1932

Abstract

Studies with model plants such as have revealed that phytohormones are central regulators of plant defense. The intricate network of phytohormone signaling pathways enables plants to activate appropriate and effective defense responses against pathogens as well as to balance defense and growth. The timing of the evolution of most phytohormone signaling pathways seems to coincide with the colonization of land, a likely requirement for plant adaptations to the more variable terrestrial environments, which included the presence of pathogens. In this review, we explore the evolution of defense hormone signaling networks by combining the model plant-based knowledge about molecular components mediating phytohormone signaling and cross talk with available genome information of other plant species. We highlight conserved hubs in hormone cross talk and discuss evolutionary advantages of defense hormone cross talk. Finally, we examine possibilities of engineering hormone cross talk for improvement of plant fitness and crop production.

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An erratum has been published for this article:
Erratum: Evolution of Hormone Signaling Networks in Plant Defense
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2017-08-04
2024-12-04
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Literature Cited

  1. Albrecht T, Argueso CT. 1.  2016. Should I fight or should I grow now? The role of cytokinins in plant growth and immunity and in the growth–defence trade-off. Ann. Bot. 119:5725–35 [Google Scholar]
  2. Aleman F, Yazaki J, Lee M, Takahashi Y, Kim AY. 2.  et al. 2016. An ABA-increased interaction of the PYL6 ABA receptor with MYC2 transcription factor: a putative link of ABA and JA signaling. Sci. Rep. 6:28941 [Google Scholar]
  3. Alvarez A, Montesano M, Schmelz E, de Leon IP. 3.  2016. Activation of shikimate, phenylpropanoid, oxylipins, and auxin pathways in Pectobacterium carotovorum elicitors-treated moss. Front. Plant Sci. 7:328 [Google Scholar]
  4. Anderson JP, Badruzsaufari E, Schenk PM, Manners JM, Desmond OJ. 4.  et al. 2004. Antagonistic interaction between abscisic acid and jasmonate-ethylene signaling pathways modulates defense gene expression and disease resistance in Arabidopsis. . Plant Cell 16:3460–79 [Google Scholar]
  5. Andersson RA, Akita M, Pirhonen M, Gammelgård E, Valkonen JPT. 5.  2005. Moss-Erwinia pathosystem reveals possible similarities in pathogenesis and pathogen defense in vascular and nonvascular plants. J. Gen. Plant Pathol. 71:23–28 [Google Scholar]
  6. Argueso CT, Ferreira FJ, Epple P, To JPC, Hutchison CE. 6.  et al. 2012. Two-component elements mediate interactions between cytokinin and salicylic acid in plant immunity. PLOS Genet 8:e1002448 [Google Scholar]
  7. Assante G, Merlini L, Nasini G. 7.  1977. (+)-Abscisic acid, a metabolite of the fungus Cercospora rosicola. . Experientia 33:1556–57 [Google Scholar]
  8. Atkinson NJ, Lilley CJ, Urwin PE. 8.  2013. Identification of genes involved in the response of Arabidopsis to simultaneous biotic and abiotic stresses. Plant Physiol 162:2028–41 [Google Scholar]
  9. Audenaert K, De Meyer GB, Hofte MM. 9.  2002. Abscisic acid determines basal susceptibility of tomato to Botrytis cinerea and suppresses salicylic acid–dependent signaling mechanisms. Plant Physiol 128:491–501 [Google Scholar]
  10. Beckman KB, Ingram DS. 10.  1994. The inhibition of the hypersensitive response of potato-tuber tissues by cytokinins: similarities between senescence and plant defense responses. Physiol. Mol. Plant Pathol. 44:33–50 [Google Scholar]
  11. Berlanger I, Powelson ML. 10a.  2000. Verticillium wilt. Plant Health Instr https://doi.org/10.1094/PHI-I-2000-0801-01 [Crossref] [Google Scholar]
  12. Boller T, Felix G. 11.  2009. A renaissance of elicitors: perception of microbe-associated molecular patterns and danger signals by pattern-recognition receptors. Annu. Rev. Plant Biol. 60:379–406 [Google Scholar]
  13. Bomblies K, Weigel D. 12.  2007. Hybrid necrosis: autoimmunity as a potential gene-flow barrier in plant species. Nat. Rev. Genet. 8:382–93 [Google Scholar]
  14. Boter M, Ruiz-Rivero O, Abdeen A, Prat S. 13.  2004. Conserved MYC transcription factors play a key role in jasmonate signaling both in tomato and Arabidopsis. Gene Dev 18:1577–91 [Google Scholar]
  15. Bressendorff S, Azevedo R, Kenchappa CS, Ponce de Leon I, Olsen JV. 14.  et al. 2016. An innate immunity pathway in the moss Physcomitrella patens. Plant Cell 28:1328–42 [Google Scholar]
  16. Bruggeman Q, Raynaud C, Benhamed M, Delarue M. 15.  2015. To die or not to die? Lessons from lesion mimic mutants. Front. Plant Sci. 6:24 [Google Scholar]
  17. Burra DD, Mühlenbock P, Andreasson E. 16.  2015. Salicylic and jasmonic acid pathways are necessary for defence against Dickeya solani as revealed by a novel method for Blackleg disease screening of in vitro grown potato. Plant Biol 17:1030–38 [Google Scholar]
  18. Cai Q, Yuan Z, Chen MJ, Yin CS, Luo ZJ. 17.  et al. 2014. Jasmonic acid regulates spikelet development in rice. Nat. Commun. 5:3476 [Google Scholar]
  19. Campos ML, Yoshida Y, Major IT, de Oliveira Ferreira D, Weraduwage SM. 18.  et al. 2016. Rewiring of jasmonate and phytochrome B signalling uncouples plant growth-defense tradeoffs. Nat. Commun. 7:12570 [Google Scholar]
  20. Catinot J, Buchala A, Abou-Mansour E, Metraux JP. 19.  2008. Salicylic acid production in response to biotic and abiotic stress depends on isochorismate in Nicotiana benthamiana. . FEBS Lett. 582:473–78 [Google Scholar]
  21. Chater C, Kamisugi Y, Movahedi M, Fleming A, Cuming AC. 20.  et al. 2011. Regulatory mechanism controlling stomatal behavior conserved across 400 million years of land plant evolution. Curr. Biol. 21:1025–29 [Google Scholar]
  22. Chen HM, Xue L, Chintamanani S, Germain H, Lin HQ. 21.  et al. 2009. ETHYLENE INSENSITIVE3 and ETHYLENE INSENSITIVE3-LIKE1 repress SALICYLIC ACID INDUCTION DEFICIENT2 expression to negatively regulate plant innate immunity in Arabidopsis. . Plant Cell 21:2527–40 [Google Scholar]
  23. Chen R, Jiang HL, Li L, Zhai QZ, Qi LL. 22.  et al. 2012. The Arabidopsis mediator subunit MED25 differentially regulates jasmonate and abscisic acid signaling through interacting with the MYC2 and ABI5 transcription factors. Plant Cell 24:2898–916 [Google Scholar]
  24. Chen X, Steed A, Travella S, Keller B, Nicholson P. 23.  2009. Fusarium graminearum exploits ethylene signalling to colonize dicotyledonous and monocotyledonous plants. New Phytol 182:975–83 [Google Scholar]
  25. Chen Y, Shen H, Wang MY, Li Q, He ZH. 24.  2013. Salicyloyl-aspartate synthesized by the acetyl-amido synthetase GH3.5 is a potential activator of plant immunity in Arabidopsis. . Acta Biochim. Biophys. Sin. 45:827–36 [Google Scholar]
  26. Cheon J, Fujioka S, Dilkes BP, Choe S. 25.  2013. Brassinosteroids regulate plant growth through distinct signaling pathways in Selaginella and Arabidopsis. . PLOS ONE 8:e81938 [Google Scholar]
  27. Choi J, Huh SU, Kojima M, Sakakibara H, Paek KH, Hwang I. 26.  2010. The cytokinin-activated transcription factor ARR2 promotes plant immunity via TGA3/NPR1-dependent salicylic acid signaling in Arabidopsis. Dev. Cell 19:284–95 [Google Scholar]
  28. Chono M, Honda I, Zeniya H, Yoneyama K, Saisho D. 27.  et al. 2003. A semidwarf phenotype of barley uzu results from a nucleotide substitution in the gene encoding a putative brassinosteroid receptor. Plant Physiol 133:1209–19 [Google Scholar]
  29. Chung SH, Rosa C, Scully ED, Peiffer M, Tooker JF. 28.  et al. 2013. Herbivore exploits orally secreted bacteria to suppress plant defenses. PNAS 110:15728–33 [Google Scholar]
  30. Cook DE, Mesarich CH, Thomma BPHJ. 29.  2015. Understanding plant immunity as a surveillance system to detect invasion. Annu. Rev. Phytopathol. 53:541–63 [Google Scholar]
  31. Cui HT, Tsuda K, Parker JE. 30.  2015. Effector-triggered immunity: from pathogen perception to robust defense. Annu. Rev. Plant Biol. 66:487–511 [Google Scholar]
  32. Cuming AC, Stevenson SR. 31.  2015. From pond slime to rain forest: the evolution of ABA signalling and the acquisition of dehydration tolerance. New Phytol 206:5–7 [Google Scholar]
  33. De Bruyne L, Hofte M, De Vleesschauwer D. 32.  2014. Connecting growth and defense: the emerging roles of brassinosteroids and gibberellins in plant innate immunity. Mol. Plant 7:943–59 [Google Scholar]
  34. Delaguardia M, Benlloch M. 33.  1980. Effects of potassium and gibberellic acid on stem growth of whole sunflower plants. Physiol. Plant. 49:443–48 [Google Scholar]
  35. de Leon IP, Montesano M. 34.  2013. Activation of defense mechanisms against pathogens in mosses and flowering plants. Int. J. Mol. Sci. 14:3178–200 [Google Scholar]
  36. Dempsey DA, Vlot AC, Wildermuth MC, Klessig DF. 35.  2011. Salicylic acid biosynthesis and metabolism. Arabidopsis Book 9:e0156 [Google Scholar]
  37. Denoux C, Galletti R, Mammarella N, Gopalan S, Werck D. 36.  et al. 2008. Activation of defense response pathways by OGs and Flg22 elicitors in Arabidopsis seedlings. Mol. Plant 1:423–45 [Google Scholar]
  38. Depuydt S, Hardtke CS. 37.  2011. Hormone signalling crosstalk in plant growth regulation. Curr. Biol. 21:R365–73 [Google Scholar]
  39. de Torres Zabala M, Zhai B, Jayaraman S, Eleftheriadou G, Winsbury R. 38.  et al. 2016. Novel JAZ co-operativity and unexpected JA dynamics underpin Arabidopsis defence responses to Pseudomonas syringae infection. New Phytol 209:1120–34 [Google Scholar]
  40. De Vleesschauwer D, Seifi HS, Filipe O, Haeck A, Huu SN. 39.  et al. 2016. The DELLA protein SLR1 integrates and amplifies salicylic acid– and jasmonic acid–dependent innate immunity in rice. Plant Physiol 170:1831–47 [Google Scholar]
  41. De Vleesschauwer D, Van Buyten E, Satoh K, Balidion J, Mauleon R. 40.  et al. 2012. Brassinosteroids antagonize gibberellin- and salicylate-mediated root immunity in rice. Plant Physiol 158:1833–46 [Google Scholar]
  42. De Vleesschauwer D, Yang Y, Cruz CV, Hofte M. 41.  2010. Abscisic acid–induced resistance against the brown spot pathogen Cochliobolus miyabeanus in rice involves MAP kinase-mediated repression of ethylene signaling. Plant Physiol 152:2036–52 [Google Scholar]
  43. Diezel C, von Dahl CC, Gaquerel E, Baldwin IT. 42.  2009. Different lepidopteran elicitors account for cross-talk in herbivory-induced phytohormone signaling. Plant Physiol 150:1576–86 [Google Scholar]
  44. Ding X, Cao Y, Huang L, Zhao J, Xu C. 43.  et al. 2008. Activation of the indole-3-acetic acid-amido synthetase GH3-8 suppresses expansin expression and promotes salicylate- and jasmonate-independent basal immunity in rice. Plant Cell 20:228–40 [Google Scholar]
  45. Ding Y, Wei W, Wu W, Davis RE, Jiang Y. 44.  et al. 2013. Role of gibberellic acid in tomato defence against potato purple top phytoplasma infection. Ann. Appl. Biol. 162:191–99 [Google Scholar]
  46. Ding YZ, Dommel M, Mou ZL. 45.  2016. Abscisic acid promotes proteasome-mediated degradation of the transcription coactivator NPR1 in Arabidopsis thaliana. . Plant J. 86:20–34 [Google Scholar]
  47. Djamei A, Schipper K, Rabe F, Ghosh A, Vincon V. 46.  et al. 2011. Metabolic priming by a secreted fungal effector. Nature 478:395–98 [Google Scholar]
  48. Dobzhansky T. 47.  1937. Genetics and the Origin of Species New York: Columbia Univ. Press [Google Scholar]
  49. Du MM, Zhai QZ, Deng L, Li SY, Li HS. 48.  et al. 2014. Closely related NAC transcription factors of tomato differentially regulate stomatal closure and reopening during pathogen attack. Plant Cell 26:3167–84 [Google Scholar]
  50. Ekengren SK, Liu YL, Schiff M, Dinesh-Kumar SP, Martin GB. 49.  2003. Two MAPK cascades, NPR1, and TGA transcription factors play a role in Pto-mediated disease resistance in tomato. Plant J 36:905–17 [Google Scholar]
  51. Fan M, Bai MY, Kim JG, Wang TN, Oh E. 50.  et al. 2014. The bHLH transcription factor HBI1 mediates the trade-off between growth and pathogen-associated molecular pattern-triggered immunity in Arabidopsis. . Plant Cell 26:828–41 [Google Scholar]
  52. Feng SG, Yue RQ, Tao S, Yang YJ, Zhang L. 51.  et al. 2015. Genome-wide identification, expression analysis of auxin-responsive GH3 family genes in maize (Zea mays L.) under abiotic stresses. J. Integr. Plant Biol. 57:783–95 [Google Scholar]
  53. Fu J, Liu HB, Li Y, Yu HH, Li XH. 52.  et al. 2011. Manipulating broad-spectrum disease resistance by suppressing pathogen-induced auxin accumulation in rice. Plant Physiol 155:589–602 [Google Scholar]
  54. Fu J, Wang SP. 53.  2011. Insights into auxin signaling in plant-pathogen interactions. Front. Plant Sci. 2:74 [Google Scholar]
  55. Fu ZQ, Yan SP, Saleh A, Wang W, Ruble J. 54.  et al. 2012. NPR3 and NPR4 are receptors for the immune signal salicylic acid in plants. Nature 486:228–32 [Google Scholar]
  56. Gaige AR, Ayella A, Shuai B. 55.  2010. Methyl jasmonate and ethylene induce partial resistance in Medicagotruncatula against the charcoal rot pathogen Macrophomina phaseolina. . Physiol. Mol. Plant Pathol. 74:412–18 [Google Scholar]
  57. Glazebrook J. 56.  2005. Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. Annu. Rev. Phytopathol. 43:205–27 [Google Scholar]
  58. Gong T, Shu D, Zhao M, Zhong J, Deng HY, Tan H. 57.  2014. Isolation of genes related to abscisic acid production in Botrytis cinerea TB-3-H8 by cDNA-AFLP. J. Basic Microb. 54:204–14 [Google Scholar]
  59. Goodstein DM, Shu SQ, Howson R, Neupane R, Hayes RD. 58.  et al. 2012. Phytozome: a comparative platform for green plant genomics. Nucleic Acids Res 40:D1178–86 [Google Scholar]
  60. Grellet-Bournonville CF, Martinez-Zamora MG, Castagnaro AP, Díaz-Ricci JC. 59.  2012. Temporal accumulation of salicylic acid activates the defense response against Colletotrichum in strawberry. Plant Physiol. Biochem. 54:10–16 [Google Scholar]
  61. Gross J, Cho WK, Lezhneva L, Falk J, Krupinska K. 60.  et al. 2006. A plant locus essential for phylloquinone (vitamin K1) biosynthesis originated from a fusion of four eubacterial genes. J. Biol. Chem. 281:17189–96 [Google Scholar]
  62. Grosskinsky DK, Naseem M, Abdelmohsen UR, Plickert N, Engelke T. 61.  et al. 2011. Cytokinins mediate resistance against Pseudomonas syringae in tobacco through increased antimicrobial phytoalexin synthesis independent of salicylic acid signaling. Plant Physiol 157:815–30 [Google Scholar]
  63. Gu YN, Zebell SG, Liang ZZ, Wang S, Kang BH, Dong XN. 62.  2016. Nuclear pore permeabilization is a convergent signaling event in effector-triggered immunity. Cell 166:1526–38 [Google Scholar]
  64. Haberlach GT, Budde AD, Sequeira L, Helgeson JP. 63.  1978. Modification of disease resistance of tobacco callus tissues by cytokinins. Plant Physiol 62:522–25 [Google Scholar]
  65. Halim VA, Eschen-Lippold L, Altmann S, Birschwilks M, Scheel D, Rosahl S. 64.  2007. Salicylic acid is important for basal defense of Solanumtuberosum against Phytophthora infestans. . Mol. Plant-Microbe Interact. 20:1346–52 [Google Scholar]
  66. Hayashi K, Horie K, Hiwatashi Y, Kawaide H, Yamaguchi S. 65.  et al. 2010. Endogenous diterpenes derived from ent-kaurene, a common gibberellin precursor, regulate protonema differentiation of the moss Physcomitrella patens. Plant Physiol 153:1085–97 [Google Scholar]
  67. Hedden P, Phillips AL. 66.  2000. Gibberellin metabolism: new insights revealed by the genes. Trends Plant Sci 5:523–30 [Google Scholar]
  68. Heijari J, Nerg AM, Kainulainen P, Viiri H, Vuorinen M, Holopainen JK. 67.  2005. Application of methyl jasmonate reduces growth but increases chemical defence and resistance against Hylobius abietis in Scots pine seedlings. Entomol. Exp. Appl. 115:117–24 [Google Scholar]
  69. Heinrich M, Hettenhausen C, Lange T, Wunsche H, Fang JJ. 68.  et al. 2013. High levels of jasmonic acid antagonize the biosynthesis of gibberellins and inhibit the growth of Nicotiana attenuata stems. Plant J 73:591–606 [Google Scholar]
  70. Helliwell EE, Wang Q, Yang YN. 69.  2013. Transgenic rice with inducible ethylene production exhibits broad-spectrum disease resistance to the fungal pathogens Magnaporthe oryzae and Rhizoctonia solani. Plant Biotechnol. J 11:33–42 [Google Scholar]
  71. Hirano K, Nakajima M, Asano K, Nishiyama T, Sakakibara H. 70.  et al. 2007. The GID1-mediated gibberellin perception mechanism is conserved in the lycophyte Selaginella moellendorffii but not in the bryophyte Physcomitrella patens. . Plant Cell 19:3058–79 [Google Scholar]
  72. Hoffman T, Schmidt JS, Zheng X, Bent AF. 71.  1999. Isolation of ethylene-insensitive soybean mutants that are altered in pathogen susceptibility and gene-for-gene disease resistance. Plant Physiol 119:935–50 [Google Scholar]
  73. Hoffmannbenning S, Kende H. 72.  1992. On the role of abscisic acid and gibberellin in the regulation of growth in rice. Plant Physiol 99:1156–61 [Google Scholar]
  74. Hok S, Allasia V, Andrio E, Naessens E, Ribes E. 73.  et al. 2014. The receptor kinase IMPAIRED OOMYCETE SUSCEPTIBILITY1 attenuates abscisic acid responses in Arabidopsis. . Plant Physiol. 166:1506–18 [Google Scholar]
  75. Hong GJ, Xue XY, Mao YB, Wang LJ, Chen XY. 74.  2012. Arabidopsis MYC2 interacts with DELLA proteins in regulating sesquiterpene synthase gene expression. Plant Cell 24:2635–48 [Google Scholar]
  76. Hou XL, Lee LYC, Xia KF, Yen YY, Yu H. 75.  2010. DELLAs modulate jasmonate signaling via competitive binding to JAZs. Dev. Cell 19:884–94 [Google Scholar]
  77. Howe GA, Jander G. 76.  2008. Plant immunity to insect herbivores. Annu. Rev. Plant Biol. 59:41–66 [Google Scholar]
  78. Huang JL, Gu M, Lai ZB, Fan BF, Shi K. 77.  et al. 2010. Functional analysis of the Arabidopsis PAL gene family in plant growth, development, and response to environmental stress. Plant Physiol 153:1526–38 [Google Scholar]
  79. 78.  Deleted in proof
  80. Ishikawa T, Okazaki K, Kuroda H, Itoh K, Mitsui T, Hori H. 79.  2007. Molecular cloning of Brassica rapa nitrilases and their expression during clubroot development. Mol. Plant Pathol. 8:623–37 [Google Scholar]
  81. Jiang CJ, Shimono M, Sugano S, Kojima M, Liu XQ. 80.  et al. 2013. Cytokinins act synergistically with salicylic acid to activate defense gene expression in rice. Mol. Plant-Microbe Interact. 26:287–96 [Google Scholar]
  82. Jones JDG, Dangl JL. 81.  2006. The plant immune system. Nature 444:323–29 [Google Scholar]
  83. Ju CL, Van de Poel B, Cooper ED, Thierer JH, Gibbons TR. 82.  et al. 2015. Conservation of ethylene as a plant hormone over 450 million years of evolution. Nat. Plants 1:14004 [Google Scholar]
  84. Kakei Y, Mochida K, Sakurai T, Yoshida T, Shinozaki K, Shimada Y. 83.  2015. Transcriptome analysis of hormone-induced gene expression in Brachypodium distachyon. Sci. Rep. 5:14476 [Google Scholar]
  85. Kazan K, Lyons R. 84.  2014. Intervention of phytohormone pathways by pathogen effectors. Plant Cell 26:2285–309 [Google Scholar]
  86. Kazan K, Manners JM. 85.  2013. MYC2: the master in action. Mol. Plant 6:686–703 [Google Scholar]
  87. Kim DS, Hwang BK. 86.  2014. An important role of the pepper phenylalanine ammonia-lyase gene (PAL1) in salicylic acid–dependent signalling of the defence response to microbial pathogens. J. Exp. Bot. 65:2295–306 [Google Scholar]
  88. Kissoudis C, Sri S, van de Wiel C, Visser RGF, van der Linden CG, Bai YL. 87.  2016. Responses to combined abiotic and biotic stress in tomato are governed by stress intensity and resistance mechanism. J. Exp. Bot. 67:5119–32 [Google Scholar]
  89. Kliebenstein DJ, Figuth A, Mitchell-Olds T. 88.  2002. Genetic architecture of plastic methyl jasmonate responses in Arabidopsis thaliana. Genetics 161:1685–96 [Google Scholar]
  90. Koga H, Dohi K, Mori M. 89.  2004. Abscisic acid and low temperatures suppress the whole plant-specific resistance reaction of rice plants to the infection of Magnaporthe grisea. . Physiol. Mol. Plant Pathol. 65:3–9 [Google Scholar]
  91. Koornneef A, Leon-Reyes A, Ritsema T, Verhage A, Den Otter FC. 90.  et al. 2008. Kinetics of salicylate-mediated suppression of jasmonate signaling reveal a role for redox modulation. Plant Physiol 147:1358–68 [Google Scholar]
  92. Kumar R, Agarwal P, Tyagi AK, Sharma AK. 91.  2012. Genome-wide investigation and expression analysis suggest diverse roles of auxin-responsive GH3 genes during development and response to different stimuli in tomato (Solanum lycopersicum). Mol. Genet. Genom 287:221–35 [Google Scholar]
  93. Kusajima M, Yasuda M, Kawashima A, Nojiri H, Yamane H. 92.  et al. 2010. Suppressive effect of abscisic acid on systemic acquired resistance in tobacco plants. J. Gen. Plant Pathol. 76:161–67 [Google Scholar]
  94. Lacombe S, Rougon-Cardoso A, Sherwood E, Peeters N, Dahlbeck D. 93.  et al. 2010. Interfamily transfer of a plant pattern-recognition receptor confers broad-spectrum bacterial resistance. Nat. Biotechnol. 28:365–69 [Google Scholar]
  95. Lahey KA, Yuan RC, Burns JK, Ueng PP, Timmer LW, Chung KR. 94.  2004. Induction of phytohormones and differential gene expression in citrus flowers infected by the fungus Colletotrichum acutatum. . Mol. Plant-Microbe Interact. 17:1394–401 [Google Scholar]
  96. Lavy M, Prigge MJ, Tao S, Shain S, Kuo A. 95.  et al. 2016. Constitutive auxin response in Physcomitrella reveals complex interactions between Aux/IAA and ARF proteins. eLife 5:e13325 [Google Scholar]
  97. Li J, Besseau S, Toronen P, Sipari N, Kollist H. 96.  et al. 2013. Defense-related transcription factors WRKY70 and WRKY54 modulate osmotic stress tolerance by regulating stomatal aperture in Arabidopsis. . New Phytol. 200:457–72 [Google Scholar]
  98. Li J, Brader G, Palva ET. 97.  2004. The WRKY70 transcription factor: a node of convergence for jasmonate-mediated and salicylate-mediated signals in plant defense. Plant Cell 16:319–31 [Google Scholar]
  99. Li YZ, Zhang L, Lu WJ, Wang XL, Wu CA, Guo XQ. 98.  2014. Overexpression of cotton GhMKK4 enhances disease susceptibility and affects abscisic acid, gibberellin and hydrogen peroxide signalling in transgenic Nicotiana benthamiana. Mol. Plant Pathol. 15:94–108 [Google Scholar]
  100. Lind C, Dreyer I, Lopez-Sanjurjo EJ, von Meyer K, Ishizaki K. 99.  et al. 2015. Stomatal guard cells co-opted an ancient ABA-dependent desiccation survival system to regulate stomatal closure. Curr. Biol. 25:928–35 [Google Scholar]
  101. Liu J, Zhang TR, Jia JZ, Sun JQ. 100.  2016. The wheat mediator subunit TaMED25 interacts with the transcription factor TaEIL1 to negatively regulate disease resistance against powdery mildew. Plant Physiol 170:1799–816 [Google Scholar]
  102. Liu TL, Song TQ, Zhang X, Yuan HB, Su LM. 101.  et al. 2014. Unconventionally secreted effectors of two filamentous pathogens target plant salicylate biosynthesis. Nat. Commun. 5:4686 [Google Scholar]
  103. Liu YD, Zhang SQ. 102.  2004. Phosphorylation of 1-aminocyclopropane-1-carboxylic acid synthase by MPK6, a stress-responsive mitogen-activated protein kinase, induces ethylene biosynthesis in Arabidopsis. . Plant Cell 16:3386–99 [Google Scholar]
  104. Liu ZJ, Bushnell WR. 103.  1986. Effects of cytokinins on fungus development and host response in powdery mildew of barley. Physiol. Mol. Plant Pathol. 29:41–52 [Google Scholar]
  105. Livne S, Lor VS, Nir I, Eliaz N, Aharoni A. 104.  et al. 2015. Uncovering DELLA-independent gibberellin responses by characterizing new tomato procera mutants. Plant Cell 27:1579–94 [Google Scholar]
  106. Lozano-Duran R, Macho AP, Boutrot F, Segonzac C, Somssich IE, Zipfel C. 105.  2013. The transcriptional regulator BZR1 mediates trade-off between plant innate immunity and growth. eLife 2:e00983 [Google Scholar]
  107. Ludwig-Muller J, Julke S, Bierfreund NM, Decker EL, Reski R. 106.  2009. Moss (Physcomitrella patens) GH3 proteins act in auxin homeostasis. New Phytol 181:323–38 [Google Scholar]
  108. Lund ST, Stall RE, Klee HJ. 107.  1998. Ethylene regulates the susceptible response to pathogen infection in tomato. Plant Cell 10:371–82 [Google Scholar]
  109. Ma KW, Ma WB. 108.  2016. Phytohormone pathways as targets of pathogens to facilitate infection. Plant Mol. Biol. 91:713–25 [Google Scholar]
  110. Ma X, Xu G, He P, Shan L. 109.  2016. SERKing coreceptors for receptors. Trends Plant Sci 21:1017–33 [Google Scholar]
  111. Makandar R, Nalam VJ, Lee H, Trick HN, Dong YH, Shah J. 110.  2012. Salicylic acid regulates basal resistance to Fusarium head blight in wheat. Mol. Plant-Microbe Interact. 25:431–49 [Google Scholar]
  112. McAdam SAM, Brodribb TJ, Banks JA, Hedrich R, Atallah NM. 111.  et al. 2016. Abscisic acid controlled sex before transpiration in vascular plants. PNAS 113:12862–67 [Google Scholar]
  113. McCune DC, Galston AW. 112.  1959. Inverse effects of gibberellin on peroxidase activity and growth in dwarf strains of peas and corn. Plant Physiol 34:416–18 [Google Scholar]
  114. Melotto M, Underwood W, He SY. 113.  2008. Role of stomata in plant innate immunity and foliar bacterial diseases. Annu. Rev. Phytopathol. 46:101–22 [Google Scholar]
  115. Melotto M, Underwood W, Koczan J, Nomura K, He SY. 114.  2006. Plant stomata function in innate immunity against bacterial invasion. Cell 126:969–80 [Google Scholar]
  116. Mine A, Nobori T, Salazar‐Rondon MC, Winkelmüller TM, Anver S. 115.  et al. 2017. An incoherent feed‐forward loop mediates robustness and tunability in a plant immune network. EMBO Rep 18:3464–76 [Google Scholar]
  117. Mittag J, Sola I, Rusak G, Ludwig-Muller J. 116.  2015. Physcomitrella patens auxin conjugate synthetase (GH3) double knockout mutants are more resistant to Pythium infection than wild type. J. Plant Physiol 183:75–83 [Google Scholar]
  118. Montes RAC, Rosas-Cardenas FD, De Paoli E, Accerbi M, Rymarquis LA. 117.  et al. 2014. Sample sequencing of vascular plants demonstrates widespread conservation and divergence of microRNAs. Nat. Commun. 5:3722 [Google Scholar]
  119. Mosher S, Moeder W, Nishimura N, Jikumaru Y, Joo SH. 118.  et al. 2010. The lesion-mimic mutant cpr22 shows alterations in abscisic acid signaling and abscisic acid insensitivity in a salicylic acid–dependent manner. Plant Physiol 152:1901–13 [Google Scholar]
  120. Muller H. 119.  1942. Isolating mechanisms, evolution, and temperature. Biol. Symp. 6:71–124 [Google Scholar]
  121. Mutka AM, Fawley S, Tsao T, Kunkel BN. 120.  2013. Auxin promotes susceptibility to Pseudomonas syringae via a mechanism independent of suppression of salicylic acid–mediated defenses. Plant J 74:746–54 [Google Scholar]
  122. Nakashima K, Takasaki H, Mizoi J, Shinozaki K, Yamaguchi-Shinozaki K. 121.  2012. NAC transcription factors in plant abiotic stress responses. Biochim. Biophys. Acta 1819:97–103 [Google Scholar]
  123. Navarro L, Bari R, Achard P, Lison P, Nemri A. 122.  et al. 2008. DELLAs control plant immune responses by modulating the balance and salicylic acid signaling. Curr. Biol. 18:650–55 [Google Scholar]
  124. Navarro L, Dunoyer P, Jay F, Arnold B, Dharmasiri N. 123.  et al. 2006. A plant miRNA contributes to antibacterial resistance by repressing auxin signaling. Science 312:436–39 [Google Scholar]
  125. Nuruzzaman M, Manimekalai R, Sharoni AM, Satoh K, Kondoh H. 124.  et al. 2010. Genome-wide analysis of NAC transcription factor family in rice. Gene 465:30–44 [Google Scholar]
  126. O'Donnell PJ, Schmelz E, Block A, Miersch O, Wasternack C. 125.  et al. 2003. Multiple hormones act sequentially to mediate a susceptible tomato pathogen defense response. Plant Physiol 133:1181–89 [Google Scholar]
  127. Okrent RA, Brooks MD, Wildermuth MC. 126.  2009. Arabidopsis GH3.12 (PBS3) conjugates amino acids to 4-substituted benzoates and is inhibited by salicylate. J. Biol. Chem. 284:9742–54 [Google Scholar]
  128. Okrent RA, Wildermuth MC. 127.  2011. Evolutionary history of the GH3 family of acyl adenylases in rosids. Plant Mol. Biol. 76:489–505 [Google Scholar]
  129. Olivas N, Kruijer W, Gort G, Wijen CL, van Loon J, Dicke M. 128.  2017. Genome-wide association analysis reveals distinct genetic architectures for single and combined stress responses in Arabidopsis thaliana. . New Phytol. 213:838–51 [Google Scholar]
  130. Olsen AN, Ernst HA, Lo Leggio L, Skriver K. 129.  2005. NAC transcription factors: structurally distinct, functionally diverse. Trends Plant Sci 10:79–87 [Google Scholar]
  131. Ostrowski M, Jakubowska A. 130.  2013. GH3 expression and IAA-amide synthetase activity in pea (Pisum sativum L.) seedlings are regulated by light, plant hormones and auxinic herbicides. J. Plant Physiol. 170:361–68 [Google Scholar]
  132. Pallas JA, Paiva NL, Lamb C, Dixon RA. 131.  1996. Tobacco plants epigenetically suppressed in phenylalanine ammonia–lyase expression do not develop systemic acquired resistance in response to infection by tobacco mosaic virus. Plant J 10:281–93 [Google Scholar]
  133. Park JE, Park JY, Kim YS, Staswick PE, Jeon J. 132.  et al. 2007. GH3-mediated auxin homeostasis links growth regulation with stress adaptation response in Arabidopsis. J. Biol. Chem. 282:10036–46 [Google Scholar]
  134. Pascual MB, Canovas FM, Avila C. 133.  2015. The NAC transcription factor family in maritime pine (Pinus pinaster): molecular regulation of two genes involved in stress responses. BMC Plant Biol 15:254 [Google Scholar]
  135. Pieterse CM, Leon-Reyes A, Van der Ent S, Van Wees SC. 134.  2009. Networking by small-molecule hormones in plant immunity. Nat. Chem. Biol. 5:308–16 [Google Scholar]
  136. Pinheiro GL, Marques CS, Costa MDBL, Reis PAB, Alves MS. 135.  et al. 2009. Complete inventory of soybean NAC transcription factors: sequence conservation and expression analysis uncover their distinct roles in stress response. Gene 444:10–23 [Google Scholar]
  137. Pinweha N, Asvarak T, Viboonjun U, Narangajavana J. 136.  2015. Involvement of miR160/miR393 and their targets in cassava responses to anthracnose disease. J. Plant Physiol. 174:26–35 [Google Scholar]
  138. Ponce De Leon I, Schmelz EA, Gaggero C, Castro A, Alvarez A, Montesano M. 137.  2012. Physcomitrella patens activates reinforcement of the cell wall, programmed cell death and accumulation of evolutionary conserved defence signals, such as salicylic acid and 12-oxo-phytodienoic acid, but not jasmonic acid, upon Botrytis cinerea infection. Mol. Plant Pathol 13:960–74 [Google Scholar]
  139. Pye MF, Hakuno F, MacDonald JD, Bostock RM. 138.  2013. Induced resistance in tomato by SAR activators during predisposing salinity stress. Front. Plant Sci. 4:116 [Google Scholar]
  140. Qiu DY, Xiao J, Ding XH, Xiong M, Cai M. 139.  et al. 2007. OsWRKY13 mediates rice disease resistance by regulating defense-related genes in salicylate- and jasmonate-dependent signaling. Mol. Plant-Microbe Interact. 20:492–99 [Google Scholar]
  141. Radhika V, Kost C, Bonaventure G, David A, Boland W. 140.  2012. Volatile emission in bracken fern is induced by jasmonates but not by Spodoptera littoralis or strongylogaster multifasciata herbivory. PLOS ONE 7:e48050 [Google Scholar]
  142. Rao MV, Lee H, Creelman RA, Mullet JE, Davis KR. 141.  2000. Jasmonic acid signaling modulates ozone-induced hypersensitive cell death. Plant Cell 12:1633–46 [Google Scholar]
  143. Rasmussen S, Barah P, Suarez-Rodriguez MC, Bressendorff S, Friis P. 142.  et al. 2013. Transcriptome responses to combinations of stresses in Arabidopsis. . Plant Physiol. 161:1783–94 [Google Scholar]
  144. Riemann M, Muller A, Korte A, Furuya M, Weiler EW, Nick P. 143.  2003. Impaired induction of the jasmonate pathway in the rice mutant hebiba. Plant Physiol 133:1820–30 [Google Scholar]
  145. Robert-Seilaniantz A, Grant M, Jones JDG. 144.  2011. Hormone crosstalk in plant disease and defense: more than just jasmonate-salicylate antagonism. Annu. Rev. Phytopathol. 49:317–43 [Google Scholar]
  146. Ross JJ, Reid JB. 145.  2010. Evolution of growth-promoting plant hormones. Funct. Plant Biol. 37:795–805 [Google Scholar]
  147. Schmiesing A, Emonet A, Gouhier-Darimont C, Reymond P. 146.  2016. Arabidopsis MYC transcription factors are the target of hormonal salicylic acid/jasmonic acid cross talk in response to Pieris brassicae egg extract. Plant Physiol 170:2432–43 [Google Scholar]
  148. Seyfferth C, Tsuda K. 147.  2014. Salicylic acid signal transduction: the initiation of biosynthesis, perception and transcriptional reprogramming. Front. Plant Sci. 5:697 [Google Scholar]
  149. Sheikh AH, Raghuram B, Eschen-Lippold L, Scheel D, Lee J, Sinha AK. 148.  2014. Agroinfiltration by cytokinin-producing Agrobacterium sp. strain GV3101 primes defense responses in Nicotiana tabacum. . Mol. Plant-Microbe Interact. 27:1175–85 [Google Scholar]
  150. Shen XL, Liu HB, Yuan B, Li XH, Xu CG, Wang SP. 149.  2011. OsEDR1 negatively regulates rice bacterial resistance via activation of ethylene biosynthesis. Plant Cell Environ 34:179–91 [Google Scholar]
  151. Shibata Y, Kawakita K, Takemoto D. 150.  2010. Age-related resistance of Nicotiana benthamiana against hemibiotrophic pathogen Phytophthora infestans requires both ethylene- and salicylic acid–mediated signaling pathways. Mol. Plant-Microbe Interact 23:1130–42 [Google Scholar]
  152. Shigenaga AM, Argueso CT. 151.  2016. No hormone to rule them all: interactions of plant hormones during the responses of plants to pathogens. Semin. Cell Dev. Biol. 56:174–89 [Google Scholar]
  153. Shine MB, Yang JW, El-Habbak M, Nagyabhyru P, Fu DQ. 152.  et al. 2016. Cooperative functioning between phenylalanine ammonia lyase and isochorismate synthase activities contributes to salicylic acid biosynthesis in soybean. New Phytol 212:627–36 [Google Scholar]
  154. Shoji T, Hashimoto T. 153.  2011. Tobacco MYC2 regulates jasmonate-inducible nicotine biosynthesis genes directly and by way of the NIC2-locus ERF genes. Plant Cell Physiol 52:1117–30 [Google Scholar]
  155. Smith-Becker J, Marois E, Huguet EJ, Midland SL, Sims JJ, Keen NT. 154.  1998. Accumulation of salicylic acid and 4-hydroxybenzoic acid in phloem fluids of cucumber during systemic acquired resistance is preceded by a transient increase in phenylalanine ammonia-lyase activity in petioles and stems. Plant Physiol 116:231–38 [Google Scholar]
  156. Spaepen S, Vanderleyden J. 155.  2011. Auxin and plant-microbe interactions. Cold Spring Harb. Perspect. Biol. 3:a001438 [Google Scholar]
  157. Spoel SH, Johnson JS, Dong X. 156.  2007. Regulation of tradeoffs between plant defenses against pathogens with different lifestyles. PNAS 104:18842–47 [Google Scholar]
  158. Staswick PE, Tiryaki I, Rowe ML. 157.  2002. Jasmonate response locus JAR1 and several related Arabidopsis genes encode enzymes of the firefly luciferase superfamily that show activity on jasmonic, salicylic, and indole-3-acetic acids in an assay for adenylation. Plant Cell 14:1405–15 [Google Scholar]
  159. Stintzi A, Browse J. 158.  2000. The Arabidopsis male-sterile mutant, opr3, lacks the 12-oxophytodienoic acid reductase required for jasmonate synthesis. PNAS 97:10625–30 [Google Scholar]
  160. Strange RN, Scott PR. 159.  2005. Plant disease: a threat to global food security. Annu. Rev. Phytopathol. 43:83–116 [Google Scholar]
  161. Strawn MA, Marr SK, Inoue K, Inada N, Zubieta C, Wildermuth MC. 160.  2007. Arabidopsis isochorismate synthase functional in pathogen-induced salicylate biosynthesis exhibits properties consistent with a role in diverse stress responses. J. Biol. Chem. 282:5919–33 [Google Scholar]
  162. Stumpe M, Gobel C, Faltin B, Beike AK, Hause B. 161.  et al. 2010. The moss Physcomitrella patens contains cyclopentenones but no jasmonates: mutations in allene oxide cyclase lead to reduced fertility and altered sporophyte morphology. New Phytol 188:740–49 [Google Scholar]
  163. Sugano S, Sugimoto T, Takatsuji H, Jiang CJ. 162.  2013. Induction of resistance to Phytophthora sojae in soyabean (Glycine max) by salicylic acid and ethylene. Plant Pathol 62:1048–56 [Google Scholar]
  164. Sunkar R, Zhu JK. 163.  2004. Novel and stress-regulated microRNAs and other small RNAs from Arabidopsis. . Plant Cell 16:2001–19 [Google Scholar]
  165. Taheri P, Tarighi S. 164.  2010. Riboflavin induces resistance in rice against Rhizoctonia solani via jasmonate-mediated priming of phenylpropanoid pathway. J. Plant Physiol. 167:201–8 [Google Scholar]
  166. Takasaki H, Maruyama K, Takahashi F, Fujita M, Yoshida T. 165.  et al. 2015. SNAC-As, stress-responsive NAC transcription factors, mediate ABA-inducible leaf senescence. Plant J 84:1114–23 [Google Scholar]
  167. Takezawa D, Watanabe N, Ghosh TK, Saruhashi M, Suzuki A. 166.  et al. 2015. Epoxycarotenoid-mediated synthesis of abscisic acid in Physcomitrella patens implicating conserved mechanisms for acclimation to hyperosmosis in embryophytes. New Phytol 206:209–19 [Google Scholar]
  168. Terol J, Domingo C, Talon M. 167.  2006. The GH3 family in plants: genome wide analysis in rice and evolutionary history based on EST analysis. Gene 371:279–90 [Google Scholar]
  169. Thaler JS, Humphrey PT, Whiteman NK. 168.  2012. Evolution of jasmonate and salicylate signal crosstalk. Trends Plant Sci 17:260–70 [Google Scholar]
  170. Thines B, Katsir L, Melotto M, Niu Y, Mandaokar A. 169.  et al. 2007. JAZ repressor proteins are targets of the SCF(COI1) complex during jasmonate signalling. Nature 448:661–65 [Google Scholar]
  171. Tintor N, Ross A, Kanehara K, Yamada K, Fan L. 170.  et al. 2013. Layered pattern receptor signaling via ethylene and endogenous elicitor peptides during Arabidopsis immunity to bacterial infection. PNAS 110:6211–16 [Google Scholar]
  172. Tsuda K, Sato M, Stoddard T, Glazebrook J, Katagiri F. 171.  2009. Network properties of robust immunity in plants. PLOS Genet 5:e1000772 [Google Scholar]
  173. Ueno Y, Yoshida R, Kishi-Kaboshi M, Matsushita A, Jiang C-J. 172.  et al. 2015. Abiotic stresses antagonize the rice defence pathway through the tyrosine-dephosphorylation of OsMPK6. PLOS Pathog 11:e1005231 [Google Scholar]
  174. Ulferts S, Delventhal R, Splivallo R, Karlovsky P, Schaffrath U. 173.  2015. Abscisic acid negatively interferes with basal defence of barley against Magnaporthe oryzae. . BMC Plant Biol. 15:7 [Google Scholar]
  175. Uppalapati SR, Ishiga Y, Wangdi T, Kunkel BN, Anand A. 174.  et al. 2007. The phytotoxin coronatine contributes to pathogen fitness and is required for suppression of salicylic acid accumulation in tomato inoculated with Pseudomonas syringae pv. tomato DC3000. Mol. Plant-Microbe Interact 20:955–65 [Google Scholar]
  176. Van Den Boom CEM, Van Beek TA, Posthumus MA, De Groot A, Dicke M. 175.  2004. Qualitative and quantitative variation among volatile profiles induced by Tetranychus urticae feeding on plants from various families. J. Chem. Ecol. 30:69–89 [Google Scholar]
  177. van Leeuwen H, Kliebenstein DJ, West MAL, Kim K, van Poecke R. 176.  et al. 2007. Natural variation among Arabidopsis thaliana accessions for transcriptome response to exogenous salicylic acid. Plant Cell 19:2099–110 [Google Scholar]
  178. van Wersch R, Li X, Zhang YL. 177.  2016. Mighty dwarfs: Arabidopsis autoimmune mutants and their usages in genetic dissection of plant immunity. Front. Plant Sci. 7:1717 [Google Scholar]
  179. Vos IA, Moritz L, Pieterse CMJ, Van Wees SCM. 178.  2015. Impact of hormonal crosstalk on plant resistance and fitness under multi-attacker conditions. Front. Plant Sci. 6:639 [Google Scholar]
  180. Vriet C, Lemmens K, Vandepoele K, Reuzeau C, Russinova E. 179.  2015. Evolutionary trails of plant steroid genes. Trends Plant Sci 20:301–8 [Google Scholar]
  181. Wang CY, Liu Y, Li SS, Han GZ. 180.  2015. Insights into the origin and evolution of the plant hormone signaling machinery. Plant Physiol 167:872–86 [Google Scholar]
  182. Wang D, Pajerowska-Mukhtar K, Culler AH, Dong XN. 181.  2007. Salicylic acid inhibits pathogen growth in plants through repression of the auxin signaling pathway. Curr. Biol. 17:1784–90 [Google Scholar]
  183. Wang H, Mao HL. 182.  2014. On the origin and evolution of plant brassinosteroid receptor kinases. J. Mol. Evol. 78:118–29 [Google Scholar]
  184. Wang HH, Wijeratne A, Wijeratne S, Lee S, Taylor CG. 183.  et al. 2012. Dissection of two soybean QTL conferring partial resistance to Phytophthora sojae through sequence and gene expression analysis. BMC Genom 13:428 [Google Scholar]
  185. Ward EWB, Cahill DM, Bhattacharyya MK. 184.  1989. Abscisic acid suppression of phenylalanine ammonia-lyase activity and mRNA, and resistance of soybeans to Phytophthora megasperma f. sp. glycinea. Plant Physiol 91:23–27 [Google Scholar]
  186. Wasternack C, Hause B. 185.  2013. Jasmonates: biosynthesis, perception, signal transduction and action in plant stress response, growth and development. An update to the 2007 review in Annals of Botany . Ann. Bot 111:1021–58 [Google Scholar]
  187. Westfall CS, Sherp AM, Zubieta C, Alvarez S, Schraft E. 186.  et al. 2016. Arabidopsis thaliana GH3.5 acyl acid amido synthetase mediates metabolic crosstalk in auxin and salicylic acid homeostasis. PNAS 113:13917–22 [Google Scholar]
  188. Wildermuth MC, Dewdney J, Wu G, Ausubel FM. 187.  2001. Isochorismate synthase is required to synthesize salicylic acid for plant defence. Nature 414:562–65 [Google Scholar]
  189. Wolter M, Hollricher K, Salamini F, Schulze-Lefert P. 188.  1993. The MLO resistance alleles to powdery mildew infection in barley trigger a developmentally controlled defense mimic phenotype. Mol. Gen. Genet. 239:122–28 [Google Scholar]
  190. Wu Y, Zhang D, Chu JY, Boyle P, Wang Y. 189.  et al. 2012. The Arabidopsis NPR1 protein is a receptor for the plant defense hormone salicylic acid. Cell Rep 1:639–47 [Google Scholar]
  191. Xin XF, Nomura K, Aung K, Velasquez AC, Yao J. 190.  et al. 2016. Bacteria establish an aqueous living space in plants crucial for virulence. Nature 539:524–29 [Google Scholar]
  192. Xu MJ, Dong JF, Wang HZ, Huang LQ. 191.  2009. Complementary action of jasmonic acid on salicylic acid in mediating fungal elicitor-induced flavonol glycoside accumulation of Ginkgo biloba cells. Plant Cell Environ 32:960–67 [Google Scholar]
  193. Yan Y, Christensen S, Isakeit T, Engelberth J, Meeley R. 192.  et al. 2012. Disruption of OPR7 and OPR8 reveals the versatile functions of jasmonic acid in maize development and defense. Plant Cell 24:1420–36 [Google Scholar]
  194. Yang JW, Yi H-S, Kim H, Lee B, Lee S. 193.  et al. 2011. Whitefly infestation of pepper plants elicits defence responses against bacterial pathogens in leaves and roots and changes the below-ground microflora. J. Ecol. 99:46–56 [Google Scholar]
  195. Yang Y, Ou B, Zhang JZ, Si W, Gu HY. 194.  et al. 2014. The Arabidopsis Mediator subunit MED16 regulates iron homeostasis by associating with EIN3/EIL1 through subunit MED25. Plant J 77:838–51 [Google Scholar]
  196. Yang YJ, Yue RQ, Sun T, Zhang L, Chen W. 195.  et al. 2015. Genome-wide identification, expression analysis of GH3 family genes in Medicago truncatula under stress-related hormones and Sinorhizobium meliloti infection. Appl. Microbiol. Biot 99:841–54 [Google Scholar]
  197. Yasuda M, Ishikawa A, Jikumaru Y, Seki M, Umezawa T. 196.  et al. 2008. Antagonistic interaction between systemic acquired resistance and the abscisic acid–mediated abiotic stress response in Arabidopsis. . Plant Cell 20:1678–92 [Google Scholar]
  198. Yin C, Park JJ, Gang DR, Hulbert SH. 197.  2014. Characterization of a tryptophan 2-monooxygenase gene from Puccinia graminis f. sp. tritici involved in auxin biosynthesis and rust pathogenicity. Mol. Plant-Microbe Interact 27:227–35 [Google Scholar]
  199. Yuan YA, Chung JD, Fu XY, Johnson VE, Ranjan P. 198.  et al. 2009. Alternative splicing and gene duplication differentially shaped the regulation of isochorismate synthase in Populus and Arabidopsis. . PNAS 106:22020–25 [Google Scholar]
  200. Yuan YX, Zhong SH, Li Q, Zhu ZR, Lou YG. 199.  et al. 2007. Functional analysis of rice NPR1-like genes reveals that OsNPR1/NH1 is the rice orthologue conferring disease resistance with enhanced herbivore susceptibility. Plant Biotechnol. J. 5:313–24 [Google Scholar]
  201. Yue JP, Hu XY, Huang JL. 200.  2014. Origin of plant auxin biosynthesis. Trends Plant Sci 19:764–70 [Google Scholar]
  202. Zaveska Drabkova L, Dobrev PI, Motyka V. 201.  2015. Phytohormone profiling across the bryophytes. PLOS ONE 10:e0125411 [Google Scholar]
  203. Zhai QZ, Yan LH, Tan D, Chen R, Sun JQ. 202.  et al. 2013. Phosphorylation-coupled proteolysis of the transcription factor MYC2 is important for jasmonate-signaled plant immunity. PLOS Genet 9:e1003422 [Google Scholar]
  204. Zhang HT, Hedhili S, Montiel G, Zhang YX, Chatel G. 203.  et al. 2011. The basic helix-loop-helix transcription factor CrMYC2 controls the jasmonate-responsive expression of the ORCA genes that regulate alkaloid biosynthesis in Catharanthus roseus. . Plant J. 67:61–71 [Google Scholar]
  205. Zhang SW, Li CH, Cao J, Zhang YC, Zhang SQ. 204.  et al. 2009. Altered architecture and enhanced drought tolerance in rice via the down-regulation of indole-3-acetic acid by TLD1/OsGH3.13 activation. Plant Physiol 151:1889–901 [Google Scholar]
  206. Zhang X, Zhu ZQ, An FY, Hao DD, Li PP. 205.  et al. 2014. Jasmonate-activated MYC2 represses ETHYLENE INSENSITIVE3 activity to antagonize ethylene-promoted apical hook formation in Arabidopsis. . Plant Cell 26:1105–17 [Google Scholar]
  207. Zhang ZQ, Li Q, Li ZM, Staswick PE, Wang MY. 206.  et al. 2007. Dual regulation role of GH3.5 in salicylic acid and auxin signaling during ArabidopsisPseudomonas syringae interaction. Plant Physiol 145:450–64 [Google Scholar]
  208. Zhao YF, Thilmony R, Bender CL, Schaller A, He SY, Howe GA. 207.  2003. Virulence systems of Pseudomonassyringae pv. tomato promote bacterial speck disease in tomato by targeting the jasmonate signaling pathway. Plant J 36:485–99 [Google Scholar]
  209. Zhao YT, Wang M, Wang ZM, Fang RX, Wang XJ, Jia YT. 208.  2015. Dynamic and coordinated expression changes of rice small RNAs in response to Xanthomonas oryzae pv. oryzae. . J. Genet. Genom. 42:625–37 [Google Scholar]
  210. Zheng X-Y, Spivey NW, Zeng W, Liu P-P, Fu ZQ. 209.  et al. 2012. Coronatine promotes Pseudomonas syringae virulence in plants by activating a signaling cascade that inhibits salicylic acid accumulation. Cell Host Microbe 11:587–96 [Google Scholar]
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