecular perspective. Environ Exp Bot 153:249–261

Kazan K, Lyons R (2014) Intervention of phytohormone pathways by pathogen effectors. Plant Cell 26:2285–2309

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

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 80:67–74

Khan MIR, Fatma M, Per TS, Anjum NA, Khan NA (2015) Salicylic acid-induced abiotic stress tolerance and underlying mechanisms in plants. Front Plant Sci 6:462

Kim TW, Wang ZY (2010) Brassinosteroid signal transduction from receptor kinases to transcription factors. Annu Rev Plant Biol 61:681–704

Kim Y-W, Youn J-H, Roh J, Kim J-M, Kim S-K, Kim T-W (2022) Brassinosteroids enhance salicylic acid-mediated immune responses by inhibiting BIN2 phosphorylation of clade I TGA transcription factors in Arabidopsis. Mol Plant 15:991–1007

Kiraly Z, Pozsar B, Hammady ME (1966) Cytokinin activity in rust-infected plants: juvenility and senescence in diseased leaf tissues. Acta Phytopathol Acad Sci Hung 1:29–37

Kiraly Z, Hammady ME, Pozsar B (1967) Increased cytokinin activity of rust-infected bean and broad bean leaves. Phytopathology 57:93–94

Koga H, Dohi K, Mori M (2004) Abscisic acid and low temperatures suppress the whole plant-specific resistance reaction of rice plants to the infection of Magnaporthe grisea. Physiol Mol Plant Pathol 65:3–9

Križnik M, Petek M, Dobnik D, Ramšak Ž, Baebler Š, Pollmann S, Kreuze JF, Žel J, Gruden K (2017) Salicylic acid perturbs sRNA-gibberellin regulatory network in immune response of potato to potato virus Y infection. Front Plant Sci 8:2192

Ku Y-S, Sintaha M, Cheung M-Y, Lam H-M (2018) Plant hormone signaling crosstalks between biotic and abiotic stress responses. Int J Mol Sci 19:3206

Kuiper D, Schuit J, Kuiper PJC (1990) Actual cytokinin concentrations in plant tissue as an indicator for salt resistance in cereals. Plant Soil 123:243–250

Kurotani K, Hayashi K, Hatanaka S, Toda Y, Ogawa D, Ichikawa H, Ishimaru Y, Tashita R, Suzuki T, Ueda M et al (2015) Elevated levels of CYP94 family gene expression alleviate the jasmonate response and enhance salt tolerance in rice. Plant Cell Physiol 56:779–789

Kusajima M, Fujita M, Soudthedlath K, Nakamura H, Yoneyama K, Nomura T, Akiyama K, Maruyama-Nakashita A, Asami T, Nakashita H (2022) Strigolactones modulate salicylic acid-mediated disease resistance in Arabidopsis thaliana. Int J Mol Sci 23:5246

Lanceras JC, Pantuwan G, Jongdee B, Toojinda T (2004) Quantitative trait loci associated with drought tolerance at reproductive stage in rice. Plant Physiol 135:384–399

Lee HY, Byeon Y, Tan DX, Reiter RJ, Back K (2015) Arabidopsis serotonin N-acetyltransferase knockout mutant plants exhibit decreased melatonin and salicylic acid levels resulting in susceptibility to an avirulent pathogen. J Pineal Res 58:291–299

Lefevere H, Bauters L, Gheysen G (2020) Salicylic acid biosynthesis in plants. Front Plant Sci 11:338

Leslie CA, Romani RJ (1986) Salicylic acid: a new inhibitor of ethylene biosynthesis. Plant Cell Rep 5:144–146

Li Z, Ahammed GJ (2023) Salicylic acid and jasmonic acid in elevated CO2-induced plant defense response to pathogens. J Plant Physiol 286:154019

Liu J, Qiu G, Liu C, Li H, Chen X, Fu Q, Lin Y, Guo B (2022) Salicylic acid, a multifaceted hormone combats abiotic stresses in plants. Life 12:886

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

Lopez-Orenes A, Alba JM, Kant MR, Calderon AA, Ferrer MA (2020) OPDA and ABA accumulation in Pb-stressed Zygophyllum fabago can be primed by salicylic acid and coincides with organ-specific differences in accumulation of phenolics. Plant Physiol Biochem 154:612–621

Luo Y, Wei Y, Sun S, Wang J, Wang W, Han D, Shao H, Jia H, Fu Y (2019) Selenium modulates the level of auxin to alleviate the toxicity of cadmium in tobacco. Int J Mol Sci 20:3772

Martínez-Medina A, Roldán A, Albacete A, Pascual JA (2011) The interaction with arbuscular mycorrhizal fungi or Trichoderma harzianum alters the shoot hormonal profile in melon plants. Phytochemistry 72:223–229

Mathur P, Singh VP, Kapoor R (2018) Interactive effects of CO2 concentrations and Alternaria brassicae (Berk.) Sacc. infection on defense signalling in Brassica juncea (L.) Czern & Coss. Eur J Plant Pathol 151:413–425

Melotto M, Underwood W, Koczan J, Nomura K, He SY (2006) Plant stomata function in innate immunity against bacterial invasion. Cell 126:969–980

Mhamdi A, Noctor G (2016) High CO2 primes plant biotic stress defences through redox-linked pathways. Plant Physiol 172:929–942

Miao Y, Zentgraf U (2007) The antagonist function of Arabidopsis WRKY53 and ESR/ESP in leaf senescence is modulated by the jasmonic and salicylic acid equilibrium. Plant Cell 19:819–830

Miao Y, Laun T, Zimmermann P, Zentgraf U (2004) Targets of the WRKY53 transcription factor and its role during leaf senescence in Arabidopsis. Plant Mol Biol 55:853–867

Mishra AK, Baek K-H (2021) Salicylic acid biosynthesis and metabolism: a divergent pathway for plants and bacteria. Biomolecules 11:705

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

Munne-Bosch S, Penuelas J (2003) Photo- and antioxidative protection, and a role for salicylic acid during drought and recovery in field-grown Phillyrea angustifolia plants. Planta 217:758–766

Munoz-Espinoza VA, Lopez-Climent MF, Casaretto JA, Gomez-Cadenas A (2015) Water stress responses of tomato mutants impaired in hormone biosynthesis reveal abscisic acid, jasmonic acid and salicylic acid interactions. Front Plant Sci 6:997

Mur LAJ, Kenton P, Atzorn R, Miersch O, Wasternack C (2006) The outcomes of concentration-specific interactions between salicylate and jasmonate signaling include synergy, antagonism and oxidative stress leading to cell death. Plant Physiol 140:249–262

Navarro L, Bari R, Achard P, Lison P, Nemri A, Harberd NP, Jones JD (2008) DELLAs control plant immune responses by modulating the balance of jasmonic acid and salicylic acid signaling. Curr Biol 18:650–655

Nazar R, Umar S, Khan N, Sareer O (2015) Salicylic acid supplementation improves photosynthesis and growth in mustard through changes in proline accumulation and ethylene formation under drought stress. S Afr J Bot 98:84–94

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 162:569–574

Nolan TM, Vukasinovic N, Liu D, Russinova E, Yin Y (2020) Brassinosteroids: multidimensional regulators of plant growth, development, and stress responses. Plant Cell 32:295–318

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 46:1062–1072

Pál M, Szalai G, Janda T (2015) Speculation: polyamines are important in abiotic stress signaling. Plant Sci 237:16–23

Pedranzani H, Racagni G, Alemano S, Miersch O, Ramirez I, Pena-Cortes H, Taleisnik E, Machado-Domenech E, Abdala G (2003) Salt tolerant tomato plants show increased levels of jasmonic acid. Plant Growth Regul 41:149–158

Peng Y, Yang J, Li X, Zhang Y (2021) Salicylic acid: biosynthesis and signaling. Annu Rev Plant Biol 72:761–791

Pertry I, Vaclavıkova K, Depuydt S, Galuszka P, Spıchal L, Temmerman W, Stes E, Schmulling T, Kakimoto T, Montagu MCEV et al (2009) Identification of Rhodococcus fascians cytokinins and their modus operandi to reshape the plant. Proc Natl Acad Sci USA 106:929–934

Prodhan MY, Munemasa S, Nahar MNEN, Nakamura Y, Murata Y (2018) Guard cell salicylic acid signaling is integrated into abscisic acid signaling via the Ca2+/CPK-dependent pathway. Plant Physiol 178:441–450

Prodhan Y, Issak M, Munemasa S, Nakamura Y, Murata Y (2020) Salicylic acid receptor NPR1 is involved in guard cell chitosan signaling. Biosci Biotechnol Biochem 84:963–969

Qiao L, Zheng L, Sheng C, Zhao H, Jin H, Niu D (2020) Rice siR109944 suppresses plant immunity to sheath blight and impacts multiple agronomic traits by affecting auxin homeostasis. Plant J 102:948–964

Rafique N, Ilyas N, Aqeel M et al (2023) Interactive effects of melatonin and salicylic acid on Brassica napus under drought condition. Plant Soil. https://doi.org/10.1007/s11104-023-05942-7

Rao MV, Lee H-I, Davis KR (2002) Ozone-induced ethylene production is dependent on salicylic acid, and both salicylic acid and ethylene act in concert to regulate ozone-induced cell death. Plant J 32:447–456

Raskin I, Skubatz H, Tang W, Meeuse BJD (1990) Salicylic-acid levels in thermogenic and nonthermogenic plants. Ann Bot 66:369–373

Ribot C, Hirsch J, Balzergue S, Tharreau D, Notteghem JL, Lebrun MH, Morel JB (2008) Susceptibility of rice to the blast fungus, Magnaporthe grisea. J Plant Physiol 165:114–124

Rohde A, Morreel K, Ralph J, Goeminne G, Hostyn V et al (2004) Molecular phenotyping of the pal1 and pal2 mutants of Arabidopsis thaliana reveals far-reaching consequences on phenylpropanoid, amino acid, and carbohydrate metabolism. Plant Cell 16:2749–2771

Rossi FR, Gárriz A, Marina M, Pieckenstain FL (2021) Modulation of polyamine metabolism in Arabidopsis thaliana by salicylic acid. Physiol Plant 173:843–855

Sano H, Seo S, Koizumi N, Niki T, Iwamura H, Ohashi Y (1996) Regulation by cytokinins of endogenous levels of jasmonic and salicylic acids in mechanically wounded tobacco plants. Plant Cell Physiol 37:762–769

Sawada H, Shim IS, Usui K (2006) Induction of benzoic acid 2-hydroxylase and salicylic acid biosynthesis—modulation by salt stress in rice seedlings. Plant Sci 171:263–270

Shakirova FM, Bezrukova MV, Allagulova CR, Maslennikova DR, Lubyanova AR (2017) Wheat germ agglutinin and dehydrins as Aba-regulated components of sa-induced cadmium resistance in wheat plants. In: Khan NA, Iqbal N, Nazar R (eds) Salicylic acid: a multifaceted hormone. Springer, Singapore, pp 77–96

Silverman P, Seskar M, Kanter D, Schweizer P, Metraux JP, Raskin I (1995) Salicylic acid in rice (biosynthesis, conjugation, and possible role). Plant Physio 108:633–639

Singh A, Roychoudhury A (2023) Abscisic acid in plants under abiotic stress: crosstalk with major phytohormones. Plant Cell Rep 42:961–974

Singla J, Krattinger SG, Wrigley CW, Faubion J, Corke H, Seetharaman K (2016) Biotic stress resistance genes in wheat. Encyclopedia of food grains. Elsevier, Oxford, pp 388–392

Synkova H, Semoradova S, Burketova L (2004) High content of endogenous cytokinins stimulates activity of enzymes and proteins involved in stress response in Nicotiana tabacum. Plant Cell Tiss Org Cult 79:169–179

Székács A, Hegedüs G, Tóbiás I, Pogány M, Barna B (2000) Immunoassays for plant cytokinins as tools for the assessment of environmental stress and disease resistance. Anal Chim Acta 42:135–146

Tang Q, Zheng X-d, Guo J, Yu T (2022) Tomato SlPti5 plays a regulative role in the plant immune response against Botrytis cinerea through modulation of ROS system and hormone pathways. J Integr Agric 21:697–709

Tirani MM, Nasibi F, Kalantari KM (2013) Interaction of salicylic acid and ethylene and their effects on some physiological and biochemical parameter in canola plants (Brassica napus L.). Photosynthetica 51:411–418

Tiwari P, Indoliya Y, Chauhan AS, Singh P, Singh PK, Singh PC, Srivastava S, Pande V, Chakrabarty D (2020) Auxin-salicylic acid cross-talk ameliorates OsMYB-R1 mediated defense towards heavy metal, drought and fungal stress. J Hazard Mater 399:122811

Torun H, Novák O, Mikulík J, Strnad M, Ayaz FA (2022) The effects of exogenous salicylic acid on endogenous phytohormone status in Hordeum vulgare L. under salt stress. Plants 11:618

Tuna AL, Kaya C, Dikilitas M, Higgs D (2008) The combined effects of gibberellic acid and salinity on some antioxidant enzyme activities, plant growth parameters and nutritional status in maize plants. Environ Exp Bot 62:1–9

Vallad GE, Goodman RM (2004) Systemic acquired resistance and induced systemic resistance in conventional agriculture. Crop Sci 44:1920–1934

Walters DR, McRoberts N (2006) Plants and biotrophs: a pivotal role for cytokinins? Trends Plant Sci 11:581–586

Wang D, Pajerowska-Mukhtar K, Culler AH, Dong X (2007) Salicylic acid inhibits pathogen growth in plants through repression of the auxin signaling pathway. Curr Biol 17:1784–1790

Wang W, Wang X, Huang M, Cai J, Zhou Q, Dai T, Cao W, Jiang D (2018) Hydrogen peroxide and abscisic acid mediate salicylic acid-induced freezing tolerance in wheat. Front Plant Sci 9:1137

Xu Y, Wang Y, Xu J, Zhengxin L, Manzoor MA, Mao J, Zhang X, Liu R, Whiting MD, Jiu S, Zhang C (2023) Strigolactone and salicylic acid regulate the expression of multiple stress-related genes and enhance the drought resistance of cherry rootstocks. Sci Hort 313:111827

Yamaguchi S (2008) Gibberellin metabolism and its regulation. Annu Rev Plant Biol 59:225–251

Yang Y, Ahammed G, Wu C, Fan S, Zhou Y (2014) Crosstalk among Jasmonate, salicylate and ethylene signaling pathways in plant disease and immune responses. Curr Protein Pept Sci 16:450–461

Yang H, Chen X, Yang R, Cheng J, Chen Y, Joosten MHAJ, Du Y (2023) The potato StMKK5-StSIPK module enhances resistance to Phytophthora pathogens through activating the salicylic acid and ethylene signalling pathways. Mol Plant Pathol 24:399–412

Yasuda M, Ishikawa A, Jikumaru Y, Seki M, Umezawa T, Asami T, Maruyama-Nakashita A, Kudo T, Shinozaki K, Yoshida S, Nakashita H (2008) Antagonistic interaction between systemic acquired resistance and the abscisic acid-mediated abiotic stress response in Arabidopsis. Plant Cell 20:1678–1692

Yu Y, Gui Y, Li Z, Jiang C, Guo J, Niu D (2022) Induced systemic resistance for improving plant immunity by beneficial microbes. Plants 11:386

Zhang S, Li X, Sun Z, Shao S, Hu L, Ye M, Zhou Y, Xia X, Yu J, Shi K (2015) Antagonism between phytohormone signalling underlies the variation in disease susceptibility of tomato plants under elevated CO2. J Exp Bot 66:1951–1963

Zhang S, Zheng X, Reiter RJ, Feng S, Wang Y, Liu S, Jin L, Li Z, Datla R, Ren M (2017) Melatonin attenuates potato late blight by disrupting cell growth, stress tolerance, fungicide susceptibility and homeostasis of gene expression in Phytophthora infestans. Front Plant Sci 8:1993

Zhang Y, Song RF, Yuan HM, Li TT, Wang LF, Lu KK, Guo JX, Liu WC (2021) Overexpressing the N-terminus of CATALASE2 enhances plant jasmonic acid biosynthesis and resistance to necrotrophic pathogen Botrytis cinerea B05.10. Mol Plant Pathol 22:1226–1238

Zhang Y, Fu X, Feng Y, Zhang X, Bi H, Ai X (2022) Abscisic acid mediates salicylic acid induced chilling tolerance of grafted cucumber by activating H2O2 biosynthesis and accumulation. Int J Mol Sci 23:16057

Zhao P, Lu GH, Yang YH (2017) Salicylic acid signaling and its role in responses to stresses in plants. Mech Plant Horm Signal under Stress 39:413–444

Zheng Y, Wang X, Cui X, Wang K, Wang Y, He Y (2023) Phytohormones regulate the abiotic stress: an overview of physiological, biochemical, and molecular responses in horticultural crops. Front Plant Sci 13:1095363