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. 1995 Aug;108(4):1741–1746. doi: 10.1104/pp.108.4.1741

Salicylic Acid Inhibits Synthesis of Proteinase Inhibitors in Tomato Leaves Induced by Systemin and Jasmonic Acid.

S H Doares 1, J Narvaez-Vasquez 1, A Conconi 1, C A Ryan 1
PMCID: PMC157556  PMID: 12228577

Abstract

Salicylic acid (SA) and acetylsalicylic acid (ASA), previously shown to inhibit proteinase inhibitor synthesis induced by wounding, oligouronides (H.M. Doherty, R.R. Selvendran, D.J. Bowles [1988] Physiol Mol Plant Pathol 33: 377-384), and linolenic acid (H. Pena-Cortes, T. Albrecht, S. Prat, E.W. Weiler, L. Willmitzer [1993] Planta 191: 123-128), are shown here to be potent inhibitors of systemin-induced and jasmonic acid (JA)-induced synthesis of proteinase inhibitor mRNAs and proteins. The inhibition by SA and ASA of proteinase inhibitor synthesis induced by systemin and JA, as well as by wounding and oligosaccharide elicitors, provides further evidence that both oligosaccharide and polypeptide inducer molecules utilize the octadecanoid pathway to signal the activation of proteinase inhibitor genes. Tomato (Lycopersicon esculentum) leaves were pulse labeled with [35S]methionine, followed by sodium dodecyl sulfate-polyacrylamide gel electrophoresis, and the inhibitory effects of SA are shown to be specific for the synthesis of a small number of JA-inducible proteins that includes the proteinase inhibitors. Previous results have shown that SA inhibits the conversion of 13S-hydroperoxy linolenic acid to 12-oxo-phytodienoic acid, thereby inhibiting the signaling pathway by blocking synthesis of JA. Here we report that the inhibition of synthesis of proteinase inhibitor proteins and mRNAs by SA in both light and darkness also occurs at a step in the signal transduction pathway, after JA synthesis but preceding transcription of the inhibitor genes.

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Selected References

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

  1. Bishop P. D., Pearce G., Bryant J. E., Ryan C. A. Isolation and characterization of the proteinase inhibitor-inducing factor from tomato leaves. Identity and activity of poly- and oligogalacturonide fragments. J Biol Chem. 1984 Nov 10;259(21):13172–13177. [PubMed] [Google Scholar]
  2. Bradford M. M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem. 1976 May 7;72:248–254. doi: 10.1016/0003-2697(76)90527-3. [DOI] [PubMed] [Google Scholar]
  3. Brown W. E., Ryan C. A. Isolation and characterization of a wound-induced trypsin inhibitor from alfalfa leaves. Biochemistry. 1984 Jul 17;23(15):3418–3422. doi: 10.1021/bi00310a006. [DOI] [PubMed] [Google Scholar]
  4. Conconi A., Widmer R. M., Koller T., Sogo J. M. Two different chromatin structures coexist in ribosomal RNA genes throughout the cell cycle. Cell. 1989 Jun 2;57(5):753–761. doi: 10.1016/0092-8674(89)90790-3. [DOI] [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. Graham J. S., Pearce G., Merryweather J., Titani K., Ericsson L., Ryan C. A. Wound-induced proteinase inhibitors from tomato leaves. I. The cDNA-deduced primary structure of pre-inhibitor I and its post-translational processing. J Biol Chem. 1985 Jun 10;260(11):6555–6560. [PubMed] [Google Scholar]
  9. Joosten M. H., De Wit P. J. Identification of Several Pathogenesis-Related Proteins in Tomato Leaves Inoculated with Cladosporium fulvum (syn. Fulvia fulva) as 1,3-beta-Glucanases and Chitinases. Plant Physiol. 1989 Mar;89(3):945–951. doi: 10.1104/pp.89.3.945. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Lee J. S., Brown W. E., Graham J. S., Pearce G., Fox E. A., Dreher T. W., Ahern K. G., Pearson G. D., Ryan C. A. Molecular characterization and phylogenetic studies of a wound-inducible proteinase inhibitor I gene in Lycopersicon species. Proc Natl Acad Sci U S A. 1986 Oct;83(19):7277–7281. doi: 10.1073/pnas.83.19.7277. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Métraux J. P., Signer H., Ryals J., Ward E., Wyss-Benz M., Gaudin J., Raschdorf K., Schmid E., Blum W., Inverardi B. Increase in salicylic Acid at the onset of systemic acquired resistance in cucumber. Science. 1990 Nov 16;250(4983):1004–1006. doi: 10.1126/science.250.4983.1004. [DOI] [PubMed] [Google Scholar]
  12. 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]
  13. Ryan C. A. Quantitative determination of soluble cellular proteins by radial diffusion in agar gels containing antibodies. Anal Biochem. 1967 Jun;19(3):434–440. doi: 10.1016/0003-2697(67)90233-3. [DOI] [PubMed] [Google Scholar]
  14. Sun D., Wimmers L. E., Turgeon R. Scintillation counting of 14C-labeled soluble and insoluble compounds in plant tissue. Anal Biochem. 1988 Mar;169(2):424–427. doi: 10.1016/0003-2697(88)90307-7. [DOI] [PubMed] [Google Scholar]
  15. Thornburg R. W., An G., Cleveland T. E., Johnson R., Ryan C. A. Wound-inducible expression of a potato inhibitor II-chloramphenicol acetyltransferase gene fusion in transgenic tobacco plants. Proc Natl Acad Sci U S A. 1987 Feb;84(3):744–748. doi: 10.1073/pnas.84.3.744. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Trautman R., Cowan K. M., Wagner G. G. Data processing for radial immunodiffusion. Immunochemistry. 1971 Oct;8(10):901–916. doi: 10.1016/0019-2791(71)90429-0. [DOI] [PubMed] [Google Scholar]
  17. 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]
  18. Wingate V. P., Broadway R. M., Ryan C. A. Isolation and characterization of a novel, developmentally regulated proteinase inhibitor I protein and cDNA from the fruit of a wild species of tomato. J Biol Chem. 1989 Oct 25;264(30):17734–17738. [PubMed] [Google Scholar]
  19. Yalpani N., Silverman P., Wilson T. M., Kleier D. A., Raskin I. Salicylic acid is a systemic signal and an inducer of pathogenesis-related proteins in virus-infected tobacco. Plant Cell. 1991 Aug;3(8):809–818. doi: 10.1105/tpc.3.8.809. [DOI] [PMC free article] [PubMed] [Google Scholar]

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