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

  • Naeem KhanEmail author
  • Asghari Bano
  • Shahid Ali
  • Md. Ali Babar
Review paper
  • 42 Downloads

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.

Keywords

Phytohormone Cross-talk Signaling network Abiotic stresses 

Notes

Author 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.

Compliance with ethical standards

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.

References

  1. 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 15:2825PubMedPubMedCentralCrossRefGoogle Scholar
  2. 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 311:94PubMedCrossRefGoogle Scholar
  3. Ahemad M, Kibret M (2014) Mechanisms and applications of plant growth promoting rhizobacteria: current perspective. JKSUS 1:20Google Scholar
  4. 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):612CrossRefGoogle Scholar
  5. An C, Mou Z (2011) Salicylic acid and its function in plant immunity. J Integr Plant Biol 1:428CrossRefGoogle Scholar
  6. 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 1:3479CrossRefGoogle Scholar
  7. 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 1:153CrossRefGoogle Scholar
  8. Ashraf MF, Foolad M (2007) Roles of glycine betaine and proline in improving plant abiotic stress resistance. Environ Exp Bot 1:206–216CrossRefGoogle Scholar
  9. Asselbergh B, De Vleesschauwer D, Höfte M (2008) Global switches and fine-tuning—ABA modulates plant pathogen defense. Mol Plant-Microbe Interact 21:719PubMedCrossRefGoogle Scholar
  10. Babalola OO (2010) Beneficial bacteria of agricultural importance. Biotechnol Lett 1:1559–1570CrossRefGoogle Scholar
  11. Bari R, Jones JD (2009) Role of plant hormones in plant defence responses. Plant Mol Biol 1:473–488CrossRefGoogle Scholar
  12. Beneduzi A, Ambrosini A, Passaglia LM (2012) Plant growth-promoting rhizobacteria (PGPR): their potential as antagonists and biocontrol agents. Gen Mol Biol 35:1044–1051CrossRefGoogle Scholar
  13. 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 3:573Google Scholar
  14. Berrocal-Lobo M, Molina A, Solano R (2002) Constitutive expression of ETHYLENE‐RESPONSE‐FACTOR1 in Arabidopsis confers resistance to several necrotrophic fungi. Plant J 29:23–32PubMedCrossRefGoogle Scholar
  15. Bielach A, Hrtyan M, Tognetti V (2017) Plants under stress: Involvement of auxin and cytokinin. Int J Mol Sci 18:1427PubMedCentralCrossRefPubMedGoogle Scholar
  16. 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 1:1591CrossRefGoogle Scholar
  17. Bradford KJ, Nonogaki H (2007) Seed development, dormancy and germination. Blackwell Publishing, OxfordCrossRefGoogle Scholar
  18. 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 29:9909–9914CrossRefGoogle Scholar
  19. 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 1:28–35CrossRefGoogle Scholar
  20. 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 29:1425–1439PubMedPubMedCentralCrossRefGoogle Scholar
  21. 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 19:2430–2439PubMedPubMedCentralCrossRefGoogle Scholar
  22. 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 17:199Google Scholar
  23. 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 448:497PubMedPubMedCentralCrossRefGoogle Scholar
  24. 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 38:432–447PubMedCrossRefGoogle Scholar
  25. Cohen P (1982) The role of protein phosphorylation in neural and hormonal control of cellular activity. Nature 296:613PubMedCrossRefGoogle Scholar
  26. 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):739PubMedCentralCrossRefPubMedGoogle Scholar
  27. 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 5:449–459CrossRefGoogle Scholar
  28. Dai A (2013) Increasing drought under global warming in observations and models. Nat Clim Change 3:52CrossRefGoogle Scholar
  29. Dash M, Panda SK (2001) Salt stress induced changes in growth and enzyme activities in germinating Phaseolus mungo seeds. Biol Plant 44:587–589CrossRefGoogle Scholar
  30. 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 13:138Google Scholar
  31. De Lucia EH, Nabity PD, Zavala JA, Berenbaum MR (2012) Climate change: resetting plant-insect interactions. Plant Physiol 160:1677–1685CrossRefGoogle Scholar
  32. Depuydt S, Hardtke CS (2011) Hormone signalling crosstalk in plant growth regulation. Curr Biol 21:R365–R373PubMedCrossRefPubMedCentralGoogle Scholar
  33. Dimkpa C, Weinand T, Asch F (2009) Plant–rhizobacteria interactions alleviate abiotic stress conditions. Plant Cell Environ 32:1682–1694PubMedCrossRefPubMedCentralGoogle Scholar
  34. 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:e19008PubMedPubMedCentralCrossRefGoogle Scholar
  35. Dodd IC, Pérez-Alfocea F (2012) Microbial amelioration of crop salinity stress. J Exp Bot 8;63(9):3415–3428CrossRefGoogle Scholar
  36. 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 19:2225–2245PubMedPubMedCentralCrossRefGoogle Scholar
  37. 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 20:207–215PubMedCrossRefPubMedCentralGoogle Scholar
  38. Egamberdieva D (2009) Alleviation of salt stress by plant growth regulators and IAA producing bacteria in wheat. Acta Physiol Plant 31:861–864CrossRefGoogle Scholar
  39. 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 47:197–205CrossRefGoogle Scholar
  40. 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 2:72–78PubMedPubMedCentralCrossRefGoogle Scholar
  41. 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 22:4907–4921CrossRefGoogle Scholar
  42. Farooq M, Hussain M, Wahid A, Siddique KH (2012) Drought stress in plants: an overview. InPlant responses to drought stress. Springer, Berlin, pp 1–33CrossRefGoogle Scholar
  43. 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 23:701–715PubMedPubMedCentralCrossRefGoogle Scholar
  44. Finkelstein R (2013) Abscisic acid synthesis and response. The Arabidopsis Book/American Society of Plant Biologists, Rockville, p 11Google Scholar
  45. Foyer CH, Noctor G (2016) Stress-triggered redox signalling: what's in pROSpect? Plant Cell Environ 39:951–964PubMedCrossRefGoogle Scholar
  46. 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 3–26Google Scholar
  47. 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 142:553–563PubMedPubMedCentralCrossRefGoogle Scholar
  48. 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 426:147PubMedCrossRefGoogle Scholar
  49. Fu X, Harberd NP (2003) Auxin promotes Arabidopsis root growth by modulating gibberellin response. Nature 421:740PubMedCrossRefGoogle Scholar
  50. 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 9:436–442PubMedCrossRefGoogle Scholar
  51. 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):233–244CrossRefGoogle Scholar
  52. 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 177:89PubMedPubMedCentralCrossRefGoogle Scholar
  53. Gazzarrini S, Mccourt P (2003) Cross-talk in plant hormone signalling: what Arabidopsis mutants are telling us. Ann Bot 91:605–612PubMedPubMedCentralCrossRefGoogle Scholar
  54. Gray WM (2004) Hormonal regulation of plant growth and development. PLoS Biol 2(9):e311PubMedPubMedCentralCrossRefGoogle Scholar
  55. Grennan AK (2006) Abiotic stress in rice. An “omic” approach. Plant Physiol 140:1139–1141PubMedPubMedCentralCrossRefGoogle Scholar
  56. Guo H, Ecker JR (2004) The ethylene signaling pathway: new insights. Curr Opin Plant Biol 7:40–49PubMedCrossRefGoogle Scholar
  57. 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 63:236–244PubMedCrossRefGoogle Scholar
  58. Hartmann A, Rothballer M, Hense BA, Schröder P (2014) Bacterial quorum sensing compounds are important modulators of microbe-plant interactions. Front Plant Sci 5:131PubMedPubMedCentralCrossRefGoogle Scholar
  59. Hassan MK, McInroy JA, Kloepper JW (2019) The interactions of rhizodeposits with plant growth-promoting rhizobacteria in the rhizosphere: a review. Agriculture 9(7):142CrossRefGoogle Scholar
  60. Horváth E, Szalai G, Janda T (2007) Induction of abiotic stress tolerance by salicylic acid signaling. J Plant Growth Regul 26:290–300CrossRefGoogle Scholar
  61. Ilangumaran G, Smith DL (2017) Plant growth promoting rhizobacteria in amelioration of salinity stress: a systems biology perspective. Front Plant Sci 23:8:1768CrossRefGoogle Scholar
  62. 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):45CrossRefGoogle Scholar
  63. 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 109:19486–19491PubMedCrossRefGoogle Scholar
  64. 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 24:106–112PubMedCrossRefGoogle Scholar
  65. Kangasjärvi J, Jaspers P, Kollist H (2005) Signalling and cell death in ozone-exposed plants. Plant Cell Environ 28:1021–1036CrossRefGoogle Scholar
  66. Kazan K, Manners JM (2012) JAZ repressors and the orchestration of phytohormone crosstalk. Trends Plant Sci 17:22–31PubMedCrossRefGoogle Scholar
  67. 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 18:1258–1269CrossRefGoogle Scholar
  68. 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 80:67–74PubMedCrossRefGoogle Scholar
  69. 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 6:38–47CrossRefGoogle Scholar
  70. 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 72:195–205CrossRefGoogle Scholar
  71. 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 13:239–247CrossRefGoogle Scholar
  72. 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 42:115–132PubMedCrossRefGoogle Scholar
  73. 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 88:424–438Google Scholar
  74. 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 83:285–291PubMedCrossRefGoogle Scholar
  75. 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 108:5891–5896CrossRefGoogle Scholar
  76. 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):1642–1661PubMedPubMedCentralCrossRefGoogle Scholar
  77. 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 153:716–727PubMedPubMedCentralCrossRefGoogle Scholar
  78. 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):185–197PubMedCrossRefGoogle Scholar
  79. 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):550–563PubMedPubMedCentralCrossRefGoogle Scholar
  80. 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 344:516–519PubMedCrossRefGoogle Scholar
  81. 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):10736–10741PubMedCrossRefGoogle Scholar
  82. 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):8211PubMedPubMedCentralCrossRefGoogle Scholar
  83. 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 56:613–626PubMedCrossRefGoogle Scholar
  84. Matsuo S, Kikuchi K, Fukuda M, Honda I, Imanishi S (2012) Roles and regulation of cytokinins in tomato fruit development. J Exp Bot 63:5569–5579PubMedPubMedCentralCrossRefGoogle Scholar
  85. Mattsson J, Ckurshumova W, Berleth T (2003) Auxin signaling in Arabidopsis leaf vascular development. Plant Physiol 131:1327–1339PubMedPubMedCentralCrossRefGoogle Scholar
  86. McSteen P, Zhao Y (2008) Plant hormones and signaling: common themes and new developments. Develop Cell 14:467–473CrossRefGoogle Scholar
  87. 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 138:1149–1162PubMedPubMedCentralCrossRefGoogle Scholar
  88. 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 43:170CrossRefGoogle Scholar
  89. 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 9:2243–2259PubMedPubMedCentralGoogle Scholar
  90. Müller B, Sheen J (2008) Cytokinin and auxin interaction in root stem-cell specification during early embryogenesis. Nature 453:1094PubMedPubMedCentralCrossRefGoogle Scholar
  91. 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):78PubMedCrossRefGoogle Scholar
  92. 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 24:1793–1814PubMedPubMedCentralCrossRefGoogle Scholar
  93. 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 110:4840–4845PubMedCrossRefGoogle Scholar
  94. O'Neill DP, Ross JJ (2002) Auxin regulation of the gibberellin pathway in pea. Plant Physiol 130:1974–1982PubMedPubMedCentralCrossRefGoogle Scholar
  95. Pacifici E, Polverari L, Sabatini S (2015) Plant hormone cross-talk: the pivot of root growth. J Exp Bot 66:1113–1121PubMedCrossRefGoogle Scholar
  96. 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):261–268CrossRefGoogle Scholar
  97. Peleg Z, Blumwald E (2011) Hormone balance and abiotic stress tolerance in crop plants. Curr Opin Plant Biol 14:290–295PubMedCrossRefGoogle Scholar
  98. 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 87:97CrossRefGoogle Scholar
  99. Pieterse CM, Leon-Reyes A, Van der Ent S, Van Wees SC (2009) Networking by small-molecule hormones in plant immunity. Nat Chem Biol 5:308PubMedCrossRefGoogle Scholar
  100. 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 28:521CrossRefGoogle Scholar
  101. Pospíšilová J (2003) Participation of phytohormones in the stomatal regulation of gas exchange during water stress. Biol Plant 46:491–506CrossRefGoogle Scholar
  102. 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):e0187412PubMedPubMedCentralCrossRefGoogle Scholar
  103. 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):1783–1794PubMedPubMedCentralCrossRefGoogle Scholar
  104. Robert-Seilaniantz A, Grant M, Jones JD (2010) Hormone crosstalk in plant disease and defense: more than just jasmonate-salicylate antagonism. Ann Rev Phytopathol 49:317–343CrossRefGoogle Scholar
  105. 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 5:2535–2546Google Scholar
  106. 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 49:759CrossRefGoogle Scholar
  107. Ross JJ, O'neill DP, Smith JJ, Kerckhoffs LH, Elliott RC (2000) Evidence that auxin promotes gibberellin A1 biosynthesis in pea. Plant J 21:547–552PubMedCrossRefGoogle Scholar
  108. 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 20:353PubMedCrossRefGoogle Scholar
  109. Ryan RP, Dow JM (2008) Diffusible signals and interspecies communication in bacteria. Microbiol 154(7):1845–1858CrossRefGoogle Scholar
  110. 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 99:463–472PubMedCrossRefGoogle Scholar
  111. Santner A, Estelle M (2009) Recent advances and emerging trends in plant hormone signalling. Nature 459:1071PubMedCrossRefGoogle Scholar
  112. Santner A, Calderon-Villalobos LI, Estelle M (2009) Plant hormones are versatile chemical regulators of plant growth. Nat Chem Biol 5:301PubMedCrossRefGoogle Scholar
  113. 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):13CrossRefGoogle Scholar
  114. Scarpella E, Marcos D, Friml J, Berleth T (2006) Control of leaf vascular patterning by polar auxin transport. Gen Dev 20:1027CrossRefGoogle Scholar
  115. 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 25:3117–3132PubMedPubMedCentralCrossRefGoogle Scholar
  116. 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 28:12CrossRefGoogle Scholar
  117. 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 42:155–159CrossRefGoogle Scholar
  118. Sharma R, De Vleesschauwer D, Sharma MK, Ronald PC (2013) Recent advances in dissecting stress-regulatory crosstalk in rice. Mol Plant 6:250–260PubMedCrossRefGoogle Scholar
  119. Shi JH, Yang ZB (2011) Is ABP1 an auxin receptor yet? Mol Plant 4:635–640PubMedPubMedCentralCrossRefGoogle Scholar
  120. 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):2578–2595PubMedPubMedCentralCrossRefGoogle Scholar
  121. Shinozaki K, Yamaguchi-Shinozaki K (2007) Gene networks involved in drought stress response and tolerance. J Exp Bot 58:221–227PubMedCrossRefGoogle Scholar
  122. Singh RP, Jha PN (2017) The PGPR Stenotrophomonas maltophilia SBP-9 augments resistance against biotic and abiotic stress in wheat plants. Front Microbiol 8:1945PubMedPubMedCentralCrossRefGoogle Scholar
  123. 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 9:1277Google Scholar
  124. Smith DL, Subramanian S, Lamont JR, Bywater-Ekegärd M (2015) Signaling in the phytomicrobiome: breadth and potential. Front Plant Sci 6:709PubMedPubMedCentralGoogle Scholar
  125. Spoel SH, Dong X (2008) Making sense of hormone crosstalk during plant immune responses. Cell Host Microbe 3:348–351PubMedCrossRefGoogle Scholar
  126. Sun TP, Gubler F (2004) Molecular mechanism of gibberellin signaling in plants. Annu Rev Plant Biol 55:197–223PubMedCrossRefGoogle Scholar
  127. 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 19:777PubMedPubMedCentralCrossRefGoogle Scholar
  128. Tabur S, Demir K (2010) Protective roles of exogenous polyamines on chromosomal aberrations in Hordeum vulgare exposed to salinity. Biologia 65:947–953CrossRefGoogle Scholar
  129. Tanaka Y, Sano T, Tamaoki M, Nakajima N, Kondo N, Hasezawa S (2005) Ethylene inhibits abscisic acid-induced stomatal closure in Arabidopsis. Plant Physiol 138:2337–2343PubMedPubMedCentralCrossRefGoogle Scholar
  130. 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 57:2259–2266PubMedCrossRefGoogle Scholar
  131. 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 7:847PubMedCrossRefGoogle Scholar
  132. Thaler JS, Humphrey PT, Whiteman NK (2012) Evolution of jasmonate and salicylate signal crosstalk. Trends Plant Sci 17:270PubMedCrossRefGoogle Scholar
  133. 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 38:333CrossRefGoogle Scholar
  134. 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 4:18Google Scholar
  135. 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 6:247PubMedPubMedCentralCrossRefGoogle Scholar
  136. Umamaheswari A, Nuni A, Shreevidya R (2010) Evaluation of antibacterial activity of Boerhaavia diffusa L. leaves. Int J Green Pharm (IJGP) 4(2)CrossRefGoogle Scholar
  137. Venkateswarlu B, Shanker AK (2009) Climate change and agriculture: adaptation and mitigation stategies. Indian J Agron 54(2):226Google Scholar
  138. 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 4:539PubMedPubMedCentralCrossRefGoogle Scholar
  139. 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 231:131–141PubMedCrossRefGoogle Scholar
  140. 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 54:269CrossRefGoogle Scholar
  141. Wani SH, Kumar V, Shriram V, Sah SK (2016) Phytohormones and their metabolic engineering for abiotic stress tolerance in crop plants. Crop J 4:162–176CrossRefGoogle Scholar
  142. Weiss D, Ori N (2007) Mechanisms of cross talk between gibberellin and other hormones. Plant Physiol 144:1240–1246PubMedPubMedCentralCrossRefGoogle Scholar
  143. Wolbang CM, Ross JJ (2001) Auxin promotes gibberellin biosynthesis in decapitated tobacco plants. Planta 214:153–157PubMedCrossRefGoogle Scholar
  144. Wolters H, Jürgens G (2009) Survival of the flexible: hormonal growth control and adaptation in plant development. Nat Rev Gen 10:305CrossRefGoogle Scholar
  145. 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 277:8596PubMedCrossRefGoogle Scholar
  146. 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 26:1621–1631CrossRefGoogle Scholar
  147. Yang J, Kloepper JW, Ryu CM (2009) Rhizosphere bacteria help plants tolerate abiotic stress. Trends Plant Sci 14(1):1–4PubMedCrossRefGoogle Scholar
  148. 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 233:219–229PubMedCrossRefGoogle Scholar
  149. 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:E1200PubMedCrossRefGoogle Scholar
  150. 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 10:1036PubMedPubMedCentralCrossRefGoogle Scholar
  151. 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 126:103–108CrossRefGoogle Scholar
  152. 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 27:122PubMedCrossRefGoogle Scholar
  153. 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):e0152927CrossRefGoogle Scholar
  154. 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 11:138PubMedPubMedCentralCrossRefGoogle Scholar
  155. 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):557–565PubMedCrossRefPubMedCentralGoogle Scholar

Copyright information

© Springer Nature B.V. 2020

Authors and Affiliations

  • Naeem Khan
    • 1
    Email author
  • Asghari Bano
    • 2
  • Shahid Ali
    • 3
  • Md. Ali Babar
    • 1
  1. 1.Department of AgronomyUniversity of FloridaGainesvilleUSA
  2. 2.Department of BioscienceUniversity of WahWah CanttPakistan
  3. 3.Plant Epigenetic and DevelopmentNortheast Forestry University HarbinHarbinChina

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