Skip to main content
Log in

Aspirin prevents wound-induced gene expression in tomato leaves by blocking jasmonic acid biosynthesis

  • Published:
Planta Aims and scope Submit manuscript

Abstract

Jasmonic acid (JA) and its methyl ester, like mechanical wounding, strongly induce accumulation of proteinase inhibitor II (Pin2) in tomato and potato leaves. In plants, JA is synthesized from α-linolenic acid by a lipoxygenase (LOX)-mediated oxygenation leading to 13-hydroxyperoxylinolenic acid (13-HPLA) which is then subsequently transformed to JA by the action of hydroperoxide-dehydrase activity and additional modification steps. Both the chemical structure as well as the biosynthetic pathway of JA resemble those of the mammalian eicosanoids (prostaglandins and leukotrienes) which are derived from LOX-and cyclooxygenase (COX)-mediated reactions. To assess the role of endogenous JA in the wound response, detached tomato (Lycopersicon esculentum Mill.) leaves were supplied with different LOX and COX inhibitors and the expression of the wound-induced genes for Pin2 (Pin2), cathepsin D inhibitor (Cdi) and threonine deaminase (Td) was analyzed. Lipoxygenase inhibitors as well as some COX inhibitors blocked the wound-induced accumulation of Pin2, Cdi and Td mRNA. Quantitation of endogenous levels of JA showed that aspirin blocks the increase of this phytohormone normally observed as a result of wounding. Linolenic acid and 13-HPLA do not induce the expression of Pin2, Cdi and Td in the presence of aspirin. However, 12-oxo-phytodienoic acid and jasmonic acid are able to overcome the inhibitory effect of this substance. These results strongly indicate that aspirin prevents wound-induced gene activation by inhibiting the hydroxyperoxide-dehydrase activity that mediates the conversion of 13-HPLA to 12-oxo-phytodienoic acid.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

Abbreviations

ABA:

cis-abscisic acid

Cdi:

cathepsin D-inhibitor

COX:

cyclooxygenase

ETYA:

eicosatetraynoic acid

13-HPLA:

13-hydroxyperoxylinolenic acid

JA:

jasmonic acid

LA:

linolenic acid

LOX:

lipoxygenase

MeJa:

methyl jasmonate

12-oxo-PDA:

12-oxo-phytodienoic acid

Pin2:

proteinase inhibitor II

SHAM:

salicylhydroxamic acid

ssRb :

gene for the small subunit of ribulose-1,5-bisphosphate carboxylase-oxygenase

Td:

threonine deaminase

ZK139817:

lipoxygenase in-hibitor

References

  • Amasino, R.M. (1986) Acceleration of nucleic acid hybridization rate by polyethylenglycol. Anal. Biochem. 152, 304–307

    Google Scholar 

  • Bishop, P.D., Makus, D.J., Pearce, G., Ryan, C.A. (1981) Proteinase inhibitor-inducing factor activity in tomato leaves resides in oligosaccarides enzymically released from cell walls. Proc. Natl. Acad. Sci. USA 78, 3526–3540

    Google Scholar 

  • Creelman, R.E., Tierney, M.L., Mullet, J.E. (1992) Jasmonic acid/ methyl jasmonate accumulate in wounded soybean hypocotyls and modulate wound gene expression. Proc. Natl. Acad. Sci. USA 89, 4938–4941

    Google Scholar 

  • Doherty, H.M., Selvendran, R.R., Bowles, D.J. (1988) The wound response of plants can be inhibited by aspirin and related hydroxy-benzoic acids. Physiol. Mol. Plant Pathol. 33, 377–384

    Google Scholar 

  • Eckes, P., Schell, J., Willmitzer, L. (1985) Organ-specific expression of three leaf/stem specific cDNA's from potato is regulated by light and correlated with chloroplast development. Mol. Gen. Genet. 199, 216–224

    Google Scholar 

  • Enyedi, A.J., Yalpami, N., Silverman, P., Raskin, I. (1992) Localization, conjugation, and function of salicylic acid in tobacco during the hypersensitive reaction to tobacco mosaic virus. Proc. Natl. Acad. Sci. USA 89, 2480–2484

    Google Scholar 

  • Farmer, E.E., Ryan, C.A. (1990) Interplant communication: Airbone methyl jasmonate induces synthesis of proteinase inhibitor in plant leaves. Proc. Natl. Acad. Sci. USA 87, 7713–7716

    Google Scholar 

  • Farmer, E.E., Ryan, C.A. (1992) Octadecanoid precursors of jasmonic acid activate the synthesis of wound-inducible proteinaseinhibitors. Plant Cell 4, 129–134

    Google Scholar 

  • Farmer, E.E., Johnson, R., Ryan, C.A. (1992) Regulation of expression of proteinase inhibitor genes by methyl jasmonate and jasmonic acid. Plant Physiol. 98, 995–1002

    Google Scholar 

  • Green, T.R., Ryan, C.A. (1972) Wound-induced proteinase inhibitor in plant leaves: a possible defense mechanism against insects. Science 175, 776–777

    CAS  Google Scholar 

  • Hammond, M.L. (1989) 2,3-Dihydro-5-benzofuranols as antioxidant-based inhibitors of leukotriene biosynthesis. J. Med. Chem. 32, 1006–1020

    Google Scholar 

  • Hildmann, T., Ebneth, M., Peña-Cortés, H., Sanchez-Serrano, J., Willmitzer, L., Prat, S. (1992) General roles of abscisic acid and jasmonic acids in gene activation as a result of mechanical wounding. Plant Cell 4, 1157–1170

    Google Scholar 

  • Logemann, J., Schell, J., Willmitzer, L. (1987) Improved method for the isolation of RNA from plant tissue. Anal. Biochem. 163, 16–20

    Google Scholar 

  • Needleman, P., Turk, J., Jakschik, B.A., Morrison, A.R., Lefkowith, J.B. (1986) Arachidonic acid metabolism. Annu. Rev. Biochem. 55, 69–102

    Google Scholar 

  • Pace-Asciak, C.R., Smith, W.L. (1983) Enzyme in the biosynthesis and catabolism of the eicosanoids: Prostaglandins, thromboxanes, leukotrienes and hydroxy fatty acids. Enzymes 16, 543–603

    Google Scholar 

  • Pearce, G., Strydom, D., Johnson, S., Ryan, C.A. (1991) A polypeptide from tomato leaves induces wound-inducible proteinase inhibitor proteins. Science 253, 895–898

    Google Scholar 

  • Peña-Cortés, H., Sanchez-Serrano, J.J., Rocha-Sosa, M., Willmitzer, L. (1988) Systemic induction of proteinase-inhibitor-II gene expression in potato plants. Planta 174, 84–89

    Google Scholar 

  • Peña-Cortés, H., Sanchez-Serrano, J.J., Mertens, R., Willmitzer, L., Prat, S. (1989) Abscisic acid is involved in the wound-induced expression of the proteinase inhibitor II gene in potato and tomato. Proc. Natl. Acad. Sci. USA 86, 9851–9855

    Google Scholar 

  • Peña-Cortés, H., Willmitzer, L., Sanchez-Serrano, J.J. (1991) Abscisic acid mediates wound induction but not developmental-specific expression of the proteinase inhibitor II gene family. Plant Cell 3, 963–972

    Google Scholar 

  • Peña-Cortés, H., Liu, X., Sanchez-Serrano, J.J., Schmid, R., Willmitzer, L. (1992) Factor affecting gene expression of patatin and proteinase-inhibitor-II gene families in detached potato leaves: Implications for their co-expression in develop tubers. Planta 186, 495–502

    Google Scholar 

  • Roth, G.J., Stanford, N., Majerus, P.W. (1975) Acetylation of prostaglandin synthase by aspirin. Proc. Natl. Acad. Sci. USA 72, 3073–3076

    Google Scholar 

  • Sanchez-Serrano, J.J., Schmidt, R., Schell, J., Willmitzer, L. (1986) Nucleotide sequence of proteinase inhibitor II encoding cDNA of potato (Solanum tuberosum) and its mode of expression. Mol. Gen. Genet. 203, 15–20

    Google Scholar 

  • Smith, W.L., Marnett, L.J. (1991) Prostaglandin endoperoxide synthase: Structure and catalysis. Biochim. Biophys. Acta 1083, 1–17

    Google Scholar 

  • Vick, B.A., Zimmermann, D.C. (1979) Distribution of a fatty acid cyclase enzyme system in plants. Plant Physiol. 64, 203–205

    Google Scholar 

  • Vick, B.A., Zimmermann, D.C. (1983) The biosynthesis of jasmonic acid: A physiological role for plant lipooxygenase. Biochem. Biophys. Res. Commun. 111, 470–477

    Google Scholar 

  • Weiler, E.W., Albrecht, T., Groth, B., Xia, Z.-Q., Luxem, M., Liß, H., Andert, L., Spengler, P. (1993) Evidence for the involvement of jasmonates and their octadecanoid precursors in the tendril coiling response of Bryonia dioica. Phytochemistry, in press

  • Wildon, D.C., Thain, J.F., Minchin, P.E.H., Gubb, I.R., Reilly, A.J., Skipper, Y.D., Doherty, H.M., O'Donnell', P.J., Bowles, D.J. (1992) Electrical signalling and systemic proteinase inhibitor induction in the wounded plant. Nature 360, 62–65

    Google Scholar 

  • Wu, K.K., Sanduja, R., Tsai, A.-L., Ferhanoglu, B., Loose-Mitchell, D.S. (1991) Aspirin inhibits interleukin 1-induced prostaglandin H synthase expression in cultured endothelial cells. Proc. Natl. Acad. Sci. USA 88, 2384–2387

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Additional information

We thank Drs. Thomas Altmann and Peter Morris (Institut für Genbiologische Forschung, Berlin, FRG) for critically reading the manuscript. This work was supported by a grant from the Bundesministerium für Forschung und Technologie.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Pena-Cortés, H., Albrecht, T., Prat, S. et al. Aspirin prevents wound-induced gene expression in tomato leaves by blocking jasmonic acid biosynthesis. Planta 191, 123–128 (1993). https://doi.org/10.1007/BF00240903

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00240903

Key words

Navigation