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Methyl jasmonate-induced cell death in grapevine requires both lipoxygenase activity and functional octadecanoid biosynthetic pathway

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Abstract

Grapevine (Vitis vinifera L., cv. Limberger) leaf tissues and suspension-cultured cells were induced to undergo programmed cell death (PCD) by exogenously added methyl jasmonate (MeJA). The elicitor signaling pathway involved in MeJA-induced PCD was further investigated using pharmacological, biochemical and histological approaches. Pharmacological dissection of the early events preceding the execution of MeJA-triggered PCD indicated that this process strongly depends on both, de novo protein and mRNA synthesis. Treatment of leaf discs and cell suspensions with lipase inhibitor Ebelactone B and specific lipoxygenase inhibitor Phenidone blocked MeJA-induced PCD. These results suggest that some chloroplast membrane-derived compound(s) is required for MeJA-induced PCD in grapevine. The progression of MeJAtriggered PCD may be further inhibited by the use of metabolic inhibitors of key enzymes of octadecanoid biosynthesis including AOS, AOC, and OPR indicating that the functional jasmonate biosynthetic pathway is an integral part of the MeJA-induced signal transduction cascade that results in the coordinate expression of events leading to PCD. Finally, the activation of the octadecanoid pathway, as a critical point in MeJA-induced PCD, was independently demonstrated with cellulysin, a macromolecular elicitor acting via octadecanoid signaling. The cellulysin was shown to be a very potent enhancer of MeJA-triggered PCD in grapevine cells.

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Abbreviations

AOC:

allene oxide cyclase

AOS:

allene oxide synthase

CHX:

cycloheximide

COR:

cordycepin

DIECA:

diethyldithiocarbamic acid

HR:

hypersensitive response

JA:

jasmonic acid

LOX:

lipoxygenase

MeJA:

methyljasmonate

NIA:

necrosis-inducing activity

OPDA:

12-oxophytodienoic acid

OPR:

12-oxophytodienoic acid reductase

qRT-PCR:

quantitative real-time polymerase chain reaction

TMV:

tobacco mosaic virus

TUB:

tubulin

References

  • Avanci N., Luche D., Goldman G.H. & Goldman M.H. 2010. Jasmonates are phytohormones with multiple functions, including plant defense and reproduction. Genet. Mol. Res. 9: 484–505.

    Article  PubMed  CAS  Google Scholar 

  • Bell E., Creelman R. A. & Mullet J. E. 1995. A chloroplast lipoxygenase is required for wound-induced jasmonic acid accumulation in Arabidopsis. Proc. Natl. Acad. Sci. USA 92: 8675–8679.

    Article  PubMed  CAS  Google Scholar 

  • Chen Y., Pang Q., Dai S., Wang Y., Chen S. & Yan, X. 2011. Proteomic identification of differentially expressed proteins in Arabidopsis in response to methyl jasmonate. J. Plant Physiol. 168: 995–1008.

    Article  PubMed  CAS  Google Scholar 

  • Chini A., Fonseca S., Fernandez G., Chico J.M. & Solano R. 2007. The JAZ family of repressors is the missing link in jasmonate signalling. Nature 448: 666–671.

    Article  PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Dhondt S., Geoffroy P., Stelmach B. A., Legrand M. & Heitz T. 2000. Soluble phospholipase A2 activity is induced before oxylipin accumulation in tobacco mosaic virus-infected tobacco leaves and is contributed by patatin-like enzymes. Plant J. 23: 431–440.

    Article  PubMed  CAS  Google Scholar 

  • Ellinger D., Sting N., Kubigsteltig I.I., Bals T., Juenger M., Pollmann S., Berger S., Schuenemann D. & Mueller M.J. 2010. DONGLE and DEFECTIVE IN ANTHER DEHISCENCE1 lipases are not essential for wound- and pathogen-induced jasmonate biosynthesis: redundant lipases contribute to jasmonate formation. Plant Physiol. 153: 114–127.

    Article  PubMed  CAS  Google Scholar 

  • Feys B.J.F., Benedetti C.E., Penfold C.N. & Turner J.G. 1994. Arabidopsis mutants selected for resistance to the phytotoxin coronatine are male-sterile, insensitive to methyl JA, and resistant to a bacterial pathogen. Plant Cell 6: 751–759.

    PubMed  CAS  Google Scholar 

  • Gfeller A., Liechti R. & Farmer E. E. 2010. Arabidposis jasmonate signaling pathway. Sci. Signal. 3: 109–116.

    Google Scholar 

  • Halitschke R. & Baldwin I.T. 2003. Antisense LOX expression increases herbivore performance by decreasing defense responses and inhibiting growth-related transcriptional reorganization in Nicotiana attenuata. Plant J. 36: 794–807.

    Article  PubMed  CAS  Google Scholar 

  • Hyun Y., Choi S., Hwang H.J., Yu J., Nam S. J., Ko J., Park J.Y., Seo Y.S., Kim E.Y. & Ryu S.B. 2008. Cooperation and functional diversification of two closely related galactolipase genes for jasmonic acid (JA) biosynthesis. Dev. Cell 14: 183–192.

    Article  PubMed  CAS  Google Scholar 

  • Ishiguro S., Kawai-Oda A., Nishida I. & Okada K. 2001. The defective in anther dehiscence1 gene encodes a novel phospolipase A1 catalyzing the initial step of jasmonic acid biosynthesis, which synchronizes pollen maturation, anther dehiscence, and flower opening in Arabidopsis. Plant Cell 13: 2191–2209.

    PubMed  CAS  Google Scholar 

  • Ismail A., Riemann M. & Nick P. 2012. The jasmonate pathway mediates salt tolerance in grapevines. J. Exp. Bot. 36: 1–13.

    Google Scholar 

  • Kramell R., Miersch O., Atzorn R., Parthier B. & Wasternack C. 2000. Octadecanoid-derived alteration of gene expression and the ”oxylipin signature” in stressed barley leaves. Implications for different signaling pathways. Plant Physiol. 123: 177–188.

    CAS  Google Scholar 

  • Lorenzo O., Chico J.M., Sanchez-Serrano J.J. & Solano R. 2004. JA-INSENSITIVE1 encodes a MYC transcription factor essential to discriminate between different JA-regulated defense responses in Arabidopsis. Plant Cell 16: 1938–1950.

    Article  PubMed  CAS  Google Scholar 

  • Mueller M.J., Brodschelm W., Spannagl E. & Zenk M. 1993. Signaling in the elicitation process is mediated through the octadecanoid pathway leading to jasmonic acid. Proc. Nat. Acad. Sci. USA, 90: 7490–7494.

    Article  PubMed  CAS  Google Scholar 

  • Narvaez-Vasquez J., Florin-Christensen J. & Ryan C.A. 1999. Positional specificity of a phospholipase A2 activity induced by wounding, systemin, and oligosaccharide elicitors in tomato leaves. Plant Cell 11: 2249–2260.

    PubMed  CAS  Google Scholar 

  • Piel J., Atzorn R., Gäbler R., Kühnemann F. & Boland W. 1997. Cellulysin from the plant parasitic fungus Trichoderma viride elicits volatile biosynthesis in higher plants via the octadecanoid signalling cascade. FEBS Letters 416: 143–148.

    Article  PubMed  CAS  Google Scholar 

  • Repka V. 2002. Hydrogen peroxide generated via octadecanoid signaling pathway is neither necessary nor sufficient for methyl jasmonate-induced hypersensitive cell death. Biol. Plant. 45: 105–115.

    Article  CAS  Google Scholar 

  • Repka V. 2008. Grapevine (Vitis vinifera L.) microRNA expression profiling with miRNA bioarrays: indications for an involvement of miRNA in apoptosis and pathogenesis. Bulletin de L’OIV 81: 171–178.

    CAS  Google Scholar 

  • Repka V. & Fischerová I. 2001. New findings to the role of tunikamycin in grapevine: disease defense response. Vitis 40: 169–174.

    CAS  Google Scholar 

  • Repka V., Kubíková J. & Fischerová I. 2000. Immunodetection of PR-1-like proteins in grapevine leaves infected with Oidium tuckerii and in elicited suspension cell cultures. Vitis 39: 123–127.

    CAS  Google Scholar 

  • Repka V., Fischerová I. & Šilhárová K. 2001. Methyl jasmonate induces a hypersensitive-like response of grapevine in the absence of avirulent pathogens. Vitis 40: 5–10.

    CAS  Google Scholar 

  • Repka V., Fischerová I. & Šilhárová K. 2004. Methyl jasmonate is a potent elicitor of multiple defense responses in grapevine leaves and cell.spuspension cultures. Biol. Plant. 48: 273–283.

    Article  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Royo J., Leon J., Vancanneyt G., Albar J. P., Rosahl S., Ortego F., Castanera P. & Sanchez-Serrano J. 1999. Antisensemediated depletion of a potato lipoxygenase reduces wound induction of proteinase inhibitors and increases weight gain of insect pests. Proc. Nat. Acad. Sci. USA, 96: 1146–1151.

    Article  PubMed  CAS  Google Scholar 

  • Schäfer M., Fischer C., Meldau S., Seebald E., Oelmüller R. & Baldwin I.T. 2011. Lipase activity in insect oral secretions mediates defense responses in Arabidopsis thaliana. Plant Physiol. 156: 487–496.

    Article  Google Scholar 

  • Schaller A. & Stintzi A. 2009. Enzymes in jasmonate biosynthesis — structure, function, regulation. Phytochemistry 70: 1532–1538.

    Article  PubMed  CAS  Google Scholar 

  • Schaller F., Schaller A. & Stintzi A. F. 2005. Biosynthesis and metabolism of jasmonates. J. Plant Growth Regul. 23: 179–199.

    Google Scholar 

  • Schlink K. 2011. Gene expression profiling in wounded and systemic leaves of Fagus sylvatica reveals up-regulation of ethylene and jasmonic acid signalling. Plant Biol (Stuttg). 13: 445–452.

    Article  PubMed  CAS  Google Scholar 

  • Seeley K. A., Byrne D. H. & Colbert J.T. 1992. Red lightindependent instability of oat phytochrome mRNA in vivo. Plant Cell 4: 29–38.

    PubMed  CAS  Google Scholar 

  • Sheard L.B., Tan X., Mao H., Withers J., Ben-Nissan G., Hinds T.R., Kobayashi Y., Hsu F.F., Sharon M., Browse J., He S.Y., Rizo J., Howe G.A. & Zheng N. 2010. Jasmonate perception by inositol-phosphate-potentiated COI1-JAZ coreceptor. Nature 468: 400–405.

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Vanholme B., Grunewald W., Bateman A., Kohchi T. & Gheysen G. 2007. The tify family previously known as ZIM. Trends Plant Sci. 12: 239–244.

    Article  PubMed  CAS  Google Scholar 

  • Vick B. A. & Zimmerman D. C. 1984. Biosynthesis of jasmonic acid by several plant species. Plant Physiol. 75: 458–461.

    Article  PubMed  CAS  Google Scholar 

  • Weber H. 2002. Fatty acid-derived signals in plants. Trends Plant Sci. 7: 217–224.

    Article  PubMed  CAS  Google Scholar 

  • Weber H., Vick B. A. & Farmer E.E. 1997. Dinor-oxo-phytodienoic acid: a new hexadecanoid signal in the jasmonate family. Proc. Natl. Acad. Sci. USA, 94: 10473–10478.

    Article  PubMed  CAS  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.

    Article  PubMed  CAS  Google Scholar 

  • Zhang Y. & Turner J.G. 2008. Wound-induced endogenous Jas stunt plant growth by inhibiting mitosis. PLoS One 3: e3699.

    Article  PubMed  Google Scholar 

  • Zhu Q., Chappell J., Hendricks S. A. & Lamb C. 1995. Accurate in vitro transcription from cicrularized plasmid templates by plant whole cell extracts. Plant J. 7: 1021–1030.

    Article  PubMed  CAS  Google Scholar 

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Correspondence to Vladimír Repka.

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Repka, V., Čarná, M. & Pavlovkin, J. Methyl jasmonate-induced cell death in grapevine requires both lipoxygenase activity and functional octadecanoid biosynthetic pathway. Biologia 68, 896–903 (2013). https://doi.org/10.2478/s11756-013-0220-4

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