Hydrogen Peroxide Stimulates Salicylic Acid Biosynthesis in Tobacco (original) (raw)

Abstract

Hydrogen peroxide induced the accumulation of free benzoic acid (BA) and salicylic acid (SA) in tobacco (Nicotiana tabacum L. cv Xanthi-nc) leaves. Six hours after infiltration with 300 mM H2O2, the levels of BA and SA in leaves increased 5-fold over the levels detected in control leaves. The accumulation of BA and SA was preceded by the rapid activation of benzoic acid 2-hydroxylase (BA2H) in the H2O2-infiltrated tissues. This enzyme catalyzes the formation of SA from BA. Enzyme activation could be reproduced in vitro by addition of H2O2 or cumene hydroperoxide to the assay mixture. H2O2 was most effective in vitro when applied at 6 mM. In vitro activation of BA2H by peroxides was inhibited by the catalase inhibitor 3-amino-1,2,4-triazole. We suggest that H2O2 activates SA biosynthesis via two mechanisms. First, H2O2 stimulates BA2H activity directly or via the formation of its substrate, molecular oxygen, in a catalase-mediated reaction. Second, higher BA levels induce the accumulation of BA2H protein in the cells and provide more substrate for this enzyme.

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Selected References

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  1. Apostol I., Heinstein P. F., Low P. S. Rapid Stimulation of an Oxidative Burst during Elicitation of Cultured Plant Cells : Role in Defense and Signal Transduction. Plant Physiol. 1989 May;90(1):109–116. doi: 10.1104/pp.90.1.109. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Babbs C. F., Pham J. A., Coolbaugh R. C. Lethal hydroxyl radical production in paraquat-treated plants. Plant Physiol. 1989 Aug;90(4):1267–1270. doi: 10.1104/pp.90.4.1267. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Chen Z., Silva H., Klessig D. F. Active oxygen species in the induction of plant systemic acquired resistance by salicylic acid. Science. 1993 Dec 17;262(5141):1883–1886. doi: 10.1126/science.8266079. [DOI] [PubMed] [Google Scholar]
  4. Enyedi A. J., Raskin I. Induction of UDP-Glucose:Salicylic Acid Glucosyltransferase Activity in Tobacco Mosaic Virus-Inoculated Tobacco (Nicotiana tabacum) Leaves. Plant Physiol. 1993 Apr;101(4):1375–1380. doi: 10.1104/pp.101.4.1375. [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. Hennig J., Malamy J., Grynkiewicz G., Indulski J., Klessig D. F. Interconversion of the salicylic acid signal and its glucoside in tobacco. Plant J. 1993 Oct;4(4):593–600. doi: 10.1046/j.1365-313x.1993.04040593.x. [DOI] [PubMed] [Google Scholar]
  7. Lamb C. J., Lawton M. A., Dron M., Dixon R. A. Signals and transduction mechanisms for activation of plant defenses against microbial attack. Cell. 1989 Jan 27;56(2):215–224. doi: 10.1016/0092-8674(89)90894-5. [DOI] [PubMed] [Google Scholar]
  8. Legendre L., Heinstein P. F., Low P. S. Evidence for participation of GTP-binding proteins in elicitation of the rapid oxidative burst in cultured soybean cells. J Biol Chem. 1992 Oct 5;267(28):20140–20147. [PubMed] [Google Scholar]
  9. Legendre L., Rueter S., Heinstein P. F., Low P. S. Characterization of the Oligogalacturonide-Induced Oxidative Burst in Cultured Soybean (Glycine max) Cells. Plant Physiol. 1993 May;102(1):233–240. doi: 10.1104/pp.102.1.233. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Leon J., Yalpani N., Raskin I., Lawton M. A. Induction of Benzoic Acid 2-Hydroxylase in Virus-Inoculated Tobacco. Plant Physiol. 1993 Oct;103(2):323–328. doi: 10.1104/pp.103.2.323. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Levine A., Tenhaken R., Dixon R., Lamb C. H2O2 from the oxidative burst orchestrates the plant hypersensitive disease resistance response. Cell. 1994 Nov 18;79(4):583–593. doi: 10.1016/0092-8674(94)90544-4. [DOI] [PubMed] [Google Scholar]
  12. Malamy J., Carr J. P., Klessig D. F., Raskin I. Salicylic Acid: a likely endogenous signal in the resistance response of tobacco to viral infection. Science. 1990 Nov 16;250(4983):1002–1004. doi: 10.1126/science.250.4983.1002. [DOI] [PubMed] [Google Scholar]
  13. Mehdy M. C. Active Oxygen Species in Plant Defense against Pathogens. Plant Physiol. 1994 Jun;105(2):467–472. doi: 10.1104/pp.105.2.467. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. 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]
  15. ROSS A. F. Systemic acquired resistance induced by localized virus infections in plants. Virology. 1961 Jul;14:340–358. doi: 10.1016/0042-6822(61)90319-1. [DOI] [PubMed] [Google Scholar]
  16. Yalpani N., Leon J., Lawton M. A., Raskin I. Pathway of Salicylic Acid Biosynthesis in Healthy and Virus-Inoculated Tobacco. Plant Physiol. 1993 Oct;103(2):315–321. doi: 10.1104/pp.103.2.315. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. 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]