Skip to main content
Plant Physiology logoLink to Plant Physiology
. 1996 Oct;112(2):853–860. doi: 10.1104/pp.112.2.853

Localized Wounding by Heat Initiates the Accumulation of Proteinase Inhibitor II in Abscisic Acid-Deficient Plants by Triggering Jasmonic Acid Biosynthesis.

O Herde 1, R Atzorn 1, J Fisahn 1, C Wasternack 1, L Willmitzer 1, H Pena-Cortes 1
PMCID: PMC158010  PMID: 12226423

Abstract

To test whether the response to electrical current and heat treatment is due to the same signaling pathway that mediates mechanical wounding, we analyzed the effect of electric-current application and localized burning on proteinase inhibitor II (Pin2) gene expression in both wild-type and abscisic acid (ABA)-deficient tomato (Lycopersicon esculentum Mill.) and potato (Solanum phureja) plants. Electric-current application and localized burning led to the accumulation of Pin2 mRNA in potato and tomato wild-type plants. Among the treatments tested, only localized burning of the leaves led to an accumulation of Pin2 mRNA in the ABA-deficient plants. Electric-current application, like mechanical injury, was able to initiate ABA and jasmonic acid (JA) accumulation in wild-type but not in ABA-deficient plants. In contrast, heat treatment led to an accumulation of JA in both wild-type and ABA-deficient plants. Inhibition of JA biosynthesis by aspirin blocked the heat-induced Pin2 gene expression in tomato wild-type leaves. These results suggest that electric current, similar to mechanical wounding, requires the presence of ABA to induce Pin2 gene expression. Conversely, burning of the leaves activates Pin2 gene expression by directly triggering the biosynthesis of JA by an alternative pathway that is independent of endogenous ABA levels.

Full Text

The Full Text of this article is available as a PDF (2.1 MB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Abián J., Gelpí E., Pagès M. Effect of abscisic Acid on the linoleic Acid metabolism in developing maize embryos. Plant Physiol. 1991 Apr;95(4):1277–1283. doi: 10.1104/pp.95.4.1277. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Amasino R. M. Acceleration of nucleic acid hybridization rate by polyethylene glycol. Anal Biochem. 1986 Feb 1;152(2):304–307. doi: 10.1016/0003-2697(86)90413-6. [DOI] [PubMed] [Google Scholar]
  3. Bell E., Creelman R. A., Mullet J. E. A chloroplast lipoxygenase is required for wound-induced jasmonic acid accumulation in Arabidopsis. Proc Natl Acad Sci U S A. 1995 Sep 12;92(19):8675–8679. doi: 10.1073/pnas.92.19.8675. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Doares S. H., Narvaez-Vasquez J., Conconi A., Ryan C. A. Salicylic Acid Inhibits Synthesis of Proteinase Inhibitors in Tomato Leaves Induced by Systemin and Jasmonic Acid. Plant Physiol. 1995 Aug;108(4):1741–1746. doi: 10.1104/pp.108.4.1741. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Enyedi A. J., Yalpani N., Silverman P., Raskin I. Localization, conjugation, and function of salicylic acid in tobacco during the hypersensitive reaction to tobacco mosaic virus. Proc Natl Acad Sci U S A. 1992 Mar 15;89(6):2480–2484. doi: 10.1073/pnas.89.6.2480. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Farmer E. E., Ryan C. A. Interplant communication: airborne methyl jasmonate induces synthesis of proteinase inhibitors in plant leaves. Proc Natl Acad Sci U S A. 1990 Oct;87(19):7713–7716. doi: 10.1073/pnas.87.19.7713. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Farmer E. E., Ryan C. A. Octadecanoid Precursors of Jasmonic Acid Activate the Synthesis of Wound-Inducible Proteinase Inhibitors. Plant Cell. 1992 Feb;4(2):129–134. doi: 10.1105/tpc.4.2.129. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Gaffney T., Friedrich L., Vernooij B., Negrotto D., Nye G., Uknes S., Ward E., Kessmann H., Ryals J. Requirement of salicylic Acid for the induction of systemic acquired resistance. Science. 1993 Aug 6;261(5122):754–756. doi: 10.1126/science.261.5122.754. [DOI] [PubMed] [Google Scholar]
  9. Godoy J. A., Pardo J. M., Pintor-Toro J. A. A tomato cDNA inducible by salt stress and abscisic acid: nucleotide sequence and expression pattern. Plant Mol Biol. 1990 Nov;15(5):695–705. doi: 10.1007/BF00016120. [DOI] [PubMed] [Google Scholar]
  10. Hildmann T., Ebneth M., Peña-Cortés H., Sánchez-Serrano J. J., Willmitzer L., Prat S. General roles of abscisic and jasmonic acids in gene activation as a result of mechanical wounding. Plant Cell. 1992 Sep;4(9):1157–1170. doi: 10.1105/tpc.4.9.1157. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Kernan A., Thornburg R. W. Auxin Levels Regulate the Expression of a Wound-Inducible Proteinase Inhibitor II-Chloramphenicol Acetyl Transferase Gene Fusion in Vitro and in Vivo. Plant Physiol. 1989 Sep;91(1):73–78. doi: 10.1104/pp.91.1.73. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Logemann J., Schell J., Willmitzer L. Improved method for the isolation of RNA from plant tissues. Anal Biochem. 1987 May 15;163(1):16–20. doi: 10.1016/0003-2697(87)90086-8. [DOI] [PubMed] [Google Scholar]
  13. Martini N., Egen M., Rüntz I., Strittmatter G. Promoter sequences of a potato pathogenesis-related gene mediate transcriptional activation selectively upon fungal infection. Mol Gen Genet. 1993 Jan;236(2-3):179–186. doi: 10.1007/BF00277110. [DOI] [PubMed] [Google Scholar]
  14. McGurl B., Orozco-Cardenas M., Pearce G., Ryan C. A. Overexpression of the prosystemin gene in transgenic tomato plants generates a systemic signal that constitutively induces proteinase inhibitor synthesis. Proc Natl Acad Sci U S A. 1994 Oct 11;91(21):9799–9802. doi: 10.1073/pnas.91.21.9799. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Melan M. A., Dong X., Endara M. E., Davis K. R., Ausubel F. M., Peterman T. K. An Arabidopsis thaliana lipoxygenase gene can be induced by pathogens, abscisic acid, and methyl jasmonate. Plant Physiol. 1993 Feb;101(2):441–450. doi: 10.1104/pp.101.2.441. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Pearce G., Strydom D., Johnson S., Ryan C. A. A polypeptide from tomato leaves induces wound-inducible proteinase inhibitor proteins. Science. 1991 Aug 23;253(5022):895–897. doi: 10.1126/science.253.5022.895. [DOI] [PubMed] [Google Scholar]
  17. Peña-Cortés H., Fisahn J., Willmitzer L. Signals involved in wound-induced proteinase inhibitor II gene expression in tomato and potato plants. Proc Natl Acad Sci U S A. 1995 May 9;92(10):4106–4113. doi: 10.1073/pnas.92.10.4106. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Pēna-Cortés H., Sánchez-Serrano J. J., Mertens R., Willmitzer L., Prat S. Abscisic acid is involved in the wound-induced expression of the proteinase inhibitor II gene in potato and tomato. Proc Natl Acad Sci U S A. 1989 Dec;86(24):9851–9855. doi: 10.1073/pnas.86.24.9851. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Ryan C. A. Oligosaccharide signalling in plants. Annu Rev Cell Biol. 1987;3:295–317. doi: 10.1146/annurev.cb.03.110187.001455. [DOI] [PubMed] [Google Scholar]
  20. Staswick P. E., Huang J. F., Rhee Y. Nitrogen and methyl jasmonate induction of soybean vegetative storage protein genes. Plant Physiol. 1991 May;96(1):130–136. doi: 10.1104/pp.96.1.130. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Staswick P. E. Jasmonate, genes, and fragrant signals. Plant Physiol. 1992 Jul;99(3):804–807. doi: 10.1104/pp.99.3.804. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Taylor J. L., Fritzemeier K. H., Häuser I., Kombrink E., Rohwer F., Schröder M., Strittmatter G., Hahlbrock K. Structural analysis and activation by fungal infection of a gene encoding a pathogenesis-related protein in potato. Mol Plant Microbe Interact. 1990 Mar-Apr;3(2):72–77. [PubMed] [Google Scholar]
  23. Thornburg R. W., Li X. Wounding Nicotiana tabacum Leaves Causes a Decline in Endogenous Indole-3-Acetic Acid. Plant Physiol. 1991 Jul;96(3):802–805. doi: 10.1104/pp.96.3.802. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Vernooij B., Uknes S., Ward E., Ryals J. Salicylic acid as a signal molecule in plant-pathogen interactions. Curr Opin Cell Biol. 1994 Apr;6(2):275–279. doi: 10.1016/0955-0674(94)90147-3. [DOI] [PubMed] [Google Scholar]
  25. Vick B. A., Zimmerman D. C. The biosynthesis of jasmonic acid: a physiological role for plant lipoxygenase. Biochem Biophys Res Commun. 1983 Mar 16;111(2):470–477. doi: 10.1016/0006-291x(83)90330-3. [DOI] [PubMed] [Google Scholar]

Articles from Plant Physiology are provided here courtesy of Oxford University Press

RESOURCES