Skip to main content

Advertisement

Log in

Crosstalk amongst phytohormones from planta and PGPR under biotic and abiotic stresses

  • Review paper
  • Published:
Plant Growth Regulation Aims and scope Submit manuscript

Abstract

Phytohormones are endogenously produced organic substances indispensable for regulating plant growth and yield and also play major role in inducing tolerance to plants against various biotic and abiotic stresses. The convergence points among hormone signal transduction cascades are considered as cross-talk which are crucial for plant development as well as for plant responses to biotic and abiotic stresses. Hormones interact by activating either a second messenger or through a phosphorylation cascade. These transduction cascades lead to the regulation of gene expression that directly affects the biosynthesis or action of different hormones and developmental processes in coordination with multiple stimuli. Hormone synthesis, signal transduction, perception and cross-talk create a complex network. Interaction of plant growth promoting rhizobacteria (PGPR) which form intimate association with the roots of higher plants also modulate the level of endogenous phytohormones and demonstrate a new paradigm for hormonal interaction. The ratio of hormones changes with ontogeny of plant and the specific ratio of growth promoting and growth inhibiting hormones determine the response of plants. Furthermore, the sensitivity of plant tissue to each hormone changes with the exposure to stresses. This review is a compilation of the interactions between phytohormones and plant development. The cross talk between different hormones under abiotic and biotic stresses will be enumerated. Hormone and stress-responsive cis elements and the trans-regulation capabilities of miRNAs for the coordination of multiple hormonal responses will be discussed. Finally the role of PGPR will be evaluated under various environmental stresses with particular emphasis on phytohormone production and its interaction with host plant physiology. PGPR provides cross protective properties through improvement in defense mechanism controlling pathogen resistance through induced systemic resistance (ISR) and alleviating abiotic stress through influencing the phytohormones metabolism. PGPR isolates from stressed soil/stressed host plants impart tolerance to plants against abiotic and biotic stresses by modulating the production of phytohormones and alteration in their sensitivity to respond. Bacteria communicate with each other through quorum sensing molecules which also regulate gene expression and phytohormone production. The intricate relationship between other microbes/fungi and their residual effects on plant rhizosphere phytohormones need further investigation for better understanding of bacterial coordination with plants.

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
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

Data Availability

All the data described in this manuscript is fully accessible without any restrictions.

References

  • Achard P, Vriezen WH, Van Der Straeten D, Harberd NP (2003) Ethylene regulates Arabidopsis development via the modulation of DELLA protein growth repressor function. Plant Cell 15:2825

    PubMed  PubMed Central  CAS  Google Scholar 

  • Achard P, Cheng H, De Grauwe L, Decat J, Schoutteten H, Moritz T, Van Der Straeten D, Peng J, Harberd NP (2006) Integration of plant responses to environmentally activated phytohormonal signals. Science 311:94

    PubMed  CAS  Google Scholar 

  • Ahemad M, Kibret M (2014) Mechanisms and applications of plant growth promoting rhizobacteria: current perspective. JKSUS 1:20

    Google Scholar 

  • Ahmadi SA, Ebadi A, Jahanbakhsh S, Daneshian J, Siadat SA (2015) Changes in enzymatic and nonenzymatic antioxidant defense mechanisms of canola seedlings at different drought stress and nitrogen levels. Turk J Agric For 18(5):612

    Google Scholar 

  • An C, Mou Z (2011) Salicylic acid and its function in plant immunity. J Integr Plant Biol 1:428

    Google Scholar 

  • 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 1:3479

    Google Scholar 

  • Anuradha S, Rao SS (2001) Effect of brassinosteroids on salinity stress induced inhibition of seed germination and seedling growth of rice (Oryza sativa L.). Plant Growth Regul 1:153

    Google Scholar 

  • Ashraf MF, Foolad M (2007) Roles of glycine betaine and proline in improving plant abiotic stress resistance. Environ Exp Bot 1:206–216

    Google Scholar 

  • Asselbergh B, De Vleesschauwer D, Höfte M (2008) Global switches and fine-tuning—ABA modulates plant pathogen defense. Mol Plant-Microbe Interact 21:719

    PubMed  CAS  Google Scholar 

  • Babalola OO (2010) Beneficial bacteria of agricultural importance. Biotechnol Lett 1:1559–1570

    Google Scholar 

  • Bari R, Jones JD (2009) Role of plant hormones in plant defence responses. Plant Mol Biol 1:473–488

    Google Scholar 

  • Beneduzi A, Ambrosini A, Passaglia LM (2012) Plant growth-promoting rhizobacteria (PGPR): their potential as antagonists and biocontrol agents. Gen Mol Biol 35:1044–1051

    CAS  Google Scholar 

  • Berg G, Alavi M, Schmidt CS, Zachow C, Egamberdieva D, Kamilova F, Lugtenberg BJ (2013) Biocontrol and osmoprotection for plants under salinated conditions. Mol Microb Ecol Rhizosphere 3:573

    Google Scholar 

  • Berrocal-Lobo M, Molina A, Solano R (2002) Constitutive expression of ETHYLENE‐RESPONSE‐FACTOR1 in Arabidopsis confers resistance to several necrotrophic fungi. Plant J 29:23–32

    PubMed  CAS  Google Scholar 

  • Bielach A, Hrtyan M, Tognetti V (2017) Plants under stress: Involvement of auxin and cytokinin. Int J Mol Sci 18:1427

    PubMed Central  Google Scholar 

  • Boter M, Ruíz-Rivero O, Abdeen A, Prat S (2004) Conserved MYC transcription factors play a key role in jasmonate signaling both in tomato and Arabidopsis. Gen Dev 1:1591

    Google Scholar 

  • Bradford KJ, Nonogaki H (2007) Seed development, dormancy and germination. Blackwell Publishing, Oxford

    Google Scholar 

  • Capell T, Bassie L, Christou P (2004) Modulation of the polyamine biosynthetic pathway in transgenic rice confers tolerance to drought stress. Proc Natl Acad Sci 29:9909–9914

    Google Scholar 

  • Cassan F, Perrig D, Sgroy V, Masciarelli O, Penna C, Luna V (2009) Azospirillum brasilense Az39 and Bradyrhizobium japonicum E109, inoculated singly or in combination, promote seed germination and early seedling growth in corn (Zea mays L.) and soybean (Glycine max L.). Europ J Soil Biol 1:28–35

    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

    PubMed  PubMed Central  CAS  Google Scholar 

  • Cheng Y, Dai X, Zhao Y (2007) Auxin synthesized by the YUCCA flavin monooxygenases is essential for embryogenesis and leaf formation in Arabidopsis. Plant Cell 19:2430–2439

    PubMed  PubMed Central  CAS  Google Scholar 

  • Cheng X, Ruyter-Spira C, Bouwmeester H (2013) The interaction between strigolactones and other plant hormones in the regulation of plant development. Front Plant Sci 17:199

    Google Scholar 

  • Chinchilla D, Zipfel C, Robatzek S, Kemmerling B, Nürnberger T, Jones JD, Felix G, Boller T (2007) A flagellin-induced complex of the receptor FLS2 and BAK1 initiates plant defence. Nature 448:497

    PubMed  CAS  Google Scholar 

  • Clarke SM, Mur LA, Wood JE, Scott IM (2004) Salicylic acid dependent signaling promotes basal thermotolerance but is not essential for acquired thermotolerance in Arabidopsis thaliana. Plant J 38:432–447

    PubMed  CAS  Google Scholar 

  • Cohen P (1982) The role of protein phosphorylation in neural and hormonal control of cellular activity. Nature 296:613

    PubMed  CAS  Google Scholar 

  • Cosa S, Chaudhary SK, Chen W, Combrinck S, Viljoen A (2019) Exploring common culinary herbs and spices as potential anti-quorum sensing agents. Nutrients 11(4):739

    PubMed Central  CAS  Google Scholar 

  • Couée I, Sulmon C, Gouesbet G, El Amrani A (2006) Involvement of soluble sugars in reactive oxygen species balance and responses to oxidative stress in plants. J Exp Bot 5:449–459

    Google Scholar 

  • Dai A (2013) Increasing drought under global warming in observations and models. Nat Clim Change 3:52

    Google Scholar 

  • Dash M, Panda SK (2001) Salt stress induced changes in growth and enzyme activities in germinating Phaseolus mungo seeds. Biol Plant 44:587–589

    CAS  Google Scholar 

  • Daszkowska-Golec A, Szarejko I (2013) Open or close the gate–stomata action under the control of phytohormones in drought stress conditions. Front Plant Sci 13:138

    Google Scholar 

  • De Lucia EH, Nabity PD, Zavala JA, Berenbaum MR (2012) Climate change: resetting plant-insect interactions. Plant Physiol 160:1677–1685

    Google Scholar 

  • Depuydt S, Hardtke CS (2011) Hormone signalling crosstalk in plant growth regulation. Curr Biol 21:R365–R373

    PubMed  CAS  Google Scholar 

  • Dimkpa C, Weinand T, Asch F (2009) Plant–rhizobacteria interactions alleviate abiotic stress conditions. Plant Cell Environ 32:1682–1694

    PubMed  CAS  Google Scholar 

  • Ding L, Xu H, Yi H, Yang L, Kong Z, Zhang L, Xue S, Jia H, Ma Z (2011) Resistance to hemi-biotrophic F. graminearum infection is associated with coordinated and ordered expression of diverse defense signaling pathways. PLoS ONE 6:e19008

    PubMed  PubMed Central  CAS  Google Scholar 

  • Dodd IC, Pérez-Alfocea F (2012) Microbial amelioration of crop salinity stress. J Exp Bot 8;63(9):3415–3428

    Google Scholar 

  • Dombrecht B, Xue GP, Sprague SJ, Kirkegaard JA, Ross JJ, Reid JB, Fitt GP, Sewelam N, Schenk PM, Manners JM, Kazan K (2007) MYC2 differentially modulates diverse jasmonate-dependent functions in Arabidopsis. Plant Cell 19:2225–2245

    PubMed  PubMed Central  CAS  Google Scholar 

  • Dong H, Delaney TP, Bauer DW, Beer SV (1999) Harpin induces disease resistance in Arabidopsis through the systemic acquired resistance pathway mediated by salicylic acid and the NIM1 gene. Plant J 20:207–215

    PubMed  CAS  Google Scholar 

  • Egamberdieva D (2009) Alleviation of salt stress by plant growth regulators and IAA producing bacteria in wheat. Acta Physiol Plant 31:861–864

    CAS  Google Scholar 

  • Egamberdieva D, Kucharova Z, Davranov K, Berg G, Makarova N, Azarova T, Chebotar V, Tikhonovich I, Kamilova F, Validov SZ, Lugtenberg B (2011) Bacteria able to control foot and root rot and to promote growth of cucumber in salinated soils. Biol Fertil Soils 47:197–205

    CAS  Google Scholar 

  • Etesami H, Alikhani HA, Hosseini HM (2015) Indole-3-acetic acid (IAA) production trait, a useful screening to select endophytic and rhizosphere competent bacteria for rice growth promoting agents. MethodsX 2:72–78

    PubMed  PubMed Central  Google Scholar 

  • Fahad S, Hussain S, Bano A, Saud S, Hassan S, Shan D, Khan FA, Khan F, Chen Y, Wu C, Tabassum MA (2015) Potential role of phytohormones and plant growth-promoting rhizobacteria in abiotic stresses: consequences for changing environment. Environ Sci Pollut Res 22:4907–4921

    Google Scholar 

  • Farooq M, Hussain M, Wahid A, Siddique KH (2012) Drought stress in plants: an overview. InPlant responses to drought stress. Springer, Berlin, pp 1–33

    Google Scholar 

  • Fernández-Calvo P, Chini A, Fernández-Barbero G, Chico JM, Gimenez-Ibanez S, Geerinck J, Eeckhout D, Schweizer F, Godoy M, Franco-Zorrilla JM, Pauwels L (2011) The Arabidopsis bHLH transcription factors MYC3 and MYC4 are targets of JAZ repressors and act additively with MYC2 in the activation of jasmonate responses. Plant Cell 23:701–715

    PubMed  PubMed Central  Google Scholar 

  • Finkelstein R (2013) Abscisic acid synthesis and response. The Arabidopsis Book/American Society of Plant Biologists, Rockville, p 11

    Google Scholar 

  • Foyer CH, Noctor G (2016) Stress-triggered redox signalling: what's in pROSpect? Plant Cell Environ 39:951–964

    PubMed  CAS  Google Scholar 

  • Fraire-Velázquez S, Rodríguez-Guerra R, Sánchez-Calderón L (2011) Abiotic and biotic stress response crosstalk in plants. In: Shanker AK, Venkateswarlu B (eds) Abiotic stress response in plants- physiological, biochemical and genetic perspectives. InTech, Rijeka, pp 3–26

    Google Scholar 

  • Frigerio M, Alabadí D, Pérez-Gómez J, García-Cárcel L, Phillips AL, Hedden P, Blázquez MA (2006) Transcriptional regulation of gibberellin metabolism genes by auxin signaling in Arabidopsis. Plant Physiol 142:553–563

    PubMed  PubMed Central  CAS  Google Scholar 

  • Friml J, Vieten A, Sauer M, Weijers D, Schwarz H, Hamann T, Offringa R, Jürgens G (2003) Efflux-dependent auxin gradients establish the apical–basal axis of Arabidopsis. Nature 426:147

    PubMed  CAS  Google Scholar 

  • Fu X, Harberd NP (2003) Auxin promotes Arabidopsis root growth by modulating gibberellin response. Nature 421:740

    PubMed  CAS  Google Scholar 

  • Fujita M, Fujita Y, Noutoshi Y, Takahashi F, Narusaka Y, Yamaguchi-Shinozaki K, Shinozaki K (2006) Crosstalk between abiotic and biotic stress responses: a current view from the points of convergence in the stress signaling networks. Curr Opin Plant Biol 9:436–442

    PubMed  Google Scholar 

  • Ganeshamoorthi P, Anand T, Prakasam V, Bharani M, Ragupathi N, Samiyappan R (2008) Plant growth promoting rhizobacterial (PGPR) bioconsortia mediates induction of defense-related proteins against infection of root rot pathogen in mulberry plants. J Plant Interact 3(4):233–244

    CAS  Google Scholar 

  • Gao Y, Wang W, Zhang T, Gong Z, Zhao H, Han GZ (2018) Out of water: the origin and early diversification of plant R-genes. Plant Physiol 177:89

    PubMed  PubMed Central  CAS  Google Scholar 

  • Gazzarrini S, Mccourt P (2003) Cross-talk in plant hormone signalling: what Arabidopsis mutants are telling us. Ann Bot 91:605–612

    PubMed  PubMed Central  CAS  Google Scholar 

  • Gray WM (2004) Hormonal regulation of plant growth and development. PLoS Biol 2(9):e311

    PubMed  PubMed Central  Google Scholar 

  • Grennan AK (2006) Abiotic stress in rice. An “omic” approach. Plant Physiol 140:1139–1141

    PubMed  PubMed Central  CAS  Google Scholar 

  • Guo H, Ecker JR (2004) The ethylene signaling pathway: new insights. Curr Opin Plant Biol 7:40–49

    PubMed  CAS  Google Scholar 

  • Han Q, Kang G, Guo T (2013) Proteomic analysis of spring freeze-stress responsive proteins in leaves of bread wheat (Triticum aestivum L.). Plant Physiol Biochem 63:236–244

    PubMed  CAS  Google Scholar 

  • Hartmann A, Rothballer M, Hense BA, Schröder P (2014) Bacterial quorum sensing compounds are important modulators of microbe-plant interactions. Front Plant Sci 5:131

    PubMed  PubMed Central  Google Scholar 

  • Hassan MK, McInroy JA, Kloepper JW (2019) The interactions of rhizodeposits with plant growth-promoting rhizobacteria in the rhizosphere: a review. Agriculture 9(7):142

    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 

  • Ilangumaran G, Smith DL (2017) Plant growth promoting rhizobacteria in amelioration of salinity stress: a systems biology perspective. Front Plant Sci 23:8:1768

    Google Scholar 

  • Jayapala N, Mallikarjunaiah NH, Puttaswamy H, Gavirangappa H, Ramachandrappa NS (2019) Rhizobacteria Bacillus spp. induce resistance against anthracnose disease in chili (Capsicum annuum L.) through activating host defense response. Egypt J Biol Pest Control 29(1):45

    Google Scholar 

  • Ju C, Yoon GM, Shemansky JM, Lin DY, Ying ZI, Chang J, Garrett WM, Kessenbrock M, Groth G, Tucker ML, Cooper B (2012) CTR1 phosphorylates the central regulator EIN2 to control ethylene hormone signaling from the ER membrane to the nucleus in Arabidopsis. Proc Natl Acad Sci 109:19486–19491

    PubMed  CAS  Google Scholar 

  • Kang SM, Khan AL, You YH, Kim JG, Kamran M, Lee IJ (2014) Gibberellin production by newly isolated strain Leifsonia soli SE134 and its potential to promote plant growth. J Microbiol Biotechnol 24:106–112

    PubMed  CAS  Google Scholar 

  • Kangasjärvi J, Jaspers P, Kollist H (2005) Signalling and cell death in ozone-exposed plants. Plant Cell Environ 28:1021–1036

    Google Scholar 

  • Kazan K, Manners JM (2012) JAZ repressors and the orchestration of phytohormone crosstalk. Trends Plant Sci 17:22–31

    PubMed  CAS  Google Scholar 

  • Khan N, Bano A (2016) Modulation of phytoremediation and plant growth by the treatment with PGPR, Ag nanoparticle and untreated municipal wastewater. Int J Phytoremed 18:1258–1269

    CAS  Google Scholar 

  • Khan MI, 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

    PubMed  CAS  Google Scholar 

  • Khan Z, Rho H, Firrincieli A, Hung SH, Luna V, Masciarelli O, Kim SH, Doty SL (2016) Growth enhancement and drought tolerance of hybrid poplar upon inoculation with endophyte consortia. Curr Plant Biol 6:38–47

    Google Scholar 

  • Khan N, Bano A, Babar MA (2017) The root growth of wheat plants, the water conservation and fertility status of sandy soils influenced by plant growth promoting rhizobacteria. Symbiosis 72:195–205

    CAS  Google Scholar 

  • Khan N, Bano A, Zandi P (2018) Effects of exogenously applied plant growth regulators in combination with PGPR on the physiology and root growth of chickpea (Cicer arietinum) and their role in drought tolerance. J Plant Interact 13:239–247

    CAS  Google Scholar 

  • Khan N, Bano A, Rahman MA, Rathinasabapathi B, Babar MA (2019) UPLC-HRMS‐based untargeted metabolic profiling reveals changes in chickpea (Cicer arietinum) metabolome following long‐term drought stress. Plant Cell Environ 42:115–132

    PubMed  CAS  Google Scholar 

  • Kishor PK, Sangam S, Amrutha RN, Laxmi PS, Naidu KR, Rao KR, Rao S, Reddy KJ, Theriappan P, Sreenivasulu N (2005) Regulation of proline biosynthesis, degradation, uptake and transport in higher plants: its implications in plant growth and abiotic stress tolerance. Curr Sci 88:424–438

    CAS  Google Scholar 

  • Kudoyarova GR, Melentiev AI, Martynenko EV, Timergalina LN, Arkhipova TN, Shendel GV, Kuz'mina LY, Dodd IC, Veselov SY (2014) Cytokinin producing bacteria stimulate amino acid deposition by wheat roots. Plant Physiol Biochem 83:285–291

    PubMed  CAS  Google Scholar 

  • Lackman P, González-Guzmán M, Tilleman S, Carqueijeiro I, Pérez AC, Moses T, Seo M, Kanno Y, Häkkinen ST, Van Montagu MC, Thevelein JM (2011) Jasmonate signaling involves the abscisic acid receptor PYL4 to regulate metabolic reprogramming in Arabidopsis and tobacco. Proc Natl Aca Sci 108:5891–5896

    CAS  Google Scholar 

  • Lakshmanan V, Kitto SL, Caplan JL, Hsueh YH, Kearns DB, Wu YS, Bais HP (2012) Microbe-associated molecular patterns-triggered root responses mediate beneficial rhizobacterial recruitment in Arabidopsis. Plant Physiol 160(3):1642–1661

    PubMed  PubMed Central  CAS  Google Scholar 

  • Lee SJ, Kang JY, Park HJ, Kim MD, Bae MS, Choi HI, Kim SY (2010) DREB2C interacts with ABF2, a bZIP protein regulating abscisic acid-responsive gene expression, and its overexpression affects abscisic acid sensitivity. Plant Physiol 153:716–727

    PubMed  PubMed Central  CAS  Google Scholar 

  • Leshem Y, Seri L, Levine A (2007) Induction of phosphatidylinositol 3-kinase-mediated endocytosis by salt stress leads to intracellular production of reactive oxygen species and salt tolerance. Plant J 51(2):185–197

    PubMed  CAS  Google Scholar 

  • Li H, Jiang H, Bu Q, Zhao Q, Sun J, Xie Q, Li C (2011) The Arabidopsis RING finger E3 ligase RHA2b acts additively with RHA2a in regulating abscisic acid signaling and drought response. Plant Physiol 156(2):550–563

    PubMed  PubMed Central  CAS  Google Scholar 

  • Lobell DB, Roberts MJ, Schlenker W, Braun N, Little BB, Rejesus RM, Hammer GL (2014) Greater sensitivity to drought accompanies maize yield increase in the US Midwest. Science 344:516–519

    PubMed  CAS  Google Scholar 

  • Ludwig AA, Saitoh H, Felix G, Freymark G, Miersch O, Wasternack C, Boller T, Jones JD, Romeis T (2005) Ethylene-mediated cross-talk between calcium-dependent protein kinase and MAPK signaling controls stress responses in plants. Proc Nat Acad Sci 102(30):10736–10741

    PubMed  CAS  Google Scholar 

  • Ma Q, Zhou Q, Chen C, Cui Q, Zhao Y, Wang K, Arkorful E, Chen X, Sun K, Li X (2019) Isolation and expression analysis of CsCML genes in response to abiotic stresses in the tea plant (Camellia sinensis). Sci Rep 9(1):8211

    PubMed  PubMed Central  Google Scholar 

  • Magome H, Yamaguchi S, Hanada A, Kamiya Y, Oda K (2008) The DDF1 transcriptional activator upregulates expression of a gibberellin-deactivating gene, GA2ox7, under high‐salinity stress in Arabidopsis. Plant J 56:613–626

    PubMed  CAS  Google Scholar 

  • Matsuo S, Kikuchi K, Fukuda M, Honda I, Imanishi S (2012) Roles and regulation of cytokinins in tomato fruit development. J Exp Bot 63:5569–5579

    PubMed  PubMed Central  CAS  Google Scholar 

  • Mattsson J, Ckurshumova W, Berleth T (2003) Auxin signaling in Arabidopsis leaf vascular development. Plant Physiol 131:1327–1339

    PubMed  PubMed Central  CAS  Google Scholar 

  • McSteen P, Zhao Y (2008) Plant hormones and signaling: common themes and new developments. Develop Cell 14:467–473

    CAS  Google Scholar 

  • Mewis I, Appel HM, Hom A, Raina R, Schultz JC (2005) Major signaling pathways modulate Arabidopsis glucosinolate accumulation and response to both phloem-feeding and chewing insects. Plant Physiol 138:1149–1162

    PubMed  PubMed Central  CAS  Google Scholar 

  • Mirza MS, Mehnaz S, Normand P, Prigent-Combaret C, Moënne-Loccoz Y, Bally R, Malik KA (2006) Molecular characterization and PCR detection of a nitrogen-fixing Pseudomonas strain promoting rice growth. Biol Fertil Soils 43:170

    CAS  Google Scholar 

  • Moons A, Prinsen E, Bauw G, Van Montagu M (1997) Antagonistic effects of abscisic acid and jasmonates on salt stress-inducible transcripts in rice roots. Plant Cell 9:2243–2259

    PubMed  PubMed Central  CAS  Google Scholar 

  • Müller B, Sheen J (2008) Cytokinin and auxin interaction in root stem-cell specification during early embryogenesis. Nature 453:1094

    PubMed  PubMed Central  Google Scholar 

  • Müller H, Westendorf C, Leitner E, Chernin L, Riedel K, Schmidt S, Eberl L, Berg G (2009) Quorum-sensing effects in the antagonistic rhizosphere bacterium Serratia plymuthica HRO-C48. FEMS Microbiol Ecol 67(3):78

    PubMed  Google Scholar 

  • Naseem M, Philippi N, Hussain A, Wangorsch G, Ahmed N, Dandekar T (2012) Integrated systems view on networking by hormones in Arabidopsis immunity reveals multiple crosstalk for cytokinin. Plant Cell 24:1793–1814

    PubMed  PubMed Central  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 LS (2013) Arabidopsis AHP2, AHP3, and AHP5 histidine phosphotransfer proteins function as redundant negative regulators of drought stress response. Proc Natl Acad Sci 110:4840–4845

    PubMed  CAS  Google Scholar 

  • O'Neill DP, Ross JJ (2002) Auxin regulation of the gibberellin pathway in pea. Plant Physiol 130:1974–1982

    PubMed  PubMed Central  CAS  Google Scholar 

  • Pacifici E, Polverari L, Sabatini S (2015) Plant hormone cross-talk: the pivot of root growth. J Exp Bot 66:1113–1121

    PubMed  CAS  Google Scholar 

  • Pang Y, Liu X, Ma Y, Chernin L, Berg G, Gao K (2009) Induction of systemic resistance, root colonisation and biocontrol activities of the rhizospheric strain of Serratia plymuthica are dependent on N-acyl homoserine lactones. Eur J Plant Pathol 124(2):261–268

    CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Pereira SI, Monteiro C, Vega AL, Castro PM (2016) Endophytic culturable bacteria colonizing Lavandula dentata L. plants: isolation, characterization and evaluation of their plant growth-promoting activities. Ecol Eng 87:97

    Google Scholar 

  • Pieterse CM, Leon-Reyes A, Van der Ent S, Van Wees SC (2009) Networking by small-molecule hormones in plant immunity. Nat Chem Biol 5:308

    PubMed  CAS  Google Scholar 

  • Pieterse CM, Van der Does D, Zamioudis C, Leon-Reyes A, Van Wees SC (2012) Hormonal modulation of plant immunity. Ann Rev Cell Dev Biol 28:521

    CAS  Google Scholar 

  • Pospíšilová J (2003) Participation of phytohormones in the stomatal regulation of gas exchange during water stress. Biol Plant 46:491–506

    Google Scholar 

  • Rais A, Jabeen Z, Shair F, Hafeez FY, Hassan MN (2017) Bacillus spp., a bio-control agent enhances the activity of antioxidant defense enzymes in rice against Pyricularia oryzae. PLoS ONE 12(11):e0187412

    PubMed  PubMed Central  Google Scholar 

  • Rasmussen S, Barah P, Suarez-Rodriguez MC, Bressendorff S, Friis P, Costantino P, Bones AM, Nielsen HB, Mundy J (2013) Transcriptome responses to combinations of stresses in Arabidopsis. Plant Physiol 161(4):1783–1794

    PubMed  PubMed Central  CAS  Google Scholar 

  • Robert-Seilaniantz A, Grant M, Jones JD (2010) Hormone crosstalk in plant disease and defense: more than just jasmonate-salicylate antagonism. Ann Rev Phytopathol 49:317–343

    Google Scholar 

  • Rodriguez M, Rodriguez A, Bayer J, Vilaseca F, Girones J, Mutje P (2010) determination of corn stalk fibers’strength through modeling of the mechanical properties of its composites. BioRes 5:2535–2546

    Google Scholar 

  • Rohila JS, Yang Y (2007) Rice mitogen-activated protein kinase gene family and its role in biotic and abiotic stress response. J Integr Plant Biol 49:759

    CAS  Google Scholar 

  • Ross JJ, O'neill DP, Smith JJ, Kerckhoffs LH, Elliott RC (2000) Evidence that auxin promotes gibberellin A1 biosynthesis in pea. Plant J 21:547–552

    PubMed  CAS  Google Scholar 

  • Ross JJ, O’neill DP, Wolbang CM, Symons GM, Reid JB (2001) Auxin-gibberellin interactions and their role in plant growth. J Plant Growth Regul 20:353

    PubMed  Google Scholar 

  • Ryan RP, Dow JM (2008) Diffusible signals and interspecies communication in bacteria. Microbiol 154(7):1845–1858

    CAS  Google Scholar 

  • Sabatini S, Beis D, Wolkenfelt H, Murfett J, Guilfoyle T, Malamy J, Benfey P, Leyser O, Bechtold N, Weisbeek P, Scheres B (1999) An auxin-dependent distal organizer of pattern and polarity in the Arabidopsis root. Cell 99:463–472

    PubMed  CAS  Google Scholar 

  • Santner A, Estelle M (2009) Recent advances and emerging trends in plant hormone signalling. Nature 459:1071

    PubMed  CAS  Google Scholar 

  • Santner A, Calderon-Villalobos LI, Estelle M (2009) Plant hormones are versatile chemical regulators of plant growth. Nat Chem Biol 5:301

    PubMed  CAS  Google Scholar 

  • Santoyo G, Pacheco CH, Salmerón JH, León RH (2017) The role of abiotic factors modulating the plant-microbe-soil interactions: toward sustainable agriculture. A review. Span J Agric Res 15(1):13

    Google Scholar 

  • Scarpella E, Marcos D, Friml J, Berleth T (2006) Control of leaf vascular patterning by polar auxin transport. Gen Dev 20:1027

    CAS  Google Scholar 

  • Schweizer F, Fernández-Calvo P, Zander M, Diez-Diaz M, Fonseca S, Glauser G, Lewsey MG, Ecker JR, Solano R, Reymond P (2013) Arabidopsis basic helix-loop-helix transcription factors MYC2, MYC3, and MYC4 regulate glucosinolate biosynthesis, insect performance, and feeding behavior. Plant Cell 25:3117–3132

    PubMed  PubMed Central  CAS  Google Scholar 

  • Seckin B, Sekmen AH, Türkan I (2009) An enhancing effect of exogenous mannitol on the antioxidant enzyme activities in roots of wheat under salt stress. J Plant Growth Regul 28:12

    CAS  Google Scholar 

  • Shaharoona B, Arshad M, Zahir ZA (2006) Effect of plant growth promoting rhizobacteria containing ACC-deaminase on maize (Zea mays L.) growth under axenic conditions and on nodulation in mung bean (Vigna radiata L.). Lett App Microb 42:155–159

    CAS  Google Scholar 

  • Sharma R, De Vleesschauwer D, Sharma MK, Ronald PC (2013) Recent advances in dissecting stress-regulatory crosstalk in rice. Mol Plant 6:250–260

    PubMed  CAS  Google Scholar 

  • Shi JH, Yang ZB (2011) Is ABP1 an auxin receptor yet? Mol Plant 4:635–640

    PubMed  PubMed Central  CAS  Google Scholar 

  • Shi Y, Tian S, Hou L, Huang X, Zhang X, Guo H, Yang S (2012) Ethylene signaling negatively regulates freezing tolerance by repressing expression of CBF and type-A ARR genes in Arabidopsis. Plant Cell 24(6):2578–2595

    PubMed  PubMed Central  CAS  Google Scholar 

  • Shinozaki K, Yamaguchi-Shinozaki K (2007) Gene networks involved in drought stress response and tolerance. J Exp Bot 58:221–227

    PubMed  CAS  Google Scholar 

  • Singh RP, Jha PN (2017) The PGPR Stenotrophomonas maltophilia SBP-9 augments resistance against biotic and abiotic stress in wheat plants. Front Microbiol 8:1945

    PubMed  PubMed Central  Google Scholar 

  • Sivasakthi S, Usharani G, Saranraj P (2014) Biocontrol potentiality of plant growth promoting bacteria (PGPR)-Pseudomonas fluorescens and Bacillus subtilis: A review. Afr J Agric Res 9:1277

    Google Scholar 

  • Smith DL, Subramanian S, Lamont JR, Bywater-Ekegärd M (2015) Signaling in the phytomicrobiome: breadth and potential. Front Plant Sci 6:709

    PubMed  PubMed Central  Google Scholar 

  • Spoel SH, Dong X (2008) Making sense of hormone crosstalk during plant immune responses. Cell Host Microbe 3:348–351

    PubMed  CAS  Google Scholar 

  • Sun TP, Gubler F (2004) Molecular mechanism of gibberellin signaling in plants. Annu Rev Plant Biol 55:197–223

    PubMed  CAS  Google Scholar 

  • Sun Y, Fan XY, Cao DM, Tang W, He K, Zhu JY, He JX, Bai MY, Zhu S, Oh E, Patil S (2010) Integration of brassinosteroid signal transduction with the transcription network for plant growth regulation in Arabidopsis. Dev Cell 19:777

    PubMed  PubMed Central  CAS  Google Scholar 

  • Tabur S, Demir K (2010) Protective roles of exogenous polyamines on chromosomal aberrations in Hordeum vulgare exposed to salinity. Biologia 65:947–953

    CAS  Google Scholar 

  • Tanaka Y, Sano T, Tamaoki M, Nakajima N, Kondo N, Hasezawa S (2005) Ethylene inhibits abscisic acid-induced stomatal closure in Arabidopsis. Plant Physiol 138:2337–2343

    PubMed  PubMed Central  CAS  Google Scholar 

  • Tanaka Y, Sano T, Tamaoki M, Nakajima N, Kondo N, Hasezawa S (2006) Cytokinin and auxin inhibit abscisic acid-induced stomatal closure by enhancing ethylene production in Arabidopsis. J Exp Bot 57:2259–2266

    PubMed  CAS  Google Scholar 

  • Teale WD, Paponov IA, Palme K (2006) Auxin in action: signalling, transport and the control of plant growth and development. Nat Rev Mol Cell Biol 7:847

    PubMed  CAS  Google Scholar 

  • Thaler JS, Humphrey PT, Whiteman NK (2012) Evolution of jasmonate and salicylate signal crosstalk. Trends Plant Sci 17:270

    PubMed  CAS  Google Scholar 

  • Turan M, Ekinci M, Yildirim E, Güneş A, Karagöz K, Kotan R, Dursun A (2014) Plant growth-promoting rhizobacteria improved growth, nutrient, and hormone content of cabbage (Brassica oleracea) seedlings. Turk J Agric For 38:333

    CAS  Google Scholar 

  • Tuteja N, Gill SS, Trivedi PK, Asif MH, Nath P (2010) Plant growth regulators and their role in stress tolerance. Plant nutrition and abiotic stress tolerance I. Plant Stress 4:18

    Google Scholar 

  • Ubaidillah M, Safitri FA, Jo JH, Lee SK, Hussain A, Mun BG, Chung IK, Yun BW, Kim KM () Roles of plant hormones and anti-apoptosis genes during drought stress in rice (Oryza sativa L.). 3 Biotech 6:247

    PubMed  PubMed Central  Google Scholar 

  • Umamaheswari A, Nuni A, Shreevidya R (2010) Evaluation of antibacterial activity of Boerhaavia diffusa L. leaves. Int J Green Pharm (IJGP) 4(2)

    Google Scholar 

  • Venkateswarlu B, Shanker AK (2009) Climate change and agriculture: adaptation and mitigation stategies. Indian J Agron 54(2):226

    Google Scholar 

  • Vos IA, Verhage A, Schuurink RC, Watt LG, Pieterse CM, Van Wees S (2013) Onset of herbivore-induced resistance in systemic tissue primed for jasmonate-dependent defenses is activated by abscisic acid. Front Plant Sci 4:539

    PubMed  PubMed Central  Google Scholar 

  • Wally O, Jayaraj J, Punja ZK (2009) Broad-spectrum disease resistance to necrotrophic and biotrophic pathogens in transgenic carrots (Daucus carota L.) expressing an Arabidopsis NPR1 gene. Planta 231:131–141

    PubMed  CAS  Google Scholar 

  • Wang Y, Wang T, Li K, Li X (2008) Genetic analysis of involvement of ETR1 in plant response to salt and osmotic stress. Plant Growth Regul 54:269

    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 

  • Weiss D, Ori N (2007) Mechanisms of cross talk between gibberellin and other hormones. Plant Physiol 144:1240–1246

    PubMed  PubMed Central  CAS  Google Scholar 

  • Wolbang CM, Ross JJ (2001) Auxin promotes gibberellin biosynthesis in decapitated tobacco plants. Planta 214:153–157

    PubMed  CAS  Google Scholar 

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

    CAS  Google Scholar 

  • Xiong L, Lee H, Ishitani M, Zhu JK (2002) Regulation of osmotic stress-responsive gene expression by the LOS6/ABA1 locus in Arabidopsis. J Biol Chem 277:8596

    PubMed  CAS  Google Scholar 

  • Yang JC, Zhang JH, Wang ZQ, Zhu QS, Liu LJ (2003) Involvement of abscisic acid and cytokinins in the senescence and remobilization of carbon reserves in wheat subjected to water stress during grain filling. Plant Cell Environ 26:1621–1631

    CAS  Google Scholar 

  • Yang J, Kloepper JW, Ryu CM (2009) Rhizosphere bacteria help plants tolerate abiotic stress. Trends Plant Sci 14(1):1–4

    PubMed  CAS  Google Scholar 

  • Yang W, Liu XD, Chi XJ, Wu CA, Li YZ, Song LL, Liu XM, Wang YF, Wang FW, Zhang C, Liu Y (2011) Dwarf apple MbDREB1 enhances plant tolerance to low temperature, drought, and salt stress via both ABA-dependent and ABA-independent pathways. Planta 233:219–229

    PubMed  CAS  Google Scholar 

  • Yang DL, Yao J, Mei CS, Tong XH, Zeng LJ, Li Q, Xiao LT, Sun TP, Li J, Deng XW, Lee CM (2012) Plant hormone jasmonate prioritizes defense over growth by interfering with gibberellin signaling cascade. Proc Natl Acad Sci 109:E1200

    PubMed  CAS  Google Scholar 

  • Yang X, Kim MY, Ha J, Lee SH (2019) Overexpression of the soybean NAC gene GmNAC109 increases lateral root formation and abiotic stress tolerance in transgenic Arabidopsis plants. Front Plant Sci 10:1036

    PubMed  PubMed Central  Google Scholar 

  • Yuan GF, Jia CG, Li Z, Sun B, Zhang LP, Liu N, Wang QM (2010) Effect of brassinosteroids on drought resistance and abscisic acid concentration in tomato under water stress. Sci Horticult 126:103–108

    CAS  Google Scholar 

  • Zhao Z, Zhang Y, Liu X, Zhang X, Liu S, Yu X, Ren Y, Zheng X, Zhou K, Jiang L, Guo X (2013) A role for a dioxygenase in auxin metabolism and reproductive development in rice. Dev Cell 27:122

    PubMed  CAS  Google Scholar 

  • Zhou B, Zhang L, Ullah A, Jin X, Yang X, Zhang X (2016) Identification of multiple stress responsive genes by sequencing a normalized cDNA library from sea-land cotton (Gossypium barbadense L.). PLoS ONE 31(3):e0152927

    Google Scholar 

  • Zhu H, Dardick CD, Beers EP, Callanhan AM, Xia R, Yuan R (2011) Transcriptomics of shading-induced and NAA-induced abscission in apple (Malus domestica) reveals a shared pathway involving reduced photosynthesis, alterations in carbohydrate transport and signaling and hormone crosstalk. BMC Plant Biol 11:138

    PubMed  PubMed Central  Google Scholar 

  • Zúñiga A, Donoso RA, Ruiz D, Ruz GA, González B (2017) Quorum-sensing systems in the plant growth-promoting bacterium Paraburkholderia phytofirmans PsJN exhibit cross-regulation and are involved in biofilm formation. Mol Plant-Microbe Interact 30(7):557–565

    PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Contributions

N.K. and A.B. wrote the manuscript; M.A.B., and A.B., edited the manuscript, S.A., generated figures and review the manuscript.

Corresponding author

Correspondence to Naeem Khan.

Ethics declarations

Conflict of interest

The authors declare no conflict of interest.

Ethical approval

I testify on behalf of all co-authors that our article has not been published in whole or in part elsewhere; the manuscript is not currently being considered for publication in another journal and all authors have been personally and actively involved in substantive work leading to the manuscript.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Khan, N., Bano, A., Ali, S. et al. Crosstalk amongst phytohormones from planta and PGPR under biotic and abiotic stresses. Plant Growth Regul 90, 189–203 (2020). https://doi.org/10.1007/s10725-020-00571-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10725-020-00571-x

Keywords

Navigation