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Jasmonates: signal transduction components and their roles in environmental stress responses

Plant Molecular Biology volume 91, pages 673–689 (2016)Cite this article

Abstract

Jasmonates, oxylipin-type plant hormones, are implicated in diverse aspects of plant growth development and interaction with the environment. Following diverse developmental and environmental cues, jasmonate is produced, conjugated to the amino acid isoleucine and perceived by a co-receptor complex composed of the Jasmonate ZIM-domain (JAZ) repressor proteins and an E3 ubiquitin ligase complex containing the F-box CORONATINE INSENSITIVE 1 (COI1). This event triggers the degradation of the JAZ proteins and the release of numerous transcription factors, including MYC2 and its homologues, which are otherwise bound and inhibited by the JAZ repressors. Here, we will review the role of the COI1, JAZ and MYC2 proteins in the interaction of the plant with its environment, illustrating the significance of jasmonate signalling, and of the proteins involved, for responses to both biotic stresses caused by insects and numerous microbial pathogens and abiotic stresses caused by adverse climatic conditions. It has also become evident that crosstalk with other hormone signals, as well as light and clock signals, plays an important role in the control and fine-tuning of these stress responses. Finally, we will discuss how several pathogens exploit the jasmonate perception and early signalling machinery to decoy the plants defence systems.

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References

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

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Abe H, Ohnishi J, Narusaka M, Seo S, Narusaka Y, Tsuda S, Kobayashi M (2008) Function of jasmonate in response and tolerance of Arabidopsis to thrip feeding. Plant Cell Physiol 49:68–80

    CAS  PubMed  Article  Google Scholar 

  • Abe H, Tateishi K, Seo S, Kugimiya S, Hirai MY, Sawada Y, Murata Y, Yara K, Shimoda T, Kobayashi M (2013) Disarming the jasmonate-dependent plant defense makes nonhost Arabidopsis plants accessible to the American serpentine leafminer. Plant Physiol 163:1242–1253

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Adie BAT, Pérez-Pérez J, Pérez-Pérez MM, Godoy M, Sánchez-Serrano J-J, Schmelz EA, Solano R (2007) ABA is an essential signal for plant resistance to pathogens affecting JA biosynthesis and the activation of defenses in Arabidopsis. Plant Cell 19:1665–1681

    CAS  PubMed  PubMed Central  Article  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 16:3460–3479

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Babitha KC, Ramu SV, Pruthvi V, Mahesh P, Nataraja KN, Udayakumar M (2013) Co-expression of AtbHLH17 and AtWRKY28 confers resistance to abiotic stress in Arabidopsis. Transgenic Res 22:327–341

    CAS  PubMed  Article  Google Scholar 

  • Ballaré CL (2014) Light regulation of plant defense. Annu Rev Plant Biol 65:335–363

    PubMed  Article  CAS  Google Scholar 

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

    CAS  PubMed  Article  Google Scholar 

  • Berrocal-Lobo M, Molina A (2004) Ethylene response factor 1 mediates Arabidopsis resistance to the soilborne fungus Fusarium oxysporum. Mol Plant Microbe Interact 17:763–770

    CAS  PubMed  Article  Google Scholar 

  • Bodenhausen N, Reymond P (2007) Signaling pathways controlling induced resistance to insect herbivores in Arabidopsis. Mol Plant Microbe Interact 20:1406–1420

    CAS  PubMed  Article  Google Scholar 

  • Böhm J, Scherzer S, Krol E, Kreuzer I, von Meyer K, Lorey C, Mueller TD, Shabala L, Monte I, Solano R, Al-Rasheid KAS, Rennenberg H, Shabala S, Neher E, Hedrich R (2016) The Venus flytrap Dionaea muscipula counts prey-induced action potentials to induce sodium uptake. Curr Biol 26:286–295

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  • Bortesi L, Fischer R (2015) The CRISPR/Cas9 system for plant genome editing and beyond. Biotechnol Adv 33:41–52

    CAS  PubMed  Article  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. Genes Dev 18:1577–1591

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Boter M, Golz JF, Gímenez-Ibañez S, Fernandez-Barbero G, Franco-Zorrilla JM, Solano R (2015) FILAMENTOUS FLOWER is a direct target of JAZ3 and modulates responses to jasmonate. Plant Cell 27:3160–3174

    CAS  PubMed  Article  Google Scholar 

  • Brodhun F, Feussner I (2011) Oxylipins in fungi. FEBS J 278:1047–1063

    CAS  PubMed  Article  Google Scholar 

  • Caarls L, Pieterse CMJ, Van Wees SCM (2015) How salicylic acid takes transcriptional control over jasmonic acid signaling. Front Plant Sci 6:170

    PubMed  PubMed Central  Article  Google Scholar 

  • Campos ML, Kang J-H, Howe GA (2014) Jasmonate-triggered plant immunity. J Chem Ecol 40:657–675

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Cárdenas PD, Sonawane PD, Pollier J, Vanden Bossche R, Dewangan V, Weithorn E, Tal L, Meir S, Rogachev I, Malitsky S, Giri AP, Goossens A, Burdman S, Aharoni A (2016) GAME9 regulates the biosynthesis of steroidal alkaloids and upstream isoprenoids in the plant mevalonate pathway. Nat Commun 7:10654

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  • Çevik V, Kidd BN, Zhang P, Hill C, Kiddle S, Denby KJ, Holub EB, Cahill DM, Manners JM, Schenk PM, Beynon J, Kazan K (2012) MEDIATOR25 acts as an integrative hub for the regulation of jasmonate-responsive gene expression in Arabidopsis. Plant Physiol 160:541–555

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  • Chen R, Jiang H, Li L, Zhai Q, Qi L, Zhou W, Liu X, Li H, Zheng W, Sun J, Li C (2012) The Arabidopsis Mediator subunit MED25 differentially regulates jasmonate and abscisic acid signaling through interacting with the MYC2 and ABI5 transcription factors. Plant Cell 24:2898–2916

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Chew YH, Wenden B, Flis A, Mengin V, Taylor J, Davey CL, Tindal C, Thomas H, Ougham HJ, de Reffye P, Stitt M, Williams M, Muetzelfeldt R, Halliday KJ, Millar AJ (2014) Multiscale digital Arabidopsis predicts individual organ and whole-organism growth. Proc Natl Acad Sci USA 111:E4127–E4136

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Chico J-M, Fernández-Barbero G, Chini A, Fernández-Calvo P, Díez-Díaz M, Solano R (2014) Repression of jasmonate-dependent defenses by shade involves differential regulation of protein stability of MYC transcription factors and their JAZ repressors in Arabidopsis. Plant Cell 26:1967–1980

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Chinchilla D, Bauer Z, Regenass M, Boller T, Felix G (2006) The Arabidopsis receptor kinase FLS2 binds flg22 and determines the specificity of flagellin perception. Plant Cell 18:465–476

    CAS  PubMed  PubMed Central  Article  Google Scholar 

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

    CAS  PubMed  Article  Google Scholar 

  • Chini A, Fonseca S, Chico JM, Fernández-Calvo P, Solano R (2009) The ZIM domain mediates homo- and heteromeric interactions between Arabidopsis JAZ proteins. Plant J 59:77–87

    CAS  PubMed  Article  Google Scholar 

  • Chung HS, Howe GA (2009) A critical role for the TIFY motif in repression of jasmonate signaling by a stabilized splice variant of the JASMONATE ZIM-domain protein JAZ10 in Arabidopsis. Plant Cell 21:131–145

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Clarke SM, Cristescu SM, Miersch O, Harren FJ, Wasternack C, Mur LA (2009) Jasmonates act with salicylic acid to confer basal thermotolerance in Arabidopsis thaliana. New Phytol 182:175–187

    CAS  PubMed  Article  Google Scholar 

  • Cole SJ, Yoon AJ, Faull KF, Diener AC (2014) Host perception of jasmonates promotes infection by Fusarium oxysporum formae speciales that produce isoleucine- and leucine-conjugated jasmonates. Mol Plant Pathol 15:589–600

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Cuéllar Pérez AC, Goossens A (2013) Jasmonate signalling: a copycat of auxin signalling? Plant Cell Environ 36:2071–2084

    PubMed  Article  CAS  Google Scholar 

  • De Boer K, Tilleman S, Pauwels L, Vanden Bossche R, De Sutter V, Vanderhaeghen R, Hilson P, Hamill JD, Goossens A (2011) APETALA2/ETHYLENE RESPONSE FACTOR and basic helix-loop-helix tobacco transcription factors cooperatively mediate jasmonate-elicited nicotine biosynthesis. Plant J 66:1053–1065

    PubMed  Article  CAS  Google Scholar 

  • De Geyter N, Gholami A, Goormachtig S, Goossens A (2012) Transcriptional machineries in jasmonate-elicited plant secondary metabolism. Trends Plant Sci 17:349–359

    PubMed  Article  CAS  Google Scholar 

  • de Torres Zabala M, Zhai B, Jayaraman S, Eleftheriadou G, Winsbury R, Yang R, Truman W, Tang S, Smirnoff N, Grant M (2016) Novel JAZ co-operativity and unexpected JA dynamics underpin Arabidopsis defence responses to Pseudomonas syringae infection. New Phytol 209:1120–1134

    CAS  PubMed  Article  Google Scholar 

  • de Wit M, Spoel SH, Sanchez-Perez GF, Gommers CMM, Pieterse CMJ, Voesenek LACJ, Pierik R (2013) Perception of low red:far-red ratio compromises both salicylic acid- and jasmonic acid-dependent pathogen defences in Arabidopsis. Plant J 75:90–103

    PubMed  Article  CAS  Google Scholar 

  • Demianski AJ, Chung KM, Kunkel BN (2012) Analysis of Arabidopsis JAZ gene expression during Pseudomonas syringae pathogenesis. Mol Plant Pathol 13:46–57

    CAS  PubMed  Article  Google Scholar 

  • Demole E, Lederer E, Mercier D (1962) Isolement et détermination de la structure du jasmonate de méthyle, constituant odorant caractéristique de l’essence de jasmin. Helv Chim Acta 45:675–685

    CAS  Article  Google Scholar 

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

    CAS  PubMed  Article  Google Scholar 

  • Domagalska MA, Leyser O (2011) Signal integration in the control of shoot branching. Nat Rev Mol Cell Biol 12:211–221

    CAS  PubMed  Article  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

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Durek P, Schmidt R, Heazlewood JL, Jones A, MacLean D, Nagel A, Kersten B, Schulze WX (2010) PhosPhAt: the Arabidopsis thaliana phosphorylation site database. An update. Nucleic Acids Res 38:D828–D834

    CAS  PubMed  Article  Google Scholar 

  • Fernández-Calvo P, Chini A, Fernández-Barbero G, Chico J-M, Gimenez-Ibanez S, Geerinck J, Eeckhout D, Schweizer F, Godoy M, Franco-Zorrilla JM, Pauwels L, Witters E, Puga MI, Paz-Ares J, Goossens A, Reymond P, De Jaeger G, Solano R (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  Article  CAS  Google Scholar 

  • Feys BJF, Benedetti CE, Penfold CN, Turner JG (1994) Arabidopsis mutants selected for resistance to the phytotoxin coronatine are male sterile, insensitive to methyl jasmonate, and resistant to a bacterial pathogen. Plant Cell 6:751–759

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Figueroa P, Browse J (2015) Male sterility in Arabidopsis induced by overexpression of a MYC5-SRDX chimeric repressor. Plant J 81:849–860

    CAS  PubMed  Article  Google Scholar 

  • Floková K, Feussner K, Herrfurth C, Miersch O, Mik V, Tarkowská D, Strnad M, Feussner I, Wasternack C, Novák O (2016) A previously undescribed jasmonate compound in flowering Arabidopsis thaliana—The identification of cis-(+)-OPDA-Ile. Phytochemistry 122:230–237

    PubMed  Article  CAS  Google Scholar 

  • Fonseca S, Chini A, Hamberg M, Adie B, Porzel A, Kramell R, Miersch O, Wasternack C, Solano R (2009) (+)-7-iso-Jasmonoyl-l-isoleucine is the endogenous bioactive jasmonate. Nat Chem Biol 5:344–350

    CAS  PubMed  Article  Google Scholar 

  • Fonseca S, Fernández-Calvo P, Fernández GM, Diez-Diaz M, Gimenez-Ibanez S, López-Vidriero I, Godoy M, Fernández-Barbero G, Van Leene J, De Jaeger G, Franco-Zorrilla JM, Solano R (2014a) bHLH003, bHLH013 and bHLH017 are new targets of JAZ repressors negatively regulating JA responses. PLoS One 9:e86182

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  • Fonseca S, Rosado A, Vaughan-Hirsch J, Bishopp A, Chini A (2014b) Molecular locks and keys: the role of small molecules in phytohormone research. Front Plant Sci 5:709

    PubMed  PubMed Central  Article  Google Scholar 

  • Frerigmann H, Berger B, Gigolashvili T (2014) bHLH05 is an interaction partner of MYB51 and a novel regulator of glucosinolate biosynthesis in Arabidopsis. Plant Physiol 166:349–369

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  • Gasperini D, Chételat A, Acosta IF, Goossens J, Pauwels L, Goossens A, Dreos R, Alfonso E, Farmer EE (2015) Multilayered organization of jasmonate signalling in the regulation of root growth. PLoS Genet 11:e1005300

    PubMed  PubMed Central  Article  Google Scholar 

  • Gimenez-Ibanez S, Boter M, Fernández-Barbero G, Chini A, Rathjen JP, Solano R (2014) The bacterial effector HopX1 targets JAZ transcriptional repressors to activate jasmonate signaling and promote infection in Arabidopsis. PLoS Biol 12:e1001792

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  • Gimenez-Ibanez S, Boter M, Solano R (2015) Novel players fine-tune plant trade-offs. Essays Biochem 58:83–100

    PubMed  Article  Google Scholar 

  • Gimenez-Ibanez S, Chini A, Solano R (2016) How microbes twist jasmonate signaling around their little fingers. Plants 5:9

    PubMed Central  Article  Google Scholar 

  • Glazebrook J (2005) Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. Annu Rev Phytopathol 43:205–227

    CAS  PubMed  Article  Google Scholar 

  • Gómez-Gómez L, Boller T (2000) FLS2: an LRR receptor-like kinase involved in the perception of the bacterial elicitor flagellin in Arabidopsis. Mol Cell 5:1003–1011

    PubMed  Article  Google Scholar 

  • Goodspeed D, Chehab EW, Min-Venditti A, Braam J, Covington MF (2012) Arabidopsis synchronizes jasmonate-mediated defense with insect circadian behavior. Proc Natl Acad Sci USA 109:4674–4677

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Goossens J, Swinnen G, Vanden Bossche R, Pauwels L, Goossens A (2015) Change of a conserved amino acid in the MYC2 and MYC3 transcription factors leads to release of JAZ repression and increased activity. New Phytol 206:1229–1237

    CAS  PubMed  Article  Google Scholar 

  • Grunewald W, Vanholme B, Pauwels L, Plovie E, Inzé D, Gheysen G, Goossens A (2009) Expression of the Arabidopsis jasmonate signalling repressor JAZ1/TIFY10A is stimulated by auxin. EMBO Rep 10:923–928

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Gu Y, Innes RW (2011) The KEEP ON GOING protein of Arabidopsis recruits the ENHANCED DISEASE RESISTANCE1 protein to trans-Golgi network/early endosome vesicles. Plant Physiol 155:1827–1838

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Guo X, Stotz HU (2007) Defense against Sclerotinia sclerotiorum in Arabidopsis is dependent on jasmonic acid, salicylic acid, and ethylene signaling. Mol Plant Microbe Interact 20:1384–1395

    CAS  PubMed  Article  Google Scholar 

  • Hamberg M, Gardner HW (1992) Oxylipin pathway to jasmonates: biochemistry and biological significance. Biochim Biophys Acta 1165:1–18

    CAS  PubMed  Article  Google Scholar 

  • Heil M, Baldwin IT (2002) Fitness costs of induced resistance: emerging experimental support for a slippery concept. Trends Plant Sci 7:61–67

    CAS  PubMed  Article  Google Scholar 

  • Heim MA, Jakoby M, Werber M, Martin C, Weisshaar B, Bailey PC (2003) The basic helix-loop-helix transcription factor family in plants: a genome-wide study of protein structure and functional diversity. Mol Biol Evol 20:735–747

    CAS  PubMed  Article  Google Scholar 

  • Heitz T, Widemann E, Lugan R, Miesch L, Ullmann P, Désaubry L, Holder E, Grausem B, Kandel S, Miesch M, Werck-Reichhart D, Pinot F (2012) Cytochromes P450 CYP94C1 and CYP94B3 catalyze two successive oxidation steps of plant hormone Jasmonoy l-isoleucine for catabolic turnover. J Biol Chem 287:6296–6306

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Hong G-J, Xue X-Y, Mao Y-B, Wang L-J, Chen X-Y (2012) Arabidopsis MYC2 interacts with DELLA proteins in regulating sesquiterpene synthase gene expression. Plant Cell 24:2635–2648

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Hou X, Lee LYC, Xia K, Yan Y, Yu H (2010) DELLAs modulate jasmonate signaling via competitive binding to JAZs. Dev Cell 19:884–894

    CAS  PubMed  Article  Google Scholar 

  • Howe GA, Jander G (2008) Plant immunity to insect herbivores. Annu Rev Plant Biol 59:41–66

    CAS  PubMed  Article  Google Scholar 

  • Hsieh H-L, Okamoto H (2014) Molecular interaction of jasmonate and phytochrome A signalling. J Exp Bot 65:2847–2857

    PubMed  Article  Google Scholar 

  • Hsieh H-L, Okamoto H, Wang M, Ang L-H, Matsui M, Goodman H, Deng XW (2000) FIN219, an auxin-regulated gene, defines a link between phytochrome A and the downstream regulator COP1 in light control of Arabidopsis development. Genes Dev 14:1958–1970

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hu Y, Jiang L, Wang F, Yu D (2013) Jasmonate regulates the INDUCER OF CBF EXPRESSION–C-REPEAT BINDING FACTOR/DRE BINDING FACTOR1 cascade and freezing tolerance in Arabidopsis. Plant Cell 25:2907–2924

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Huot B, Yao J, Montgomery BL, He SY (2014) Growth-defense tradeoffs in plants: a balancing act to optimize fitness. Mol Plant 7:1267–1287

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Ingle RA, Stoker C, Stone W, Adams N, Smith R, Grant M, Carré I, Roden LC, Denby KJ (2015) Jasmonate signalling drives time-of-day differences in susceptibility of Arabidopsis to the fungal pathogen Botrytis cinerea. Plant J 84:937–948

    CAS  PubMed  Article  Google Scholar 

  • Irvine NM, Yerkes CN, Graupner PR, Roberts RE, Hahn DR, Pearce C, Gerwick BC (2008) Synthesis and characterization of synthetic analogs of cinnacidin, a novel phytotoxin from Nectria sp. Pest Manag Sci 64:891–899

    CAS  PubMed  Article  Google Scholar 

  • Jiang S, Yao J, Ma K-W, Zhou H, Song J, He SY, Ma W (2013) Bacterial effector activates jasmonate signaling by directly targeting JAZ transcriptional repressors. PLoS Pathog 9:e1003715

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  • Jirschitzka J, Mattern DJ, Gershenzon J, D’Auria JC (2013) Learning from nature: new approaches to the metabolic engineering of plant defense pathways. Curr Opin Biotechnol 24:320–328

    CAS  PubMed  Article  Google Scholar 

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

    CAS  PubMed  Article  Google Scholar 

  • Kagale S, Links MG, Rozwadowski K (2010) Genome-wide analysis of ethylene-responsive element binding factor-associated amphiphilic repression motif-containing transcriptional regulators in Arabidopsis. Plant Physiol 152:1109–1134

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Katsir L, Schilmiller AL, Staswick PE, He SY, Howe GA (2008) COI1 is a critical component of a receptor for jasmonate and the bacterial virulence factor coronatine. Proc Natl Acad Sci USA 105:7100–7105

    CAS  PubMed  PubMed Central  Article  Google Scholar 

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

    CAS  PubMed  Article  Google Scholar 

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

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Kazan K, Manners JM (2009) Linking development to defense: auxin in plant-pathogen interactions. Trends Plant Sci 14:373–382

    CAS  PubMed  Article  Google Scholar 

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

    CAS  PubMed  Article  Google Scholar 

  • Kazan K, Manners JM (2013) MYC2: the master in action. Mol Plant 6:686–703

    CAS  PubMed  Article  Google Scholar 

  • Kidd BN, Edgar CI, Kumar KK, Aitken EA, Schenk PM, Manners JM, Kazan K (2009) The Mediator complex subunit PFT1 is a key regulator of jasmonate-dependent defense in Arabidopsis. Plant Cell 21:2237–2252

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Kitaoka N, Matsubara T, Sato M, Takahashi K, Wakuta S, Kawaide H, Matsui H, Nabeta K, Matsuura H (2011) Arabidopsis CYP94B3 encodes jasmonyl-l-isoleucine 12-hydroxylase, a key enzyme in the oxidative catabolism of jasmonate. Plant Cell Physiol 52:1757–1765

    CAS  PubMed  Article  Google Scholar 

  • Kloek AP, Verbsky ML, Sharma SB, Schoelz JE, Vogel J, Klessig DF, Kunkel BN (2001) Resistance to Pseudomonas syringae conferred by an Arabidopsis thaliana coronatine-insensitive (coi1) mutation occurs through two distinct mechanisms. Plant J 26:509–522

    CAS  PubMed  Article  Google Scholar 

  • Koo AJK, Cooke TF, Howe GA (2011) Cytochrome P450 CYP94B3 mediates catabolism and inactivation of the plant hormone jasmonoyl-l-isoleucine. Proc Natl Acad Sci USA 108:9298–9303

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Koo AJ, Thireault C, Zemelis S, Poudel AN, Zhang T, Kitaoka N, Brandizzi F, Matsuura H, Howe GA (2014) Endoplasmic reticulum-associated inactivation of the hormone jasmonoyl-l-isoleucine by multiple members of the cytochrome P450 94 family in Arabidopsis. J Biol Chem 289:29728–29738

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Laha D, Johnen P, Azevedo C, Dynowski M, Weiß M, Capolicchio S, Mao H, Iven T, Steenbergen M, Freyer M, Gaugler P, de Campos MKF, Zheng N, Feussner I, Jessen HJ, Van Wees SCM, Saiardi A, Schaaf G (2015) VIH2 regulates the synthesis of inositol pyrophosphate InsP8 and jasmonate-dependent defenses in Arabidopsis. Plant Cell 27:1082–1097

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Leone M, Keller MM, Cerrudo I, Ballaré CL (2014) To grow or defend? Low red: far-red ratios reduce jasmonate sensitivity in Arabidopsis seedlings by promoting DELLA degradation and increasing JAZ10 stability. New Phytol 204:355–367

    CAS  PubMed  Article  Google Scholar 

  • Li H, Sun J, Xu Y, Jiang H, Wu X, Li C (2007) The bHLH-type transcription factor AtAIB positively regulates ABA response in Arabidopsis. Plant Mol Biol 65:655–665

    CAS  PubMed  Article  Google Scholar 

  • Li R, Weldegergis BT, Li J, Jung C, Qu J, Sun Y, Qian H, Tee C, van Loon JJA, Dicke M, Chua N-H, Liu S-S, Ye J (2014) Virulence factors of geminivirus interact with MYC2 to subvert plant resistance and promote vector performance. Plant Cell 26:4991–5008

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Liu H, Stone SL (2010) Abscisic acid increases Arabidopsis ABI5 transcription factor levels by promoting KEG E3 ligase self-ubiquitination and proteasomal degradation. Plant Cell 22:2630–2641

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Lorenzo O, Chico JM, Sánchez-Serrano JJ, Solano R (2004) JASMONATE-INSENSITIVE1 encodes a MYC transcription factor essential to discriminate between different jasmonate-regulated defense responses in Arabidopsis. Plant Cell 16:1938–1950

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Mafli A, Goudet J, Farmer EE (2012) Plants and tortoises: mutations in the Arabidopsis jasmonate pathway increase feeding in a vertebrate herbivore. Mol Cell 21:2534–2541

    Google Scholar 

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

    CAS  PubMed  Article  Google Scholar 

  • Melotto M, Mecey C, Niu Y, Chung HS, Katsir L, Yao J, Zeng W, Thines B, Staswick PE, Browse J, Howe GA, He SY (2008) A critical role of two positively charged amino acids in the Jas motif of Arabidopsis JAZ proteins in mediating coronatine- and jasmonoyl isoleucine-dependent interactions with the COI1 F-box protein. Plant J 55:979–988

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Memelink J (2009) Regulation of gene expression by jasmonate hormones. Phytochemistry 70:1560–1570

    CAS  PubMed  Article  Google Scholar 

  • Mengiste T (2012) Plant immunity to necrotrophs. Annu Rev Phytopathol 50:267–294

    CAS  PubMed  Article  Google Scholar 

  • Mertens J, Pollier J, Vanden Bossche R, Lopez-Vidriero I, Franco-Zorrilla JM, Goossens A (2016) The bHLH transcription factors TSAR1 and TSAR2 regulate triterpene saponin biosynthesis in Medicago truncatula. Plant Physiol 170:194–210

    CAS  PubMed  Article  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

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Mewis I, Tokuhisa JG, Schultz JC, Appel HM, Ulrichs C, Gershenzon J (2006) Gene expression and glucosinolate accumulation in Arabidopsis thaliana in response to generalist and specialist herbivores of different feeding guilds and the role of defense signaling pathways. Phytochemistry 67:2450–2462

    CAS  PubMed  Article  Google Scholar 

  • Miersch O, Preiss A, Sembdner G, Schreiber K (1987) (+)-7-iso-jasmonic acid and related compounds from Botryodiplodia theobromae. Phytochemistry 26:1037–1039

    CAS  Article  Google Scholar 

  • Miersch O, Günther T, Fritsche W, Sembdner G (1993) Jasmonates from different fungal species. Nat Prod Lett 2:293–299

    CAS  Article  Google Scholar 

  • Miersch O, Bohlmann H, Wasternack C (1999a) Jasmonates and related compounds from Fusarium oxysporum. Phytochemistry 50:517–523

    CAS  Article  Google Scholar 

  • Miersch O, Porzel A, Wasternack C (1999b) Microbial conversion of jasmonates-hydroxylations by Aspergillus niger. Phytochemistry 50:1147–1152

    CAS  PubMed  Article  Google Scholar 

  • Miersch O, Regvar M, Wasternack C (1999c) Metabolism of jasmonic acid in Pisolithus tinctorius cultures. Phyton-Ann Rei Bot 39:243–247

    CAS  Google Scholar 

  • Miersch O, Neumerkel J, Dippe M, Stenzel I, Wasternack C (2008) Hydroxylated jasmonates are commonly occurring metabolites of jasmonic acid and contribute to a partial switch-off in jasmonate signaling. New Phytol 177:114–127

    CAS  PubMed  Google Scholar 

  • Mittler R, Shulaev V (2013) Functional genomics, challenges and perspectives for the future. Physiol Plant 148:317–321

    CAS  PubMed  Article  Google Scholar 

  • Monte I, Hamberg M, Chini A, Gimenez-Ibanez S, Garcia-Casado G, Porzel A, Pazos F, Boter M, Solano R (2014) Rational design of a ligand-based antagonist of jasmonate perception. Nat Chem Biol 10:671–676

    CAS  PubMed  Article  Google Scholar 

  • Moreno JE, Ballaré CL (2014) Phytochrome regulation of plant immunity in vegetation canopies. J Chem Ecol 40:848–857

    CAS  PubMed  Article  Google Scholar 

  • Moreno JE, Tao Y, Chory J, Ballaré CL (2009) Ecological modulation of plant defense via phytochrome control of jasmonate sensitivity. Proc Natl Acad Sci USA 106:4935–4940

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Moreno JE, Shyu C, Campos ML, Patel LC, Chung HS, Yao J, He SY, Howe GA (2013) Negative feedback control of jasmonate signaling by an alternative splice variant of JAZ10. Plant Physiol 162:1006–1017

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Mosblech A, Thurow C, Gatz C, Feussner I, Heilmann I (2011) Jasmonic acid perception by COI1 involves inositol polyphosphates in Arabidopsis thaliana. Plant J 65:949–957

    CAS  PubMed  Article  Google Scholar 

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

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Nagata M, Yamamoto N, Shigeyama T, Terasawa Y, Anai T, Sakai T, Inada S, Arima S, Hashiguchi M, Akashi R, Nakayama H, Ueno D, Hirsch AM, Suzuki A (2015) Red/far red light controls arbuscular mycorrhizal colonization via jasmonic acid and strigolactone signaling. Plant Cell Physiol 56:2100–2109

    PubMed  Google Scholar 

  • Nakata M, Mitsuda N, Herde M, Koo AJK, Moreno JE, Suzuki K, Howe GA, Ohme-Takagi M (2013) A bHLH-type transcription factor, ABA-INDUCIBLE BHLH-TYPE TRANSCRIPTION FACTOR/JA-ASSOCIATED MYC2-LIKE1, acts as a repressor to negatively regulate jasmonate signaling in Arabidopsis. Plant Cell 25:1641–1656

    CAS  PubMed  PubMed Central  Article  Google Scholar 

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

    CAS  PubMed  Article  Google Scholar 

  • Oka K, Kobayashi M, Mitsuhara I, Seo S (2013) Jasmonic acid negatively regulates resistance to Tobacco mosaic virus in tobacco. Plant Cell Physiol 54:1999–2010

    CAS  PubMed  Article  Google Scholar 

  • Park S-Y, Peterson FC, Mosquna A, Yao J, Volkman BF, Cutler SR (2015) Agrochemical control of plant water use using engineered abscisic acid receptors. Nature 520:545–548

    PubMed  Article  CAS  Google Scholar 

  • Paschold A, Halitschke R, Baldwin IT (2007) Co(i)-ordinating defenses: NaCOI1 mediates herbivore-induced resistance in Nicotiana attenuata and reveals the role of herbivore movement in avoiding defenses. Plant J 51:79–91

    CAS  PubMed  Article  Google Scholar 

  • Patkar RN, Benke PI, Qu Z, Constance Chen YY, Yang F, Swarup S, Naqvi NI (2015) A fungal monooxygenase-derived jasmonate attenuates host innate immunity. Nat Chem Biol 11:733–740

    CAS  PubMed  Article  Google Scholar 

  • Pauwels L, Goossens A (2011) The JAZ proteins: a crucial interface in the jasmonate signaling cascade. Plant Cell 23:3089–3100

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Pauwels L, Barbero GF, Geerinck J, Tilleman S, Grunewald W, Cuéllar Pérez A, Chico JM, Vanden Bossche R, Sewell J, Gil E, García-Casado G, Witters E, Inzé D, Long JA, De Jaeger G, Solano R, Goossens A (2010) NINJA connects the co-repressor TOPLESS to jasmonate signalling. Nature 464:788–791

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Pauwels L, Ritter A, Goossens J, Nagels Durand A, Liu H, Gu Y, Geerinck J, Boter M, Vanden Bossche R, De Clercq R, Van Leene J, Gevaert K, De Jaeger G, Solano R, Stone S, Innes RW, Callis J, Goossens A (2015) The RING E3 ligase KEEP ON GOING modulates JASMONATE ZIM-DOMAIN12 stability. Plant Physiol 169:1405–1417

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  • Pieterse CMJ, Van der Does D, Zamioudis C, Leon-Reyes A, Van Wees SCM (2012) Hormonal modulation of plant immunity. Annu Rev Cell Dev Biol 28:489–521

    CAS  PubMed  Article  Google Scholar 

  • Plett JM, Kemppainen M, Kale SD, Kohler A, Legué V, Brun A, Tyler BM, Pardo AG, Martin F (2011) A secreted effector protein of Laccaria bicolor is required for symbiosis development. Curr Biol 21:1197–1203

    CAS  PubMed  Article  Google Scholar 

  • Plett JM, Daguerre Y, Wittulsky S, Vayssières A, Deveau A, Melton SJ, Kohler A, Morrell-Falvey JL, Brun A, Veneault-Fourrey C, Martin F (2014) Effector MiSSP7 of the mutualistic fungus Laccaria bicolor stabilizes the Populus JAZ6 protein and represses jasmonic acid (JA) responsive genes. Proc Natl Acad Sci USA 111:8299–8304

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Qi T, Huang H, Song S, Xie D (2015) Regulation of jasmonate-mediated stamen development and seed production by a bHLH-MYB complex in Arabidopsis. Plant Cell 27:1620–1633

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Ralhan A, Schöttle S, Thurow C, Iven T, Feussner I, Polle A, Gatz C (2012) The vascular pathogen Verticillium longisporum requires a jasmonic acid-independent COI1 function in roots to elicit disease symptoms in Arabidopsis shoots. Plant Physiol 159:1192–1203

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Reymond P, Bodenhausen N, Van Poecke RMP, Krishnamurthy V, Dicke M, Farmer EE (2004) A conserved transcript pattern in response to a specialist and a generalist herbivore. Plant Cell 16:3132–3147

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Riemann M, Bouyer D, Hisada A, Müller A, Yatou O, Weiler EW, Takano M, Furuya M, Nick P (2009) Phytochrome A requires jasmonate for photodestruction. Planta 229:1035–1045

    CAS  PubMed  Article  Google Scholar 

  • Rigal A, Ma Q, Robert S (2014) Unraveling plant hormone signaling through the use of small molecules. Front Plant Sci 5:373

    PubMed  PubMed Central  Article  Google Scholar 

  • Robson F, Okamoto H, Patrick E, Harris S-R, Wasternack C, Brearley C, Turner JG (2010) Jasmonate and phytochrome A signaling in Arabidopsis wound and shade responses are integrated through JAZ1 stability. Plant Cell 22:1143–1160

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Romera-Branchat M, Andrés F, Coupland G (2014) Flowering responses to seasonal cues: what’s new? Curr Opin Plant Biol 21:120–127

    CAS  PubMed  Article  Google Scholar 

  • Rouached H, Stefanovic A, Secco D, Bulak Arpat A, Gout E, Bligny R, Poirier Y (2011) Uncoupling phosphate deficiency from its major effects on growth and transcriptome via PHO1 expression in Arabidopsis. Plant J 65:557–570

    CAS  PubMed  Article  Google Scholar 

  • Sasaki-Sekimoto Y, Jikumaru Y, Obayashi T, Saito H, Masuda S, Kamiya Y, Ohta H, Shirasu K (2013) Basic helix-loop-helix transcription factors JASMONATE-ASSOCIATED MYC2-LIKE1 (JAM1), JAM2, and JAM3 are negative regulators of jasmonate responses in Arabidopsis. Plant Physiol 163:291–304

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Sawa M, Kay SA (2011) GIGANTEA directly activates Flowering Locus T in Arabidopsis thaliana. Proc Natl Acad Sci USA 108:11698–11703

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Schmiesing A, Emonet A, Gouhier-Darimont C, Reymond P (2016) Arabidopsis MYC transcription factors are the target of hormonal SA/JA crosstalk in response to Pieris brassicae egg extract. Plant Physiol in press (available online 16 Fabruary 2016). doi:10.1104/pp.16.00031

  • Schoonhoven LM, van Loon JJA, Jermy T (1998) Insect-plant biology : from physiology to evolution. Chapman and Hall, London

    Book  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

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Sears MT, Zhang H, Rushton PJ, Wu M, Han S, Spano AJ, Timko MP (2014) NtERF32: a non-NIC2 locus AP2/ERF transcription factor required in jasmonate-inducible nicotine biosynthesis in tobacco. Plant Mol Biol 84:49–66

    CAS  PubMed  Article  Google Scholar 

  • Sehr EM, Agusti J, Lehner R, Farmer EE, Schwarz M, Greb T (2010) Analysis of secondary growth in the Arabidopsis shoot reveals a positive role of jasmonate signalling in cambium formation. Plant J 63:811–822

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Sheard LB, Tan X, Mao H, Withers J, Ben-Nissan G, Hinds TR, Kobayashi Y, Hsu F-F, Sharon M, Browse J, He SY, Rizo J, Howe GA, Zheng N (2010) Jasmonate perception by inositol-phosphate-potentiated COI1–JAZ co-receptor. Nature 468:400–405

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Shin J, Heidrich K, Sanchez-Villarreal A, Parker JE, Davis SJ (2012) TIME FOR COFFEE represses accumulation of the MYC2 transcription factor to provide time-of-day regulation of jasmonate signaling in Arabidopsis. Plant Cell 24:2470–2482

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Shoji T, Hashimoto T (2011) Tobacco MYC2 regulates jasmonate-inducible nicotine biosynthesis genes directly and by way of the NIC2-locus ERF genes. Plant Cell Physiol 52:1117–1130

    CAS  PubMed  Article  Google Scholar 

  • Shyu C, Figueroa P, Depew CL, Cooke TF, Sheard LB, Moreno JE, Katsir L, Zheng N, Browse J, Howe GA (2012) JAZ8 lacks a canonical degron and has an EAR motif that mediates transcriptional repression of jasmonate responses in Arabidopsis. Plant Cell 24:536–550

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Smolen GA, Pawlowski L, Wilensky SE, Bender J (2002) Dominant alleles of the basic helix-loop-helix transcription factor ATR2 activate stress-responsive genes in Arabidopsis. Genetics 161:1235–1246

    CAS  PubMed  PubMed Central  Google Scholar 

  • Song S, Huang H, Gao H, Wang J, Wu D, Liu X, Yang S, Zhai Q, Li C, Qi T, Xie D (2014) Interaction between MYC2 and ETHYLENE INSENSITIVE3 modulates antagonism between jasmonate and ethylene signaling in Arabidopsis. Plant Cell 26:263–279

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Spoel SH, Dong X (2012) How do plants achieve immunity? Defence without specialized immune cells. Nat Rev Immunol 12:89–100

    CAS  PubMed  Article  Google Scholar 

  • Spoel SH, Koornneef A, Claessens SM, Korzelius JP, Van Pelt JA, Mueller MJ, Buchala AJ, Metraux JP, Brown R, Kazan K, Van Loon LC, Dong X, Pieterse CM (2003) NPR1 modulates cross-talk between salicylate- and jasmonate-dependent defense pathways through a novel function in the cytosol. Plant Cell 15:760–770

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Staswick PE (2009) The tryptophan conjugates of jasmonic and indole-3-acetic acids are endogenous auxin inhibitors. Plant Physiol 150:1310–1321

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Stone SL, Williams LA, Farmer LM, Vierstra RD, Callis J (2006) KEEP ON GOING, a RING E3 ligase essential for Arabidopsis growth and development, is involved in abscisic acid signaling. Plant Cell 18:3415–3428

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Sugio A, Kingdom HN, MacLean AM, Grieve VM, Hogenhout SA (2011) Phytoplasma protein effector SAP11 enhances insect vector reproduction by manipulating plant development and defense hormone biosynthesis. Proc Natl Acad Sci USA 108:E1254–E1263

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Suzuki A, Suriyagoda L, Shigeyama T, Tominaga A, Sasaki M, Hiratsuka Y, Yoshinaga A, Arima S, Agarie S, Sakai T, Inada S, Jikumaru Y, Kamiya Y, Uchiumi T, Abe M, Hashiguchi M, Akashi R, Sato S, Kaneko T, Tabata S, Hirsch AM (2011) Lotus japonicus nodulation is photomorphogenetically controlled by sensing the red/far red (R/FR) ratio through jasmonic acid (JA) signaling. Proc Natl Acad Sci USA 108:16837–16842

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Swarup R, Kramer EM, Perry P, Knox K, Leyser HMO, Haseloff J, Beemster GTS, Bhalerao R, Bennett MJ (2005) Root gravitropism requires lateral root cap and epidermal cells for transport and response to a mobile auxin signal. Nat Cell Biol 7:1057–1065

    CAS  PubMed  Article  Google Scholar 

  • Talukder ZI, Hulke BS, Qi L, Scheffler BE, Pegadaraju V, McPhee K, Gulya TJ (2014) Candidate gene association mapping of Sclerotinia stalk rot resistance in sunflower (Helianthus annuus L.) uncovers the importance of COI1 homologs. Theor Appl Genet 127:193–209

    CAS  PubMed  Article  Google Scholar 

  • Thatcher LF, Manners JM, Kazan K (2009) Fusarium oxysporum hijacks COI1-mediated jasmonate signaling to promote disease development in Arabidopsis. Plant J 58:927–939

    CAS  PubMed  Article  Google Scholar 

  • Thines B, Katsir L, Melotto M, Niu Y, Mandaokar A, Liu G, Nomura K, He SY, Howe GA, Browse J (2007) JAZ repressor proteins are targets of the SCFCOI1 complex during jasmonate signalling. Nature 448:661–665

    CAS  PubMed  Article  Google Scholar 

  • Thireault C, Shyu C, Yoshida Y, St. Aubin B, Campos ML, Howe GA (2015) Repression of jasmonate signaling by a non-TIFY JAZ protein in Arabidopsis. Plant J 82:669–679

    CAS  PubMed  Article  Google Scholar 

  • Thomma BPHJ, Eggermont K, Penninckx IAMA, Mauch-Mani B, Vogelsang R, Cammue BPA, Broekaert WF (1998) Separate jasmonate-dependent and salicylate-dependent defense-response pathways in Arabidopsis are essential for resistance to distinct microbial pathogens. Proc Natl Acad Sci USA 95:15107–15111

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Toda Y, Tanaka M, Ogawa D, Kurata K, Kurotani K, Habu Y, Ando T, Sugimoto K, Mitsuda N, Katoh E, Abe K, Miyao A, Hirochika H, Hattori T, Takeda S (2013) RICE SALT SENSITIVE3 forms a ternary complex with JAZ and class-C bHLH factors and regulates jasmonate-induced gene expression and root cell elongation. Plant Cell 25:1709–1725

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Todd AT, Liu E, Polvi SL, Pammett RT, Page JE (2010) A functional genomics screen identifies diverse transcription factors that regulate alkaloid biosynthesis in Nicotiana benthamiana. Plant J 62:589–600

    CAS  PubMed  Article  Google Scholar 

  • Trusov Y, Sewelam N, Rookes JE, Kunkel M, Nowak E, Schenk PM, Botella JR (2009) Heterotrimeric G proteins-mediated resistance to necrotrophic pathogens includes mechanisms independent of salicylic acid-, jasmonic acid/ethylene- and abscisic acid-mediated defense signaling. Plant J 58:69–81

    CAS  PubMed  Article  Google Scholar 

  • Tsukada K, Takahashi K, Nabeta K (2010) Biosynthesis of jasmonic acid in a plant pathogenic fungus, Lasiodiplodia theobromae. Phytochemistry 71:2019–2023

    CAS  PubMed  Article  Google Scholar 

  • Valladares F, Gianoli E, Gómez JM (2007) Ecological limits to plant phenotypic plasticity. New Phytol 176:749–763

    PubMed  Article  Google Scholar 

  • Van der Does D, Leon-Reyes A, Koornneef A, Van Verk MC, Rodenburg N, Pauwels L, Goossens A, Körbes AP, Memelink J, Ritsema T, Van Wees SCM, Pieterse CMJ (2013) Salicylic acid suppresses jasmonic acid signaling downstream of SCFCOI1-JAZ by targeting GCC promoter motifs via transcription factor ORA59. Plant Cell 25:744–761

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  • Van Moerkercke A, Steensma P, Schweizer F, Pollier J, Gariboldi I, Payne R, Vanden Bossche R, Miettinen K, Espoz J, Purnama PC, Kellner F, Seppänen-Laakso T, O’Connor SE, Rischer H, Memelink J, Goossens A (2015) The bHLH transcription factor BIS1 controls the iridoid branch of the monoterpenoid indole alkaloid pathway in Catharanthus roseus. Proc Natl Acad Sci USA 112:8130–8135

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  • Verhage A, Vlaardingerbroek I, Raaymakers C, Van Dam NM, Dicke M, Van Wees SCM, Pieterse CMJ (2011) Rewiring of the jasmonate signaling pathway in Arabidopsis during insect herbivory. Front Plant Sci 2:47

    PubMed  PubMed Central  Article  Google Scholar 

  • Vos IA, Moritz L, Pieterse CMJ, Van Wees SCM (2015) Impact of hormonal crosstalk on plant resistance and fitness under multi-attacker conditions. Front Plant Sci 6:639

    PubMed  PubMed Central  Article  Google Scholar 

  • Wang J-G, Chen C-H, Chien C-T, Hsieh H-L (2011) FAR-RED INSENSITIVE219 modulates CONSTITUTIVE PHOTOMORPHOGENIC1 activity via physical interaction to regulate hypocotyl elongation in Arabidopsis. Plant Physiol 156:631–646

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Wasternack C (2014) Action of jasmonates in plant stress responses and development—applied aspects. Biotechnol Adv 32:31–39

    CAS  PubMed  Article  Google Scholar 

  • Wasternack C, Hause B (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 111:1021–1058

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Wathugala DL, Hemsley PA, Moffat CS, Cremelie P, Knight MR, Knight H (2012) The Mediator subunit SFR6/MED16 controls defence gene expression mediated by salicylic acid and jasmonate responsive pathways. New Phytol 195:217–230

    CAS  PubMed  Article  Google Scholar 

  • Wawrzynska A, Christiansen KM, Lan Y, Rodibaugh NL, Innes RW (2008) Powdery mildew resistance conferred by loss of the ENHANCED DISEASE RESISTANCE1 protein kinase is suppressed by a missense mutation in KEEP ON GOING, a regulator of abscisic acid signaling. Plant Physiol 148:1510–1522

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Wild M, Daviere J-M, Cheminant S, Regnault T, Baumberger N, Heintz D, Baltz R, Genschik P, Achard P (2012) The Arabidopsis DELLA RGA-LIKE3 is a direct target of MYC2 and modulates jasmonate signaling responses. Plant Cell 24:3307–3319

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • World Health Organization (2013) WHO Model List of Essential Medicines. http://www.who.int/medicines/publications/essentialmedicines/18th_EML_Final_web_8Jul13.pdf

  • Wu H, Ye H, Yao R, Zhang T, Xiong L (2015) OsJAZ9 acts as a transcriptional regulator in jasmonate signaling and modulates salt stress tolerance in rice. Plant Sci 232:1–12

    CAS  PubMed  Article  Google Scholar 

  • Xie D-X, Feys BF, James S, Nieto-Rostro M, Turner JG (1998) COI1: an Arabidopsis gene required for jasmonate-regulated defense and fertility. Science 280:1091–1094

    CAS  PubMed  Article  Google Scholar 

  • Xin X-F, He SY (2013) Pseudomonas syringae pv. tomato DC3000: a model pathogen for probing disease susceptibility and hormone signaling in plants. Annu Rev Phytopathol 51:473–498

    CAS  PubMed  Article  Google Scholar 

  • Yan Y, Stolz S, Chételat A, Reymond P, Pagni M, Dubugnon L, Farmer EE (2007) A downstream mediator in the growth repression limb of the jasmonate pathway. Plant Cell 19:2470–2483

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Yan J, Zhang C, Gu M, Bai Z, Zhang W, Qi T, Cheng Z, Peng W, Luo H, Nan F, Wang Z, Xie D (2009) The Arabidopsis CORONATINE INSENSITIVE1 protein is a jasmonate receptor. Plant Cell 21:2220–2236

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Yan J, Li H, Li S, Yao R, Deng H, Xie Q, Xie D (2013) The Arabidopsis F-box protein CORONATINE INSENSITIVE1 is stabilized by SCFCOI1 and degraded via the 26S proteasome pathway. Plant Cell 25:486–498

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Yang D-L, Yao J, Mei C-S, Tong X-H, Zeng L-J, Li Q, Xiao L-T, T-p Sun, Li J, Deng X-W, Lee CM, Thomashow MF, Yang Y, He Z, He SY (2012) Plant hormone jasmonate prioritizes defense over growth by interfering with gibberellin signaling cascade. Proc Natl Acad Sci USA 109:E1192–E1200

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Ye M, Luo SM, Xie JF, Li YF, Xu T, Liu Y, Song YY, Zhu-Salzman K, Zeng RS (2012) Silencing COI1 in rice increases susceptibility to chewing insects and impairs inducible defense. PLoS One 7:e36214

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Yu Z-X, Li J-X, Yang C-Q, Hu W-L, Wang L-J, Chen X-Y (2012) The jasmonate-responsive AP2/ERF transcription factors AaERF1 and AaERF2 positively regulate artemisinin biosynthesis in Artemisia annua L. Mol Plant 5:353–365

    CAS  PubMed  Article  Google Scholar 

  • Yu J, Zhang Y, Di C, Zhang Q, Zhang K, Wang C, You Q, Yan H, Dai SY, Yuan JS, Xu W, Su Z (2016) JAZ7 negatively regulates dark-induced leaf senescence in Arabidopsis. J Exp Bot 67:751–762

    PubMed  Article  Google Scholar 

  • Zander M, La Camera S, Lamotte O, Métraux JP, Gatz C (2010) Arabidopsis thaliana class-II TGA transcription factors are essential activators of jasmonic acid/ethylene-induced defense responses. Plant J 61:200–210

    CAS  PubMed  Article  Google Scholar 

  • Zander M, Thurow C, Gatz C (2014) TGA transcription factors activate the salicylic acid-suppressible branch of the ethylene-induced defense program by regulating ORA59 expression. Plant Physiol 165:1671–1683

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Zarate SI, Kempema LA, Walling LL (2007) Silverleaf whitefly induces salicylic acid defenses and suppresses effectual jasmonic acid defenses. Plant Physiol 143:866–875

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Zhai Q, Zhang X, Wu F, Feng H, Deng L, Xu L, Zhang M, Wang Q, Li C (2015) Transcriptional mechanism of jasmonate receptor COI1-mediated delay of flowering time in Arabidopsis. Plant Cell 27:2814–2828

    PubMed  PubMed Central  Google Scholar 

  • Zhang H, Hedhili S, Montiel G, Zhang Y, Chatel G, Pré M, Gantet P, Memelink J (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

    CAS  PubMed  Article  Google Scholar 

  • Zhang X, Wang C, Zhang Y, Sun Y, Mou Z (2012) The Arabidopsis mediator complex subunit16 positively regulates salicylate-mediated systemic acquired resistance and jasmonate/ethylene-induced defense pathways. Plant Cell 24:4294–4309

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Zhang X, Zhu Z, An F, Hao D, Li P, Song J, Yi C, Guo H (2014) Jasmonate-activated MYC2 represses ETHYLENE INSENSITIVE3 activity to antagonize ethylene-promoted apical hook formation in Arabidopsis. Plant Cell 26:1105–1117

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Zhang B, Wang L, Zeng L, Zhang C, Ma H (2015a) Arabidopsis TOE proteins convey a photoperiodic signal to antagonize CONSTANS and regulate flowering time. Genes Dev 29:975–987

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Zhang F, Yao J, Ke J, Zhang L, Lam VQ, Xin X-F, Zhou XE, Chen J, Brunzelle J, Griffin PR, Zhou M, Xu HE, Melcher K, He SY (2015b) Structural basis of JAZ repression of MYC transcription factors in jasmonate signalling. Nature 525:269–273

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Zhang L, Yao J, Withers J, Xin X-F, Banerjee R, Fariduddin Q, Nakamura Y, Nomura K, Howe GA, Boland W, Yan H, He SY (2015c) Host target modification as a strategy to counter pathogen hijacking of the jasmonate hormone receptor. Proc Natl Acad Sci USA 112:14354–14359

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Zhao M-L, Wang J-N, Shan W, Fan J-G, Kuang J-F, Wu K-Q, Li X-P, Chen W-X, He F-Y, Chen J-Y, Lu W-J (2013) Induction of jasmonate signalling regulators MaMYC2s and their physical interactions with MaICE1 in methyl jasmonate-induced chilling tolerance in banana fruit. Plant Cell Environ 36:30–51

    PubMed  Article  CAS  Google Scholar 

  • Zheng X-Y, Spivey NW, Zeng W, Liu P-P, Fu ZQ, Klessig DF, He SY, Dong X (2012) Coronatine promotes Pseudomonas syringae virulence in plants by activating a signaling cascade that inhibits salicylic acid accumulation. Cell Host Microbe 11:587–596

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Zhou Z, Wu Y, Yang Y, Du M, Zhang X, Guo Y, Li C, Zhou J-M (2015) An Arabidopsis plasma membrane proton ATPase modulates JA signaling and is exploited by the Pseudomonas syringae effector protein AvrB for stomatal invasion. Plant Cell 27:2032–2041

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Zhu Z, Lee B (2015) Friends or foes: new insights in jasmonate and ethylene co-actions. Plant Cell Physiol 56:414–420

    PubMed  Article  Google Scholar 

  • Zhu Z, An F, Feng Y, Li P, Xue L, Mu A, Jiang Z, Kim J-M, To TK, Li W, Zhang X, Yu Q, Dong Z, Chen W-Q, Seki M, Zhou J-M, Guo H (2011) Derepression of ethylene-stabilized transcription factors (EIN3/EIL1) mediates jasmonate and ethylene signaling synergy in Arabidopsis. Proc Natl Acad Sci USA 108:12539–12544

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Zipfel C, Robatzek S, Navarro L, Oakeley EJ, Jones JDG, Felix G, Boller T (2004) Bacterial disease resistance in Arabidopsis through flagellin perception. Nature 428:764–767

    CAS  PubMed  Article  Google Scholar 

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Acknowledgments

We thank Annick Bleys for help in preparing the manuscript. This work was supported by the Agency for Innovation by Science and Technology in Flanders (IWT) for a predoctoral fellowship (to J. G.), the European Union 7th Framework Programme (EU-FP7) People for a Marie Curie Intra-European postdoctoral fellowship (to P. F.-C.) and the Swiss National Foundation for an Early Postdoc Mobility grant (to F. S.).

Author Contributions

J. G., P. F.-C., F. S., and A. G. wrote the manuscript.

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    1. Department of Plant Systems Biology, Flanders Institute for Biotechnology, Technologiepark 927, 9052, Ghent, Belgium

      Jonas Goossens, Patricia Fernández-Calvo, Fabian Schweizer & Alain Goossens

    2. Department of Plant Biotechnology and Bioinformatics, Ghent University, Technologiepark 927, 9052, Ghent, Belgium

      Jonas Goossens, Patricia Fernández-Calvo, Fabian Schweizer & Alain Goossens

    Authors
    1. Jonas Goossens
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    2. Patricia Fernández-Calvo
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    3. Fabian Schweizer
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    4. Alain Goossens
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    Correspondence to Alain Goossens.

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    Jonas Goossens, Patricia Fernández-Calvo and Fabian Schweizer have contributed equally to this work.

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    Goossens, J., Fernández-Calvo, P., Schweizer, F. et al. Jasmonates: signal transduction components and their roles in environmental stress responses. Plant Mol Biol 91, 673–689 (2016). https://doi.org/10.1007/s11103-016-0480-9

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    • DOI: https://doi.org/10.1007/s11103-016-0480-9

    Keywords

    • COI1
    • Jasmonate
    • JAZ
    • Light
    • MYC2
    • Pathogen