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Volatile methyl jasmonate is a transmissible form of jasmonate and its biosynthesis is involved in systemic jasmonate response in wounding

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Abstract

Volatile organic compounds (VOCs) easily diffuse due to their high hydrophobicity. Because of this physical property, VOCs are able to act as crucial signalling molecules mediating intercellular and interplant communication. Methyl jasmonate (MeJA) is a volatile ester form of jasmonic acid (JA) that is involved in interplant communication in response to biotic and abiotic stresses. Despite its function in interplant communication, the specific role of MeJA in the regulation of intercellular jasmonate responses have been poorly understood. In this study, we demonstrated that MeJA is much more effective than JA in inducing jasmonate response, and the higher efficacy of MeJA relies on its volatile property. To understand the function of MeJA in the regulation of the jasmonate response, we analysed function of JMT gene, Jasmonic acid Methyl Transferase using its knockout mutant (jmt) and overexpressing plants (35S:JMT). Mutant plants that lack JMT expression exhibited reduced jasmonate response, while JMT-overexpressing plants exhibited a higher jasmonate response to JA treatment compared to wild-type plants. In this study, we also showed that JMT is specifically expressed in the phloem, the main vascular system for the transport of phytohormones, and that JMT expression affects systemic jasmonate response in wounding. These results suggest the volatile MeJA is a transmissible form of jasmonate and that its biosynthesis is involved in systemic jasmonate response in wounding.

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References

  • Akin DE, Rigsby LL, Morrison Iii WH (2004) Oil red as a histochemical stain for natural fibers and plant cuticle. Ind Crops Prod 19:119–124

    Article  CAS  Google Scholar 

  • Bishopp A, Lehesranta S, Vatén A, El-Showk S, Scheres B et al (2011) Phloem-transported cytokinin regulates polar auxin transport and maintains vascular pattern in the root meristem. Curr Biol 21:927–932

    Article  CAS  PubMed  Google Scholar 

  • Cheong J-J, Choi YD (2003) Methyl jasmonate as a vital substance in plants. Trends Genet 19:409–413

    Article  CAS  PubMed  Google Scholar 

  • Chini A, Fonseca S, Fernandez G, Adie B, Chico J et al (2007) The JAZ family of repressors is the missing link in jasmonate signalling. Nature 448:666–671

    Article  CAS  PubMed  Google Scholar 

  • Conconi A, Miquel M, Ryan C (1996) Intracellular levels of free linolenic and linoleic acids increase in tomato leaves in response to wounding. Plant Physiol 111:797–803

    CAS  PubMed Central  PubMed  Google Scholar 

  • Devoto A, Nieto-Rostro M, Xie D, Ellis C, Harmston R et al (2002) COI1 links jasmonate signalling and fertility to the SCF ubiquitin–ligase complex in Arabidopsis. Plant J 32:457–466

    Article  CAS  PubMed  Google Scholar 

  • Ellis C, Karafyllidis I, Wasternack C, Turner JG (2002) The Arabidopsis mutant cev1 links cell wall signaling to jasmonate and ethylene responses. Plant Cell 14:1557–1566

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Engelberth J, Schmelz EA, Alborn HT, Cardoza YJ, Huang J et al (2003) Simultaneous quantification of jasmonic acid and salicylic acid in plants by vapor-phase extraction and gas chromatography–chemical ionization-mass spectrometry. Anal Biochem 312:242–250

    Article  CAS  PubMed  Google Scholar 

  • Farmer EE, Ryan CA (1990) Interplant communication: airborne methyl jasmonate induces synthesis of proteinase inhibitors in plant leaves. Proc Natl Acad Sci USA 87:7713–7716

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Fonseca S, Chini A, Hamberg M, Adie B, Porzel A et al (2009) (+)-7-iso-Jasmonoyl-l-isoleucine is the endogenous bioactive jasmonate. Nat Chem Biol 5:344–350

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Harms K, Atzorn R, Brash A, Kuhn H, Wasternack C et al (1995) Expression of a flax allene oxide synthase cDNA leads to increased endogenous jasmonic acid (JA) levels in transgenic potato plants but not to a corresponding activation of JA-responding genes. Plant Cell 7:1645–1654

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Hause B, Stenzel I, Miersch O, Maucher H, Kramell R et al (2000) Tissue-specific oxylipin signature of tomato flowers: allene oxide cyclase is highly expressed in distinct flower organs and vascular bundles. Plant J 24:113–126

    Article  CAS  PubMed  Google Scholar 

  • Hause B, Hause G, Kutter C, Miersch O, Wasternack C (2003) Enzymes of jasmonate biosynthesis occur in tomato sieve elements. Plant Cell Physiol 44:643–648

    Article  CAS  PubMed  Google Scholar 

  • Jang G, Yi K, Pires ND, Menand B, Dolan L (2011) RSL genes are sufficient for rhizoid system development in early diverging land plants. Development 138:2273–2281

    Article  CAS  PubMed  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

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Koo YJ, Kim MA, Kim EH, Song JT, Jung C et al (2007) Overexpression of salicylic acid carboxyl methyltransferase reduces salicylic acid-mediated pathogen resistance in Arabidopsis thaliana. Plant Mol Biol 64:1–15

    Article  CAS  PubMed  Google Scholar 

  • Koo YJ, Yoon E, Song JT, Seo HS, Kim J-H et al (2008) An advanced method for the determination of carboxyl methyl esterase activity using gas chromatography–chemical ionization–mass spectrometry. J Chromatogr B 863:80–87

    Article  CAS  Google Scholar 

  • Koo YJ, Yoon ES, Seo JS, Kim J-K, Do Choi Y (2013) Characterization of a methyl jasmonate specific esterase in Arabidopsis. J Korean Soc Appl Biol Chem 56:27–33

    Article  Google Scholar 

  • Li L, Li C, Lee GI, Howe GA (2002) Distinct roles for jasmonate synthesis and action in the systemic wound response of tomato. Proc Natl Acad Sci USA 99:6416–6421

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Melotto M, Mecey C, Niu Y, Chung HS, Katsir L et al (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

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Meyer R, Rautenbach GF, Dubery IA (2003) Identification and quantification of methyl jasmonate in leaf volatiles of Arabidopsis thaliana using solid-phase microextraction in combination with gas chromatography and mass spectrometry. Phytochem Anal 14:155–159

    Article  CAS  PubMed  Google Scholar 

  • Millar AA, Clemens S, Zachgo S, Giblin EM, Taylor DC et al (1999) CUT1, an Arabidopsis gene required for cuticular wax biosynthesis and pollen fertility, encodes a very-long-chain fatty acid condensing enzyme. Plant Cell 11:825–838

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Mousavi SA, Chauvin A, Pascaud F, Kellenberger S, Farmer EE (2013) Glutamate receptor-like genes mediate leaf-to-leaf wound signalling. Nature 500:422–426

    Article  CAS  PubMed  Google Scholar 

  • Pichersky E, Gershenzon J (2002) The formation and function of plant volatiles: perfumes for pollinator attraction and defense. Curr Opin Plant Biol 5:237–243

    Article  CAS  PubMed  Google Scholar 

  • Rojo E, León J, Sánchez-Serrano JJ (1999) Cross-talk between wound signalling pathways determines local versus systemic gene expression in Arabidopsis thaliana. Plant J 20:135–142

    Article  CAS  PubMed  Google Scholar 

  • Schilmiller AL, Howe GA (2005) Systemic signaling in the wound response. Curr Opin Plant Biol 8:369–377

    Article  CAS  PubMed  Google Scholar 

  • Seo HS, Song JT, Cheong J-J, Lee Y-H, Lee Y-W et al (2001) Jasmonic acid carboxyl methyltransferase: a key enzyme for jasmonate-regulated plant responses. Proc Natl Acad Sci USA 98:4788–4793

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Seo JS, Koo YJ, Jung C, Yeu SY, Song JT et al (2013) Identification of a novel jasmonate-responsive element in the AtJMT promoter and its binding protein for AtJMT repression. PLoS ONE 8:e55482

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Sheard LB, Tan X, Mao H, Withers J, Ben-Nissan G et al (2010) Jasmonate perception by inositol-phosphate-potentiated COI1-JAZ co-receptor. Nature 468:400–405

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Song JT, Seo HS, Song SI, Lee JS, Do Choi Y (2000) NTR1 encodes a floral nectary-specific gene in Brassica campestris L. ssp. pekinensis. Plant Mol Biol 42:647–655

    Article  CAS  PubMed  Google Scholar 

  • Staswick PE, Tiryaki I (2004) The oxylipin signal jasmonic acid is activated by an enzyme that conjugates it to isoleucine in Arabidopsis. Plant Cell 16:2117–2127

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Staswick PE, Tiryaki I, Rowe ML (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 14:1405–1415

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Stenzel I, Hause B, Miersch O, Kurz T, Maucher H et al (2003) Jasmonate biosynthesis and the allene oxide cyclase family of Arabidopsis thaliana. Plant Mol Biol 51:895–911

    Article  CAS  PubMed  Google Scholar 

  • Stintzi A, Browse J (2000) The Arabidopsis male-sterile mutant, opr3, lacks the 12-oxophytodienoic acid reductase required for jasmonate synthesis. Proc Natl Acad Sci USA 97:10625–10630

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Tamogami S, Rakwal R, Agrawal GK (2008) Interplant communication: airborne methyl jasmonate is essentially converted into JA and JA-Ile activating jasmonate signaling pathway and VOCs emission. Biochem Biophys Res Commun 376:723–727

    Article  CAS  PubMed  Google Scholar 

  • Tamogami S, Noge K, Abe M, Agrawal GK, Rakwal R (2012) Methyl jasmonate is transported to distal leaves via vascular process metabolizing itself into JA-Ile and triggering VOCs emission as defensive metabolites. Plant Signal Behav 7:1378–1381

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Thines B, Katsir L, Melotto M, Niu Y, Mandaokar A et al (2007) JAZ repressor proteins are targets of the SCFCOI1 complex during jasmonate signalling. Nature 448:661–665

    Article  CAS  PubMed  Google Scholar 

  • Thorpe MR, Ferrieri AP, Herth MM, Ferrieri RA (2007) 11C-imaging: methyl jasmonate moves in both phloem and xylem, promotes transport of jasmonate, and of photoassimilate even after proton transport is decoupled. Planta 226:541–551

    Article  CAS  PubMed  Google Scholar 

  • Titarenko E, Rojo E, Leon J, Sanchez-Serrano JJ (1997) Jasmonic acid-dependent and -independent signaling pathways control wound-induced gene activation in Arabidopsis thaliana. Plant Physiol 115:817–826

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • VanDoorn A, Bonaventure G, Schmidt DD, Baldwin IT (2011) Regulation of jasmonate metabolism and activation of systemic signaling in Solanum nigrum: COI1 and JAR4 play overlapping yet distinct roles. New Phytol 190:640–652

    Article  CAS  PubMed  Google Scholar 

  • Vick BA, Zimmerman DC (1983) The biosynthesis of jasmonic acid: a physiological role for plant lipoxygenase. Biochem Biophys Res Commun 111:470–477

    Article  CAS  PubMed  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

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Wasternack C, Stenzel I, Hause B, Hause G, Kutter C et al (2006) The wound response in tomato–role of jasmonic acid. J Plant Physiol 163:297–306

    Article  CAS  PubMed  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

    Article  CAS  PubMed  Google Scholar 

  • Zhong R, Ripperger A, Ye Z-H (2000) Ectopic deposition of lignin in the pith of stems of two Arabidopsis mutants. Plant Physiol 123:59–70

    Article  CAS  PubMed Central  PubMed  Google Scholar 

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Acknowledgments

We thank the Cold Spring Harbor Laboratory and the Nottingham Arabidopsis Stock Center for providing jmt (GT8009). This work was supported by a grant from the Next-Generation BioGreen 21 Program (project nos. PJ008053 to Y.D.C. and PJ007971 to J.-K.K.), Rural Development Administration, Republic of Korea, through the National Center for GM Crops. A graduate research assistantship to J.S.S. from the Brain Korea 21 Plus project of the MOE is also acknowledged.

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Correspondence to Yang Do Choi.

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Jang, G., Shim, J.S., Jung, C. et al. Volatile methyl jasmonate is a transmissible form of jasmonate and its biosynthesis is involved in systemic jasmonate response in wounding. Plant Biotechnol Rep 8, 409–419 (2014). https://doi.org/10.1007/s11816-014-0331-6

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