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. 1995 Feb;7(2):203–212. doi: 10.1105/tpc.7.2.203

UV-B-Induced PR-1 Accumulation Is Mediated by Active Oxygen Species.

R Green 1, R Fluhr 1
PMCID: PMC160776  PMID: 12242373

Abstract

Depletion of the stratospheric ozone layer may result in an increase in the levels of potentially harmful UV-B radiation reaching the surface of the earth. We have found that UV-B is a potent inducer of the plant pathogenesis-related protein PR-1 in tobacco leaves. UV-B fluences required for PR-1 accumulation are similar to those of other UV-B-induced responses. The UV-B-induced PR-1 accumulation was confined precisely to the irradiated area of the leaf but displayed no leaf tissue specificity. A study of some of the possible components of the signal transduction pathway between UV-B and PR-1 induction showed that photosynthetic processes are not essential, and photoreversible DNA damage is not involved. Antioxidants and cycloheximide were able to block the induction of PR-1 by UV-B, and treatment of leaves with a generator of reactive oxygen resulted in the accumulation of PR-1 protein. These results demonstrate an absolute requirement for active oxygen species and protein synthesis in this UV-B signal transduction pathway. In contrast, we also show that other elicitors, notably salicylic acid, are able to elicit PR-1 via nonreactive oxygen species-requiring pathways.

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Selected References

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  1. Alexander D., Goodman R. M., Gut-Rella M., Glascock C., Weymann K., Friedrich L., Maddox D., Ahl-Goy P., Luntz T., Ward E. Increased tolerance to two oomycete pathogens in transgenic tobacco expressing pathogenesis-related protein 1a. Proc Natl Acad Sci U S A. 1993 Aug 1;90(15):7327–7331. doi: 10.1073/pnas.90.15.7327. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Anderson J. G., Toohey D. W., Brune W. H. Free Radicals Within the Antarctic Vortex: The Role of CFCs in Antarctic Ozone Loss. Science. 1991 Jan 4;251(4989):39–46. doi: 10.1126/science.251.4989.39. [DOI] [PubMed] [Google Scholar]
  3. Aruoma O. I., Halliwell B., Hoey B. M., Butler J. The antioxidant action of N-acetylcysteine: its reaction with hydrogen peroxide, hydroxyl radical, superoxide, and hypochlorous acid. Free Radic Biol Med. 1989;6(6):593–597. doi: 10.1016/0891-5849(89)90066-x. [DOI] [PubMed] [Google Scholar]
  4. Baker C. J., Orlandi E. W., Mock N. M. Harpin, An Elicitor of the Hypersensitive Response in Tobacco Caused by Erwinia amylovora, Elicits Active Oxygen Production in Suspension Cells. Plant Physiol. 1993 Aug;102(4):1341–1344. doi: 10.1104/pp.102.4.1341. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Batschauer A. A plant gene for photolyase: an enzyme catalyzing the repair of UV-light-induced DNA damage. Plant J. 1993 Oct;4(4):705–709. doi: 10.1046/j.1365-313x.1993.04040705.x. [DOI] [PubMed] [Google Scholar]
  6. Beggs C. J., Stolzer-Jehle A., Wellmann E. Isoflavonoid Formation as an Indicator of UV Stress in Bean (Phaseolus vulgaris L.) Leaves : The Significance of Photorepair in Assessing Potential Damage by Increased Solar UV-B Radiation. Plant Physiol. 1985 Nov;79(3):630–634. doi: 10.1104/pp.79.3.630. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Brederode F. T., Linthorst H. J., Bol J. F. Differential induction of acquired resistance and PR gene expression in tobacco by virus infection, ethephon treatment, UV light and wounding. Plant Mol Biol. 1991 Dec;17(6):1117–1125. doi: 10.1007/BF00028729. [DOI] [PubMed] [Google Scholar]
  8. 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]
  9. Cutt J. R., Harpster M. H., Dixon D. C., Carr J. P., Dunsmuir P., Klessig D. F. Disease response to tobacco mosaic virus in transgenic tobacco plants that constitutively express the pathogenesis-related PR1b gene. Virology. 1989 Nov;173(1):89–97. doi: 10.1016/0042-6822(89)90224-9. [DOI] [PubMed] [Google Scholar]
  10. Dangl J. L., Hauffe K. D., Lipphardt S., Hahlbrock K., Scheel D. Parsley protoplasts retain differential responsiveness to u.v. light and fungal elicitor. EMBO J. 1987 Sep;6(9):2551–2556. doi: 10.1002/j.1460-2075.1987.tb02543.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Devary Y., Gottlieb R. A., Lau L. F., Karin M. Rapid and preferential activation of the c-jun gene during the mammalian UV response. Mol Cell Biol. 1991 May;11(5):2804–2811. doi: 10.1128/mcb.11.5.2804. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Devary Y., Gottlieb R. A., Smeal T., Karin M. The mammalian ultraviolet response is triggered by activation of Src tyrosine kinases. Cell. 1992 Dec 24;71(7):1081–1091. doi: 10.1016/s0092-8674(05)80058-3. [DOI] [PubMed] [Google Scholar]
  13. Douglas C., Hoffmann H., Schulz W., Hahlbrock K. Structure and elicitor or u.v.-light-stimulated expression of two 4-coumarate:CoA ligase genes in parsley. EMBO J. 1987 May;6(5):1189–1195. doi: 10.1002/j.1460-2075.1987.tb02353.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Eyal Y., Sagee O., Fluhr R. Dark-induced accumulation of a basic pathogenesis-related (PR-1) transcript and a light requirement for its induction by ethylene. Plant Mol Biol. 1992 Jul;19(4):589–599. doi: 10.1007/BF00026785. [DOI] [PubMed] [Google Scholar]
  15. Fluhr R., Aviv D., Galun E., Edelman M. Efficient induction and selection of chloroplast-encoded antibiotic-resistant mutants in Nicotiana. Proc Natl Acad Sci U S A. 1985 Mar;82(5):1485–1489. doi: 10.1073/pnas.82.5.1485. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Fritze K., Staiger D., Czaja I., Walden R., Schell J., Wing D. Developmental and UV Light Regulation of the Snapdragon Chalcone Synthase Promoter. Plant Cell. 1991 Sep;3(9):893–905. doi: 10.1105/tpc.3.9.893. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Harlow G. R., Jenkins M. E., Pittalwala T. S., Mount D. W. Isolation of uvh1, an Arabidopsis mutant hypersensitive to ultraviolet light and ionizing radiation. Plant Cell. 1994 Feb;6(2):227–235. doi: 10.1105/tpc.6.2.227. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Kochevar I. E. UV-induced protein alterations and lipid oxidation in erythrocyte membranes. Photochem Photobiol. 1990 Oct;52(4):795–800. doi: 10.1111/j.1751-1097.1990.tb08684.x. [DOI] [PubMed] [Google Scholar]
  19. Lam E., Green P. J., Wong M., Chua N. H. Phytochrome activation of two nuclear genes requires cytoplasmic protein synthesis. EMBO J. 1989 Oct;8(10):2777–2783. doi: 10.1002/j.1460-2075.1989.tb08423.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. 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]
  21. Li J., Ou-Lee T. M., Raba R., Amundson R. G., Last R. L. Arabidopsis Flavonoid Mutants Are Hypersensitive to UV-B Irradiation. Plant Cell. 1993 Feb;5(2):171–179. doi: 10.1105/tpc.5.2.171. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Linthorst H. J., Meuwissen R. L., Kauffmann S., Bol J. F. Constitutive expression of pathogenesis-related proteins PR-1, GRP, and PR-S in tobacco has no effect on virus infection. Plant Cell. 1989 Mar;1(3):285–291. doi: 10.1105/tpc.1.3.285. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Lotan T., Fluhr R. Xylanase, a novel elicitor of pathogenesis-related proteins in tobacco, uses a non-ethylene pathway for induction. Plant Physiol. 1990 Jun;93(2):811–817. doi: 10.1104/pp.93.2.811. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Ohshima M., Itoh H., Matsuoka M., Murakami T., Ohashi Y. Analysis of stress-induced or salicylic acid-induced expression of the pathogenesis-related 1a protein gene in transgenic tobacco. Plant Cell. 1990 Feb;2(2):95–106. doi: 10.1105/tpc.2.2.95. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Pang Q., Hays J. B. UV-B-Inducible and Temperature-Sensitive Photoreactivation of Cyclobutane Pyrimidine Dimers in Arabidopsis thaliana. Plant Physiol. 1991 Feb;95(2):536–543. doi: 10.1104/pp.95.2.536. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Raz V., Fluhr R. Ethylene Signal Is Transduced via Protein Phosphorylation Events in Plants. Plant Cell. 1993 May;5(5):523–530. doi: 10.1105/tpc.5.5.523. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Roederer M., Staal F. J., Raju P. A., Ela S. W., Herzenberg L. A., Herzenberg L. A. Cytokine-stimulated human immunodeficiency virus replication is inhibited by N-acetyl-L-cysteine. Proc Natl Acad Sci U S A. 1990 Jun;87(12):4884–4888. doi: 10.1073/pnas.87.12.4884. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Ronai Z. A., Lambert M. E., Weinstein I. B. Inducible cellular responses to ultraviolet light irradiation and other mediators of DNA damage in mammalian cells. Cell Biol Toxicol. 1990 Jan;6(1):105–126. doi: 10.1007/BF00135030. [DOI] [PubMed] [Google Scholar]
  29. Sancar A., Sancar G. B. DNA repair enzymes. Annu Rev Biochem. 1988;57:29–67. doi: 10.1146/annurev.bi.57.070188.000333. [DOI] [PubMed] [Google Scholar]
  30. Schreck R., Albermann K., Baeuerle P. A. Nuclear factor kappa B: an oxidative stress-responsive transcription factor of eukaryotic cells (a review). Free Radic Res Commun. 1992;17(4):221–237. doi: 10.3109/10715769209079515. [DOI] [PubMed] [Google Scholar]
  31. Schulze-Lefert P., Dangl J. L., Becker-André M., Hahlbrock K., Schulz W. Inducible in vivo DNA footprints define sequences necessary for UV light activation of the parsley chalcone synthase gene. EMBO J. 1989 Mar;8(3):651–656. doi: 10.1002/j.1460-2075.1989.tb03422.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Smith D. B., Johnson K. S. Single-step purification of polypeptides expressed in Escherichia coli as fusions with glutathione S-transferase. Gene. 1988 Jul 15;67(1):31–40. doi: 10.1016/0378-1119(88)90005-4. [DOI] [PubMed] [Google Scholar]
  33. Stapleton A. E. Ultraviolet Radiation and Plants: Burning Questions. Plant Cell. 1992 Nov;4(11):1353–1358. doi: 10.1105/tpc.4.11.1353. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Uknes S., Dincher S., Friedrich L., Negrotto D., Williams S., Thompson-Taylor H., Potter S., Ward E., Ryals J. Regulation of pathogenesis-related protein-1a gene expression in tobacco. Plant Cell. 1993 Feb;5(2):159–169. doi: 10.1105/tpc.5.2.159. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Vernooij B., Friedrich L., Morse A., Reist R., Kolditz-Jawhar R., Ward E., Uknes S., Kessmann H., Ryals J. Salicylic Acid Is Not the Translocated Signal Responsible for Inducing Systemic Acquired Resistance but Is Required in Signal Transduction. Plant Cell. 1994 Jul;6(7):959–965. doi: 10.1105/tpc.6.7.959. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Wilson M. I., Greenberg B. M. Specificity and Photomorphogenic Nature of Ultraviolet-B-Induced Cotyledon Curling in Brassica napus L. Plant Physiol. 1993 Jun;102(2):671–677. doi: 10.1104/pp.102.2.671. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Wingender R., Röhrig H., Höricke C., Schell J. cis-regulatory elements involved in ultraviolet light regulation and plant defense. Plant Cell. 1990 Oct;2(10):1019–1026. doi: 10.1105/tpc.2.10.1019. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Zanocco A. L., Pavez R., Videla L. A., Lissi E. A. Antioxidant capacity of diethyldithiocarbamate in a metal independent lipid peroxidative process. Free Radic Biol Med. 1989;7(2):151–156. doi: 10.1016/0891-5849(89)90006-3. [DOI] [PubMed] [Google Scholar]

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