Skip to main content

Advertisement

SpringerLink
Log in

Phytohormones enhanced drought tolerance in plants: a coping strategy

  • Review Article
  • Published:
Environmental Science and Pollution Research Aims and scope Submit manuscript

Abstract

Drought stress is a severe environmental constraint among the emerging problems. Plants are highly vulnerable to drought stress and a severe decrease in yield was recorded in the last few decades. So, it is highly desirable to understand the mechanism of drought tolerance in plants and consequently enhance the tolerance against drought stress. Phytohormones are known to play vital roles in regulating various phenomenons in plants to acclimatize to varying drought environment. Abscisic acid (ABA) is considered the main hormone which intensifies drought tolerance in plants through various morpho-physiological and molecular processes including stomata regulation, root development, and initiation of ABA-dependent pathway. In addition, jasmonic acid (JA), salicylic acid (SA) ethylene (ET), auxins (IAA), gibberellins (GAs), cytokinins (CKs), and brassinosteroids (BRs) are also very important phytohormones to congregate the challenges of drought stress. However, these hormones are usually cross talk with each other to increase the survival of plants in drought conditions. On the other hand, the transgenic approach is currently the most accepted technique to engineer the genes responsible for the synthesis of phytohormones in drought stress response. Our present review highlights the regulatory circuits of phytohormones in drought tolerance mechanism.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Abe H, Urao T, Ito T, Seki M, Shinozaki K, Yamaguchi-Shinozaki K (2003) Arabidopsis AtMYC2 (bHLH) and AtMYB2 (MYB) function as transcriptional activators in abscisic acid signalling. Plant Cell 15:63–78

    CAS  Google Scholar 

  • Agarwal PK, Shukla PS, Gupta K, Jha B (2013) Bioengineering for salinity tolerance in plants: state of the art. Mol Biotechnol 54:102–123

    CAS  Google Scholar 

  • Ai L, Li ZH, Xie ZX, Tian XL, Eneji AE, Duan LS (2008) Coronatine alleviates polyethylene glycol-induced water stress in two rice (Oryza sativa L.) cultivars. J Agron Crop Sci 194:360–368

    CAS  Google Scholar 

  • Akıncı Ş, Lösel DM (2006) Plant water-stress response mechanisms. Intech publishers, pp 15–42

  • Allen GJ, Murata Y, Chu SP, Nafisi M, Schroeder JI (2002) Hypersensitivity of abscisic acid-induced cytosolic calcium increases in the Arabidopsis farnesyltransferase mutant era1-2. Plant Cell 14:1649–1662

    CAS  Google Scholar 

  • Aroca R (2012) Plant responses to drought stress. In: From Morphological to Molecular Features. Springer-Verlag GmbH, Berlin Heidelberg

    Google Scholar 

  • Arraes FBM, Beneventi MA, de Sa MEL et al (2015) Implications of ethylene biosynthesis and signalling in soybean drought stress tolerance. BMC Plant Biol 15:213

    Google Scholar 

  • Baloch MJ, Khan NU, Jatoi WA, Hassan G, Khakhwani AA, Soomro ZA, Weesar NF (2011) Drought tolerance studies through WSSI and stomata in upland cotton. Pak J Bot 43:2479–2484

    Google Scholar 

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

    CAS  Google Scholar 

  • Bandurska H, Stroinski A, Kubis J (2003) The effect of jasmonic acid on the accumulation of ABA, proline and spermidine and its influence on membrane injury under water deficit in two barley genotypes. Acta Physiol Plant 25:279–285

    CAS  Google Scholar 

  • Bandurska H, Niedziela J, Chadzinikolau T (2013) Separate and combined responses to water deficit and UV-B radiation. Plant Sci 213:98–105

    CAS  Google Scholar 

  • Basu S, Ramegowda V, Kumar A, Pereira A (2016) Plant adaptation to drought stress. F1000Res 5:F1000 faculty Rev-1554

    Google Scholar 

  • 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

    CAS  Google Scholar 

  • Boudsocq M, Lauriere C (2005) Osmotic signalling in plants: multiple pathways mediated by emerging kinase families. Plant Physiol 138:1185–1194

    CAS  Google Scholar 

  • Brodribb TJ, McAdam SA (2017) Evolution of the stomatal regulation of plant water content. Plant Physiol 174:639–649

    CAS  Google Scholar 

  • Burstenbinder K, Rzewuski G, Wirtz M, Hell R, Sauter M (2007) The role of methionine recycling for ethylene synthesis in Arabidopsis. Plant J 49:238–249

    Google Scholar 

  • Chai C, Subudhi PK (2016) Comprehensive analysis and expression profiling of the OsLAX and OsABCB auxin transporter gene families in Rice (Oryza sativa) under phytohormone stimuli and abiotic stresses. Front Plant Sci 7:593

    Google Scholar 

  • Chastain DR, Snider JL, Collins GD, Perry CD, Whitaker J, Byrd SA (2014) Water deficit in field-grown Gossypiumhirsutum primarily limits net photosynthesis by decreasing stomata conductance, increasing photorespiration, and increasing the ratio of dark respiration to gross photosynthesis. J Plant Physiol 171:1576–1585

    CAS  Google Scholar 

  • Chater CC, Oliver J, Casson S, Gray JE (2014) Putting the brakes on: abscisic acid as a central environmental regulator of stomatal development. New Phytol 202:376–391

    CAS  Google Scholar 

  • Chaves MM, Maroco JP, Pereira JS (2003) Understanding plant responses to drought-from genes to the whole plant. Funct Plant Biol 30:239–264

    CAS  Google Scholar 

  • Chaves MM, Flexas J, Pinheiro C (2009) Photosynthesis under drought and salt stress: regulation mechanisms from whole plant to cell. Ann Bot 103:551–560

    CAS  Google Scholar 

  • Chen Z, Zheng Z, Huang J, Lai Z, Fan B (2009) Biosynthesis of salicylic acid in plants. Plant Signal Behav 4:493–496

    CAS  Google Scholar 

  • Chen J, Nolan TM, Ye H, Zhang M, Tong H, Xin P, Chu J, Chu C, Li Z, Yin Y (2017) Arabidopsis WRKY46, WRKY54, and WRKY70 transcription factors are involved in brassinosteroid-regulated plant growth and drought responses. Plant Cell 29:1425–1439

    CAS  Google Scholar 

  • Chini A, Grant JJ, Seki M, Shinozaki K, Loake GJ (2004) Drought tolerance established by enhanced expression of the CC-NBS-LRR gene, ADR1, requires salicylic acid, EDS1 and ABI1. Plant J 38:810–822

    CAS  Google Scholar 

  • Chini A, Fonseca S, Fernández G, Adie B, Chico JM, Lorenzo O, García-Casado G, López-Vidriero I, Lozano FM, Ponce MR, Micol JL, Solano R (2007) The JAZ family of repressors is the missing link in Jasmonate signalling. Nature 448:666–671

    CAS  Google Scholar 

  • Colebrook EH, Thomas SG, Phillips AL, Hedden P (2014) The role of gibberellin signalling in plant responses to abiotic stress. J Exp Biol 217:67–75

    CAS  Google Scholar 

  • Comas LH, Becker SR, Cruz VMV, Byrne PF, Dierig DA (2013) Root traits contributing to plant productivity under drought. Front Plant Sci 4:1–16

    Google Scholar 

  • Cracker LEA, Abeles FB (1969) Abscission: role of abscisic acid. Plant Physiol 44:1144–1149

    CAS  Google Scholar 

  • Danquah A, Zelicourt AD, Colcombet J, Hirt H (2014) The role of ABA and MAPK signalling pathways in plant abiotic. Biotechnol Adv 32:40–52

    CAS  Google Scholar 

  • Daszkowska-Golec A, Chorazy E, Maluszynski M, Szarejko I (2013) Towards the identification of new genes involved in ABA-dependent abiotic stresses using Arabidopsis suppressor mutants of abh1 hypersensitivity to ABA during seed germination. Int J Mol Sci 14:13403–13432

    Google Scholar 

  • Davis RF, Earl HJ, Timper P (2014) Effect of simultaneous water deficit stress and meloidogyne incognita infection on cotton yield and fiber quality. J Nematol 46:108–118

    CAS  Google Scholar 

  • de Ollas C, Dodd IC (2016) Physiological impacts of ABA–JA interactions under water-limitation. Plant Mol Biol 91:641–650

    Google Scholar 

  • de Ollas C, Hernando B, Arbona V, Gómez-Cadenas A (2013) Jasmonic acid transient accumulation is needed for abscisic acid increase in citrus roots under drought stress conditions. Physiol Plant 147:296–306

    Google Scholar 

  • de Ollas C, Arbona V, GóMez-Cadenas A (2015) Jasmonoyl isoleucine accumulation is needed for abscisic acid build-up in roots of Arabidopsis under water stress conditions. Plant Cell Environ 38:2157–2170

    Google Scholar 

  • Deeba F, Pandey AK, Ranjan S, Mishra A, Singh R, Sharma YK, Shirke PA, Pandey V (2012) Physiological and proteomic responses of cotton (Gossypium herbaceum L.) to drought stress. Plant Physiol Biochem 53:6–18

    CAS  Google Scholar 

  • Delker C, Stenzel I, Hause B, Miersch O, Feussner I, Wasternack C (2006) Jasmonate biosynthesis in Arabidopsis thaliana—enzymes, products, regulation. Plant Biol 8:297–306

    CAS  Google Scholar 

  • Dolferus R, Ji X, Richards RA (2011) Abiotic stress and control of grain number in cereals. Plant Sci 181:331–341

    CAS  Google Scholar 

  • Dong T, Park Y, Hwang I (2015) Abscisic acid: biosynthesis, inactivation, homoeostasis and signalling. Essays Biochem 58:29–48

    Google Scholar 

  • Doussan C, Pierret A, Garrigues E, Pagès L (2006) Water uptake by plant roots: II—modelling of water transfer in the soil root-system with explicit account of flow within the root system—comparison with experiments. Plant Soil 283:99–117

    CAS  Google Scholar 

  • Fahad S, Hussain S, Matloob A, Khan FA, Khaliq A, Saud S, Hassan S, Shan D, Khan F, Ullah N, Faiq M, Khan MR, Tareen AK, Khan A, Ullah A, Ullah N, Huang J (2014) Phytohormones and plant responses to salinity stress: a review. Plant Growth Regul 75:391–404

    Google Scholar 

  • Fahad S, Hussain S, Saud S, Tanveer M, Bajwa AA, Hassan S, Shah AN, Ullah A, Wu C, Khan FA, Shah F, Ullah S, Chen Y, Huang J (2015) A biochar application protects rice pollen from high-temperature stress. Plant Physiol Biochem 96:281–287

    CAS  Google Scholar 

  • Fahad S, Hussain S, Saud S, Hassan S, Chauhan BS, Khan F, Ihsan MZ, Ullah A, Wu C, Bajwa AA, Alharby H, Amanullah, Nasim W, Shahzad B, Tanveer M, Huang J (2016) Responses of rapid viscoanalyzer profile and other rice grain qualities to exogenously applied plant growth regulators under high day and high night temperatures. PLoS One 11(7):e0159590

    Google Scholar 

  • Fang L, Su L, Sun X, Li X, Sun M, Karungo SK, Fang S, Chu J, Li S, Xin H (2016) Expression of Vitis amurensis NAC26 in Arabidopsis enhances drought tolerance by modulating jasmonic acid synthesis. J Exp Bot 67:2829–2845

    CAS  Google Scholar 

  • Farooq M, Basra SMA, Wahid A, Ahmad N, Saleem BA (2009) Improving the drought tolerance in rice (Oryza sativa L.) by exogenous application of salicylic acid. J Agron Crop Sci 195:237–246

    CAS  Google Scholar 

  • Feng Y, Yin Y, Fei S (2015) Down-regulation of BdBRI1, a putative brassinosteroid receptor gene produces a dwarf phenotype with enhanced drought tolerance in Brachypodium distachyon. Plant Sci 234:163–173

    CAS  Google Scholar 

  • Flexas J, Ribas-Carbó M, Bota J, Galmés J, Henkle M, Martínez-Cañellas S, Medrano H (2006) Decreased Rubisco activity during water stress is not induced by decreased relative water content but related to conditions of low stomata conductance and chloroplast CO2 concentration. New Phytol 172:73–82

    CAS  Google Scholar 

  • Flexas J, Barón M, Bota J, Ducruet JM, Gallé A, Galmés J, Jiménez M, Pou A, Ribas-Carbó M, Sajnani C, Tomàs M, Medrano H (2009) Photosynthesis limitations during water stress acclimation and recovery in the drought-adapted Vitis hybrid Richter-110 (V. berlandierix, V. rupestris). J Exp Bot 60:2361–2377

    CAS  Google Scholar 

  • Fujii H, Zhu JK (2009) Arabidopsis mutant deficient in 3 abscisic acid-activated protein kinases reveals critical roles in growth, reproduction, and stress. Proc Natl Acad Sci U S A 106:8380–8385

    CAS  Google Scholar 

  • Gall HL, Philippe F, Domon JM, Gillet F, Pelloux J, Rayon C (2015) Cell wall metabolism in response to abiotic stress. Plants 4:112–166

    Google Scholar 

  • Gao Z, Schaller GE (2009) The role of receptor interactions in regulating ethylene signal transduction. Plant Signal Behav 4:1152–1153

    Google Scholar 

  • Geiger D, Scherzer S, Mumm P, Marten I, Ache P, Matschi S, Liese A, Wellmann C, al-Rasheid KAS, Grill E, Romeis T, Hedrich R (2010) Guard cell anion channel SLAC1 is regulated by CDPK protein kinases with distinct Ca2+ affinities. Proc Natl Acad Sci U S A 107:8023–8028

    CAS  Google Scholar 

  • Gray SB, Brady SM (2016) Plant developmental responses to climate change. Dev Biol 419:64–77

    CAS  Google Scholar 

  • Ha S, Vankoa R, Yamaguchi-Shinozaki K, Shinozaki K, Tran LP (2012) Cytokinins: metabolism and function in plant adaptation to environmental stresses. Trends Plant Sci 17:172–179

    CAS  Google Scholar 

  • Harberd NP, Belfield E, Yasumura Y (2009) The angiosperm gibberellinGID1-DELLA growth regulatory mechanism: how an ‘inhibitor of an inhibitor’ enables flexible response to fluctuating environments. Plant Cell 21:1328–1339

    CAS  Google Scholar 

  • Hoffmann M, Hentrich M, Pollmann S (2011) Auxin-oxylipin crosstalk: relationship of antagonists. J Integr Plant Biol 53:429–445

    CAS  Google Scholar 

  • Hrabak EM, Chan CWM, Gribskov M, Harper JF, Choi JH, Halford N, Kudla J, Luan S, Nimmo HG, Sussman MR, Thomas M, Walker-Simmons K, Zhu JK, Harmon AC (2003) The Arabidopsis CDPK-SnRK superfamily of protein kinases. Plant Physiol 132:666–680

    CAS  Google Scholar 

  • Hugouvieux V, Murata Y, Young JJ, Kwak JM, Mackesy DZ, Schroeder JI (2002) Localization, ion channel regulation, and genetic interactions during abscisic acid signalling of the nuclear mRNA cap-binding protein, ABH1. Plant Physiol 130:1276–1287

    CAS  Google Scholar 

  • Hunter LJ, Westwood JH, Heath G et al (2013) Regulation of RNA-dependent RNA polymerase1 and isochorismate synthase gene expression in Arabidopsis. PLoS One 8:e66530

    CAS  Google Scholar 

  • Im Kim J, Baek D, Park HC et al (2013) Overexpression of Arabidopsis YUCCA6 in potato results in high-auxin developmental phenotypes and enhanced resistance to water deficit. Mol Plant 6:337–349

    Google Scholar 

  • Jiang H, Li H, Bu Q, Li C (2009) The RHA2a-interacting proteins ANAC019 and ANAC055 may play a dual role in regulating ABA response and jasmonate response. Plant Signal Behav 4:464–466

    CAS  Google Scholar 

  • Jones B, Gunneras SA, Petersson SV, Tarkowski P, Graham N, May S, Dolezal K, Sandberg G, Ljung K (2010) Cytokinin regulation of auxin synthesis in Arabidopsis involves a homeostatic feedback loop regulated via auxin and cytokinin signal transduction. Plant Cell 22:2956–2969

    CAS  Google Scholar 

  • Jumali SS, Said IM, Ismail I, Zainal Z (2011) Genes induced by high concentration of salicylic acid in'Mitragyna speciosa'. Aust J Crop Sci 5:296

    CAS  Google Scholar 

  • Jung H, Lee DK, Do Choi Y, Kim JK (2015) OsIAA6, a member of the rice Aux/IAA gene family, is involved in drought tolerance and tiller outgrowth. Plant Sci 236:304–312

    CAS  Google Scholar 

  • Kagale S, Divi UK, Krochko JE, Keller WA, Krishna P (2007) Brassinosteroid confers tolerance in Arabidopsis thaliana and Brassica napus to a range of abiotic stresses. Planta 225:353–364

    CAS  Google Scholar 

  • Kang J, Hwang JU, Lee M, Kim YY, Assmann SM, Martinoia E, Lee Y (2010) PDR-type ABC transporter mediates cellular uptake of the phytohormone abscisic acid. Proc Natl Acad Sci U S A 107:2355–2360

    CAS  Google Scholar 

  • 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 11:6066–6079

    CAS  Google Scholar 

  • Kang GZ, Li GZ, Liu GQ, Xu W, Peng XQ, Wang CY, Zhu YJ, Guo TC (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 (2013) Auxin and the integration of environmental signals into plant root development. Ann Bot 112:1655–1665

    Google Scholar 

  • Kazan K (2015) Diverse roles of jasmonates and ethylene in abiotic stress tolerance. Trends Plant Sci 20:219–229

    CAS  Google Scholar 

  • Kazan K, Manners JM (2011) JAZ repressors and the orchestration of phytohormone crosstalk. Trends Plant Sci 17:22–31

    Google Scholar 

  • Ke Q, Wang Z, Ji CY, Jeong JC, Lee HS, Li H, Xu B, Deng X, Kwak SS (2015) Transgenic poplar expressing Arabidopsis YUCCA6 exhibits auxin-overproduction phenotypes and increased tolerance to abiotic stress. Plant Physiol Biochem 94:19–27

    CAS  Google Scholar 

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

    Google Scholar 

  • Kieber JJ, Schaller GE (2014) Cytokinins. Arabidopsis Book 12:e0168

    Google Scholar 

  • Klingler JP, Batelli G, Zhu JK (2010) ABA receptors: the START of a new paradigm in phytohormone signalling. J Exp Bot 61:3199–3210

    CAS  Google Scholar 

  • Kumar DM, Pandey CL, Goswami JS (2001) Effect of growth regulators on photosynthesis, transpiration and related parameters in water stressed cotton. Biol Plant 44:475–478

    CAS  Google Scholar 

  • Kuromori T, Miyaji T, Yabuuchi H, Shimizu H, Sugimoto E, Kamiya A, Moriyama Y, Shinozaki K (2010) ABC transporter AtABCG25 is involved in abscisic acid transport and responses. Proc Natl Acad Sci U S A 107:2361–2366

    CAS  Google Scholar 

  • Lawlor DW (2002) Limitation to photosynthesis in water-stressed leaves: stomata vs. metabolism and the role of ATP. Ann Bot 89:871–885

    CAS  Google Scholar 

  • Lee SC, Kim SH, An SH, Yi SY, Hwang BK (2006) Identification and functional expression of the pepper pathogen-induced gene, CAPIP2, involved in disease resistance and drought and salt stress tolerance. Plant Mol Biol 62:151–164

    CAS  Google Scholar 

  • Lee J, Nam J, Park HC, Na G, Miura K, Jin JB, Yoo CY, Baek D, Kim DH, Jeong JC, Kim D, Lee SY, Salt DE, Mengiste T, Gong Q, Ma S, Bohnert HJ, Kwak SS, Bressan RA, Hasegawa PM, Yun DJ (2007) Salicylic acid-mediated innate immunity in Arabidopsis is regulated by SIZ1 SUMO E3 ligase. Plant J 49:79–90

    CAS  Google Scholar 

  • Li J, Sima W, Ouyang B, Wang T, Ziaf K, Luo Z, Liu L, Li H, Chen M, Huang Y, Feng Y, Hao Y, Ye Z (2012a) Tomato SlDREB gene restricts leaf expansion and internode elongation by downregulating key genes for gibberellin biosynthesis. J Exp Bot 63:6407–6420

    CAS  Google Scholar 

  • Li QF, Wang C, Jiang L, Li S, Sun SS, He JX (2012b) An interaction between BZR1 and DELLAs mediates direct signalling crosstalk between Brassinosteroids and gibberellins in Arabidopsis. Sci Signal 5:ra72

    Google Scholar 

  • Li Y, Zhang J, Zhang J, Hao L, Hua J, Duan L, Zhang M, Li Z (2013) Expression of an Arabidopsis molybdenum cofactor sulphurase gene in soybean enhances drought tolerance and increases yield under field conditions. Plant Biotechnol J 11:747–758

    CAS  Google Scholar 

  • Li W, Herrera-Estrella L, Tran LSP (2016) The Yin–Yang of cytokinin homeostasis and drought acclimation/adaptation. Trends Plant Sci 21:548–550

    CAS  Google Scholar 

  • Liang C, Meng Z, Meng Z, Malik W, Yan R, Lwin KM, Lin F, Wang Y, Sun G, Zhou T, Zhu T, Li J, Jin S, Guo S, Zhang R (2016) GhABF2, a bZIP transcription factor, confers drought and salinity tolerance in cotton (Gossypium hirsutum L.). Sci Rep 6:35040

    CAS  Google Scholar 

  • Lim CW, Baek W, Jung J, Kim JH, Lee SC (2015) Function of ABA in stomatal defense against biotic and drought stresses. Int J Mol Sci 16:15251–15270

    CAS  Google Scholar 

  • Liu C, Zhang T (2017) Expansion and stress responses of the AP2/EREBP superfamily in cotton. BMC Genomics 18:118

    Google Scholar 

  • Liu P, Xu ZS, Pan-Pan L, Hu D, Chen M, Li LC, Ma YZ (2013) A wheat PI4K gene whose product possesses threonine autophophorylation activity confers tolerance to drought and salt in Arabidopsis. J Exp Bot 64:2915–2927

    CAS  Google Scholar 

  • Liu G, Li X, Jin S, Liu X, Zhu L, Nie Y, Zhang X (2014) Overexpression of rice NAC gene SNAC1 improves drought and salt tolerance by enhancing root development and reducing transpiration rate in transgenic cotton. PLoS One 9:e86895

    Google Scholar 

  • Lo S, Ho TD, Liu Y et al (2017) Ectopic expression of specific GA2 oxidase mutants promotes yield and stress tolerance in rice. Plant Biotechnol J 15:850–864

    CAS  Google Scholar 

  • Lubovská Z, Dobrá J, Štorchová H, Wilhelmová N, Vanková R (2014) Cytokinin oxidase/dehydrogenase overexpression modifies antioxidant defense against heat, drought and their combination in Nicotiana tabacum plants. J Plant Physiol 171:1625–1633

    Google Scholar 

  • Mahajan S, Tuteja N (2005) Cold, salinity and drought stresses: an overview. Arch Biochem Biophys 444:139–158

    CAS  Google Scholar 

  • Manavalan LP, Guttikonda SK, Phan Tran LS, Nguyen HT (2009) Physiological and molecular approaches to improve drought resistance in soybean. Plant Cell Physiol 50:1260–1276

    CAS  Google Scholar 

  • Marques da Silva J, Arrabaca MC (2004) Photosynthesis in the water-stressed C grass Setariasphacelata is mainly limited by stomata with both rapidly and slowly imposed water deficits. Physiol Plant 121:409–420

    Google Scholar 

  • McWilliams D (2003) Drought strategies for cotton, cooperative extension service circular 582. College of Agriculture and Home Economics, New Mexico State University, USA

    Google Scholar 

  • Mehrotra R, Bhalothia P, Bansal P, Basantani MK, Bharti V, Mehrotra S (2014) Abscisic acid and abiotic stress tolerance—different tiers of regulation. J Plant Physiol 171:486–496

    CAS  Google Scholar 

  • Misra BB, Acharya BR, Granot D, Assmann SM, Chen S (2015) The guard cell metabolome: functions in stomatal movement and global food security. Front Plant Sci 6:334

    Google Scholar 

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

    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 73:91–104

    CAS  Google Scholar 

  • Mo Y, Wang Y, Yang R et al (2016) Regulation of plant growth, photosynthesis, antioxidation and osmosis by an arbuscular mycorrhizal fungus in watermelon seedlings under well-watered and drought conditions. Front Plant Sci 7:644

    Google Scholar 

  • Montillet JL, Leonhardt N, Mondy S, Tranchimand S, Rumeau D, Boudsocq M, Garcia AV, Douki T, Bigeard J, Laurière C, Chevalier A, Castresana C, Hirt H (2013) An abscisic acid-independent oxylipin pathway controls stomatal closure and immune defense in Arabidopsis. PLoS Biol 11:e1001513

    CAS  Google Scholar 

  • Mori IC, Murata Y, Yang Y et al (2006) CDPKs CPK6 and CPK3 function in ABA regulation of guard cell S-type anion- and Ca2+ -permeable channels and stomatal closure. PLoS Biol 4:1749–1762

    CAS  Google Scholar 

  • Munemasa S, Oda K, Watanabe-Sugimoto M, Nakamura Y, Shimoishi Y, Murata Y (2007) The coronatine-insensitive 1 mutation reveals the hormonal signalling interaction between abscisic acid and methyl jasmonate in Arabidopsis guard cells. Specific impairment of ion channel activation and second messenger production. Plant Physiol 143:1398–1407

    CAS  Google Scholar 

  • Munemasa S, Mori IC, Murata Y (2011) Methyl jasmonate signaling and signal crosstalk between methyl jasmonate and abscisic acid in guard cells. Plant Signal Behav 6:939–941

    CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • Nafie E, Hathout T, Mokadem ASA (2011) Jasmonic acid elicits oxidative defense and detoxification systems in Cucumis melo L. cells. Braz J Plant Physiol 23:161–174

    CAS  Google Scholar 

  • Nazareno AL, Hernandez BS (2017) A mathematical model of the interaction of abscisic acid, ethylene and methyl jasmonate on stomatal closure in plants. PLoS One 12:e0171065

    Google Scholar 

  • Negi J, Matsuda O, Nagasawa T, Oba Y, Takahashi H, Kawai-Yamada M, Uchimiya H, Hashimoto M, Iba K (2008) CO2 regulator SLAC1 and its homologues are essential for anion homeostasis in plant cells. Nature 452:483–486

    CAS  Google Scholar 

  • Nir I, Moshelion M, Weiss D (2014) The Arabidopsis GIBBERELLIN METHYL TRANSFERASE 1 suppresses gibberellin activity, reduces whole-plant transpiration and promotes drought tolerance in transgenic tomato. Plant Cell Environ 37:113–123

    CAS  Google Scholar 

  • Nishiyama R, Watanabe Y, Fujita Y, le DT, Kojima M, Werner T, Vankova R, Yamaguchi-Shinozaki K, Shinozaki K, Kakimoto T, Sakakibara H, Schmülling T, Tran LSP (2011) Analysis of cytokinin mutants and regulation of cytokinin metabolic genes reveals important regulatory roles of cytokinins in drought, salt and abscisic acid responses, and abscisic acid biosynthesis. Plant Cell 23:2169–2183

    CAS  Google Scholar 

  • Nishiyama R, Watanabe Y, Leyva-Gonzalez MA, van Ha C, Fujita Y, Tanaka M, Seki M, Yamaguchi-Shinozaki K, Shinozaki K, Herrera-Estrella L, Tran LSP (2013) Arabidopsis AHP2, AHP3, and AHP5 histidine phosphotransfer proteins function as redundant negative regulators of drought stress response. Proc Natl Acad Sci U S A 110:4840–4845

    CAS  Google Scholar 

  • Northey JG, Liang S, Jamshed M, Deb S, Foo E, Reid JB, McCourt P, Samuel MA (2016) Farnesylation mediates brassinosteroid biosynthesis to regulate abscisic acid responses. Nat Plant 2:16114–16114

    CAS  Google Scholar 

  • Ohkuma K, Lyon JL, Addicott FT, Smith OE (1963) Abscisin II, an abscission-accelerating substance from young cotton fruit. Science 142:1592–1593

    CAS  Google Scholar 

  • Pandey S, Zhang W, Assmann SM (2007) Roles of ion channels and transporters in guard cell signal transduction. FEBS Lett 581:2325–2336

    CAS  Google Scholar 

  • Peleg Z, Blumwald E (2011) Hormone balance and abiotic stress tolerance in crop plants. Curr Opin Plant Biol 14:290–295

    CAS  Google Scholar 

  • Riemann M, Dhakarey R, Hazman M, Miro B, Kohli A, Nick P (2015) Exploring Jasmonates in the hormonal network of drought and salinity responses. Front Plant Sci 6:1077

    Google Scholar 

  • Rivero RM, Kojima M, Gipstein A, Sakakibara H, Mittler R, Gipstein S, Blumwald E (2007) Delayed leaf senescence induces extreme drought tolerance in a flowering plant. Proc Natl Acad Sci U S A 104:19631–19636

    CAS  Google Scholar 

  • Rocher F, Chollet JF, Legros S, Jousse C, Lemoine R, Faucher M, Bush DR, Bonnemain JL (2009) Salicylic acid transport in Ricinus communis involves a pH-dependent carrier system in addition to diffusion. Plant Physiol 150:2081–2091

    CAS  Google Scholar 

  • Rowe JH, Topping JF, Liu J, Lindsey K (2016) Abscisic acid regulates root growth under osmotic stress conditions via an interacting hormonal network with cytokinin, ethylene and auxin. New Phytol 211:225–239

    CAS  Google Scholar 

  • Sah SK, Reddy KR, Li J (2016) Abscisic acid and abiotic stress tolerance in crop plants. Front Plant Sci 7:571

    Google Scholar 

  • Sahni S, Prasad BD, Liu Q, Grbic V, Sharpe A, Singh SP, Krishna P (2016) Overexpression of the brassinosteroid biosynthetic gene DWF4 in Brassica napus simultaneously increases seed yield and stress tolerance. Sci Rep 6:28298

    CAS  Google Scholar 

  • Sairam RK (1994) Effects of homobrassinolide application on plant metabolism and grain yield under irrigated and moisture-stress conditions of two wheat varieties. Plant Growth Regul 14:173–181

    CAS  Google Scholar 

  • Sánchez-Romera B, Ruiz-Lozano JM, Li G, Luu DT, Martínez-Ballesta MC, Carvajal M (2014) Enhancement of root hydraulic conductivity by methyl jasmonate and the role of calcium and abscisic acid in this process. Plant Cell Environ 37:995–1008

    Google Scholar 

  • Santino A, Taurino M, De Domenico S, Bonsegna S, Poltronieri P, Pastor V, Flors V (2013) Jasmonate signalling in plant development and defense response to multiple (a) biotic stresses. Plant Cell Rep 32:1085–1098

    CAS  Google Scholar 

  • Savchenko T, Kolla VK, Wang CQ et al (2014) Functional convergence of oxylipin and abscisic acid pathways controls stomatal closure in response to drought. Plant Physiol 164:1151–1160

    CAS  Google Scholar 

  • Scarpeci TE, Frea VS, Zanor MI, Valle EM (2016) Overexpression of AtERF019 delays plant growth and senescence, and improves drought tolerance in Arabidopsis. J Exp Bot 68:673–685

    Google Scholar 

  • Schulz P, Herde M, Romeis T (2013) Calcium-dependent protein kinases: hubs in plant stress signalling and development. Plant Physiol 163:523–530

    CAS  Google Scholar 

  • Schweighofer A, Hirt H, Meskiene I (2004) Plant PP2C phosphatases: emerging functions in stress signalling. Trends Plant Sci 9:236–243

    CAS  Google Scholar 

  • Seo M, Koshiba T (2002) Complex regulation of ABA biosynthesis in plants. Trends Plant Sci 7:41–48

    CAS  Google Scholar 

  • Seo M, Koshiba T (2011) Transport of ABA from the site of biosynthesis to the site of action. J Plant Res 124:501–507

    CAS  Google Scholar 

  • Seo PJ, Park CM (2010) MYB96-mediated abscisic acid signals induce pathogen resistance response by promoting salicylic acid biosynthesis in Arabidopsis. New Phytol 186:471–483

    CAS  Google Scholar 

  • Seo PJ, Xiang F, Qiao M, Park JY, Lee YN, Kim SG, Lee YH, Park WJ, Park CM (2009) The MYB96 transcription factor mediates abscisic acid signalling during drought stress response in Arabidopsis. Plant Physiol 151:275–289

    CAS  Google Scholar 

  • Shahnejat-Bushehri S, Tarkowska D, Sakuraba Y, Balazadeh S (2016) Arabidopsis NAC transcription factor JUB1 regulates GA/BR metabolism and signalling. Nat Plant 2:16013

    CAS  Google Scholar 

  • Shakeel S, Gao Z, Amir M, Chen YF, Rai MI, Haq NU, Schaller GE (2015) Ethylene regulates levels of ethylene-receptor/CTR1 signalling complexes in Arabidopsis thaliana. J Biol Chem 26:jbc-M115

    Google Scholar 

  • Shan C, Zhou Y, Liu M (2015) Nitric oxide participates in the regulation of the ascorbate-glutathione cycle by exogenous jasmonic acid in the leaves of wheat seedlings under drought stress. Protoplasma 252:1397–1405

    CAS  Google Scholar 

  • 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 2012:217037

    Google Scholar 

  • Sharp RE, Wu Y, Voetberg GS, Saab IN, LeNoble ME (1994) Confirmation that abscisic acid accumulation is required for maize primary root elongation at low water potentials. J Exp Bot 45:1743–1751

    CAS  Google Scholar 

  • Sharp RE, Poroyko V, Hejlek LG, Spollen WG, Springer GK, Bohnert HJ, Nguyen HT (2004) Root growth maintenance during water deficits: physiology to functional genomics. J Exp Bot 55:2343–2351

    CAS  Google Scholar 

  • Shinozaki K, Yamaguchi-Shinozaki K (2000) Molecular responses to dehydration and low temperature: differences and cross-talk between two stress signalling pathways. Curr Opin Plant Biol 3:217–223

    CAS  Google Scholar 

  • Singh VP, Prasad SM, Munné-Bosch S, Müller M (2017a) Phytohormones and the regulation of stress tolerance in plants: current status and future directions. Front Plant Sci 8:1871

    Google Scholar 

  • Singh R, Parihar P, Singh S, Mishra RK, Singh VP, Prasad SM (2017b) Reactive oxygen species signaling and stomatal movement: current updates and future perspectives. Redox Biol 11:213–218

    CAS  Google Scholar 

  • Stepanova AN, Alonso JM (2009) Ethylene signalling and response: where different regulatory modules meet. Curr Opin Plant Biol 12:548–555

    CAS  Google Scholar 

  • Tan BC, Schwartz SH, Zeevaart JAD, McCarty DR (1997) Genetic control of abscisic acid biosynthesis in maize. Proc Natl Acad Sci U S A 94:12235–12240

    CAS  Google Scholar 

  • Tong H, Xiao Y, Liu D, Gao S, Liu L, Yin Y, Jin Y, Qian Q, Chu C (2014) Brassinosteroid regulates cell elongation by modulating gibberellin metabolism in rice. Plant Cell 26:4376–4393

    CAS  Google Scholar 

  • Tsuchisaka A, Theologis A (2004) Unique and overlapping expression patterns among the Arabidopsis 1-amino-cyclopropane-1-carboxylate synthase gene family members. Plant Physiol 136:2982–3000

    CAS  Google Scholar 

  • Tuteja N (2007) Abscisic acid and abiotic stress signalling. Plant Signal Behav 2:135–138

    Google Scholar 

  • Ullah A, Heng S, Munis MF, Fahad S, Yang X (2015a) Phytoremediation of heavy metals assisted by plant growth promoting (PGP) bacteria: a review. Environ Exp Bot 117:28–40

    CAS  Google Scholar 

  • Ullah A, Mushtaq H, Ali H, Munis MF, Javed MT, Chaudhary HJ (2015b) Diazotrophs-assisted phytoremediation of heavy metals: a novel approach. Environ Sci Pollut Res 22:2505–2514

    CAS  Google Scholar 

  • Ullah A, Sun H, Yang X, Zhang X (2017) Drought coping strategies in cotton: increased crop per drop. Plant Biotechnol J 15:271–284

    CAS  Google Scholar 

  • Ullah A, Sun H, Yang X, Zhang X (2018) A novel cotton WRKY gene, GhWRKY6-like, improves salt tolerance by activating the ABA signalling pathway and scavenging of reactive oxygen species. Physiol Plant 162:439–454

    CAS  Google Scholar 

  • United Nations (2017) Department of economic and social affairs. https://www.un.org/development/desa/en/news/population/world-population-prospects-2017.html

  • Verma V, Ravindran P, Kumar PP (2016) Plant hormone-mediated regulation of stress responses. BMC Plant Biol 16:86

    Google Scholar 

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

    Google Scholar 

  • Vishwakarma K, Upadhyay N, Kumar N et al (2017) Abscisic acid signalling and abiotic stress tolerance in plants: a review on current knowledge and future prospects. Front Plant Sci 8:161

    Google Scholar 

  • Von Caemmerer S, Lawson T, Oxborough K, Baker NR, Andrews TJ, Raines CA (2004) Stomata conductance does not correlate with photosynthetic capacity in transgenic tobacco with reduced amounts of Rubisco. J Exp Bot 55:1157–1166

    Google Scholar 

  • Wager A, Browse J (2012) Social network: JAZ protein interactions expand our knowledge of jasmonate signalling. Front Plant Sci 3:41

    CAS  Google Scholar 

  • Wang C, Yang A, Yin H, Zhang J (2008) Influence of water stress on endogenous hormone contents and cell damage of maize seedlings. J Integr Plant Biol 50:427–434

    CAS  Google Scholar 

  • Wang J, Griffiths R, Ying J, McCourt P, Huang Y (2009) Development of drought-tolerant (Brassica napus L.) through genetic modulation of ABA-mediated stomata responses. Crop Sci 49:1539–1554

    Google Scholar 

  • Wani SH, Kumar V, Shriram V, Sah SK (2016) Phytohormones and their metabolic engineering for abiotic stress tolerance in crop plants. Crop J 4:162–176

    Google Scholar 

  • Wasson AP, Richards RA, Chatrath R, Misra SC, Prasad SVS, Rebetzke GJ, Kirkegaard JA, Christopher J, Watt M (2012) Traits and selection strategies to improve root systems and water uptake in water-limited wheat crops. J Exp Bot 63:3485–3498

    CAS  Google Scholar 

  • Wasternack C (2007) Jasmonates: an update on biosynthesis, signal transduction and action in plant stress response, growth and development. Ann Bot 100:681–697

    CAS  Google Scholar 

  • Werner T, Motyka V, Strnad M, Schmülling T (2001) Regulation of plant growth by cytokinin. Proc Natl Acad Sci U S A 98:10487–10492

    CAS  Google Scholar 

  • Werner T, Motyka V, Laucou V, Smets R, VanOnckelen H, Schmülling T (2003) Cytokinin-deficient transgenic Arabidopsis plants show multiple developmental alterations indicating opposite functions of cytokinins in the regulation of shoot and root meristem activity. Plant Cell 15:2532–2550

    CAS  Google Scholar 

  • Werner T, Nehnevajova E, Köllmer I, Novák O, Strnad M, Krämer U, Schmülling T (2010) Root-specific reduction of cytokinin causes enhanced root growth, drought tolerance, and leaf mineral enrichment in Arabidopsis and tobacco. Plant Cell 22:3905–3920

    Google Scholar 

  • Wolters H, Jürgens G (2009) Survival of the flexible: hormonal growth control and adaptation in plant development. Nat Rev Genet 10:305–317

    CAS  Google Scholar 

  • Wu Y, Zhang D, Chu JY, Boyle P, Wang Y, Brindle ID, De Lucy V, Després C (2012) The Arabidopsis NPR1 protein is a receptor for the plant defense hormone salicylic acid. Cell Rep 1:639–647

    CAS  Google Scholar 

  • Wu J, Kim SG, Kang KY, Kim JG, Park SR, Gupta R, Kim YH, Wang Y, Kim ST (2016) Overexpression of a pathogenesis-related protein 10 enhances biotic and abiotic stress tolerance in rice. Plant Pathol J 32:552–562

    CAS  Google Scholar 

  • Xiong L, Lee B, Ishitani M, Lee H, Zhang C, Zhu JK (2001) FIERY1 encoding an inositol polyphosphate 1-phosphatase is a negative regulator of abscisic acid and stress signalling in Arabidopsis. Genes Dev 15:1971–1984

    CAS  Google Scholar 

  • Xiong L, Wang RG, Mao G, Koczan JM (2006) Identification of drought tolerance determinants by genetic analysis of root response to drought stress and abscisic acid. Plant Physiol 142:1065–1074

    CAS  Google Scholar 

  • Xu Z, Zhou G, Shimizu H (2010) Plant responses to drought and rewatering. Plant Signal Behav 5:649–654

    CAS  Google Scholar 

  • Yamaguchi-Shinozaki K, Shinozaki K (2006) Transcriptional regulatory networks in cellular responses and tolerance to dehydration and cold stresses. Annu Rev Plant Biol 57:781–803

    CAS  Google Scholar 

  • Yang Z, Zhang Z, Zhang T, Fahad S, Cui K, Nie L, Peng S, Huang J (2017) The effect of season-long temperature increases on rice cultivars grown in the central and southern regions of China. Front Plant Sci 8:1908

    Google Scholar 

  • Ye H, Liu S, Tang B, Chen J, Xie Z, Nolan TM, Jiang H, Guo H, Lin HY, Li L, Wang Y, Tong H, Zhang M, Chu C, Li Z, Aluru M, Aluru S, Schnable PS, Yin Y (2017) RD26 mediates crosstalk between drought and brassinosteroid signalling pathways. Nat Commun 8:14573

    CAS  Google Scholar 

  • Yoshida T, Mogami J, Yamaguchi-Shinozaki K (2014) ABA-dependent and ABA-independent signalling in response to osmotic stress in plants. Curr Opin Plant Biol 21:133–139

    CAS  Google Scholar 

  • Yu L, Chen X, Wang Z, Wang S, Wang Y, Zhu Q, Li S, Xiang C (2013) Arabidopsis enhanced drought tolerance1/HOMEODOMAIN GLABROUS11 confers drought tolerance in transgenic rice without yield penalty. Plant Physiol 162:1378–1391

    CAS  Google Scholar 

  • Yu LH, Wu SJ, Peng YS et al (2015) Arabidopsis EDT1/HDG11 improves drought and salt tolerance in cotton and poplar and increases cotton yield in the field. Plant Biotechnol J 14:72–84

    Google Scholar 

  • Zhang G, Chen M, Li L, Xu Z, Chen X, Guo J, Ma Y (2009a) Overexpression of the soybean GmERF3 gene, an AP2/ERF type transcription factor for increased tolerances to salt, drought, and diseases in transgenic tobacco. J Exp Bot 60:3781–3796

    CAS  Google Scholar 

  • Zhang SW, Li CH, Cao J, Zhang YC, Zhang SQ, Xia YF, Sun DY, Sun Y (2009b) Altered architecture and enhanced drought tolerance in rice via the down-regulation of indole-3-acetic acid by TLD1/ OsGH3.13 activation. Plant Physiol 151:1889–1901

    CAS  Google Scholar 

  • Zhu JK (2002) Salt and drought stress signal transduction in plants. Annu Rev Plant Biol 3:247–273

    Google Scholar 

  • Zhu SY, Yu XC, Wang XJ, Zhao R, Li Y, Fan RC, Shang Y, du SY, Wang XF, Wu FQ, Xu YH, Zhang XY, Zhang DP (2007) Two calcium-dependent protein kinases, CPK4 and CPK11, regulate abscisic acid signal transduction in Arabidopsis. Plant Cell 19:3019–3036

    CAS  Google Scholar 

  • Zwack PJ, Rashotte AM (2015) Interactions between cytokinin signalling and abiotic stress responses. J Exp Bot 66:4863–4871

    CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. National Key Laboratory of Crop Genetic Improvement, Huazhong Agricultural University, Wuhan, 430070, Hubei, People’s Republic of China

    Abid Ullah, Hakim Manghwar, Muhammad Shaban, Aamir Hamid Khan, Adnan Akbar, Usman Ali & Shah Fahad

  2. Department of Botany, University of Malakand, Chakdara Dir Lower, Khyber Pakhtunkhwa, 18550, Pakistan

    Abid Ullah

  3. Hubei Insect Resources Utilization and Sustainable Pest Management Key Laboratory, College of Plant Science and Technology, Huazhong Agricultural University, Wuhan, 430070, People’s Republic of China

    Ehsan Ali

  4. Department of Agriculture, University of Swabi, Swabi, KPK, Pakistan

    Shah Fahad

Authors
  1. Abid Ullah
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Hakim Manghwar
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Muhammad Shaban
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Aamir Hamid Khan
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Adnan Akbar
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Usman Ali
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Ehsan Ali
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Shah Fahad
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Abid Ullah.

Additional information

Responsible editor: Philippe Garrigues

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ullah, A., Manghwar, H., Shaban, M. et al. Phytohormones enhanced drought tolerance in plants: a coping strategy. Environ Sci Pollut Res 25, 33103–33118 (2018). https://doi.org/10.1007/s11356-018-3364-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-018-3364-5

Keywords

Search

Navigation