Abstract
Exposure of Arabidopsis thaliana to ozone results in the expression of a number of defense-related genes that are also induced during a hypersensitive response. A potential common link between the activation of defense gene expression during a hypersensitive response and by ozone treatment is the production of active oxygen species and the accumulation of hydrogen peroxide. Here we report that salicylic acid accumulation, which can be induced by hydrogen peroxide and is required for the expression of both a hypersensitive response and systemic acquired resistance, is also required for the induction of some, but not all, ozone-induced mRNAs examined. In addition, we show that ozone exposure triggers induced resistance of A. thaliana to infection with virulent phytopathogenic Pseudomonas syringae strains. Infection of transgenic plants expressing salicylate hydroxylase, which prevents the accumulation of salicylic acid, or npr1 mutant plants, which are defective in the expression of systemic acquired resistance at a step downstream of salicylic acid, demonstrated that the signaling pathway activated during ozone-induced resistance overlaps with the systemic acquired resistance activation pathway and is salicylic acid dependent. Interestingly, plants expressing salicylate hydroxylase exhibited increased sensitivity to ozone exposure. These results demonstrate that ozone activates at least two distinct signaling pathways, including a salicylic acid dependent pathway previously shown to be associated with the activation of pathogen defense reactions, and that this latter pathway also induces a protective response to ozone.
Full text
PDF





Images in this article
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- Cao H., Bowling S. A., Gordon A. S., Dong X. Characterization of an Arabidopsis Mutant That Is Nonresponsive to Inducers of Systemic Acquired Resistance. Plant Cell. 1994 Nov;6(11):1583–1592. doi: 10.1105/tpc.6.11.1583. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Chameides W. L., Kasibhatla P. S., Yienger J., Levy H., 2nd Growth of continental-scale metro-agro-plexes, regional ozone pollution, and world food production. Science. 1994 Apr 1;264(5155):74–77. doi: 10.1126/science.264.5155.74. [DOI] [PubMed] [Google Scholar]
- Chandra S., Low P. S. Role of phosphorylation in elicitation of the oxidative burst in cultured soybean cells. Proc Natl Acad Sci U S A. 1995 May 9;92(10):4120–4123. doi: 10.1073/pnas.92.10.4120. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Chen Z., Malamy J., Henning J., Conrath U., Sánchez-Casas P., Silva H., Ricigliano J., Klessig D. K. Induction, modification, and transduction of the salicylic acid signal in plant defense responses. Proc Natl Acad Sci U S A. 1995 May 9;92(10):4134–4137. doi: 10.1073/pnas.92.10.4134. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Conklin P. L., Last R. L. Differential accumulation of antioxidant mRNAs in Arabidopsis thaliana exposed to ozone. Plant Physiol. 1995 Sep;109(1):203–212. doi: 10.1104/pp.109.1.203. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Delaney T. P., Uknes S., Vernooij B., Friedrich L., Weymann K., Negrotto D., Gaffney T., Gut-Rella M., Kessmann H., Ward E., Ryals J. A central role of salicylic Acid in plant disease resistance. Science. 1994 Nov 18;266(5188):1247–1250. doi: 10.1126/science.266.5188.1247. [DOI] [PubMed] [Google Scholar]
- Dietrich R. A., Delaney T. P., Uknes S. J., Ward E. R., Ryals J. A., Dangl J. L. Arabidopsis mutants simulating disease resistance response. Cell. 1994 May 20;77(4):565–577. doi: 10.1016/0092-8674(94)90218-6. [DOI] [PubMed] [Google Scholar]
- Eckey-Kaltenbach H., Ernst D., Heller W., Sandermann H., Jr Biochemical Plant Responses to Ozone (IV. Cross-Induction of Defensive Pathways in Parsley (Petroselinum crispum L.) Plants). Plant Physiol. 1994 Jan;104(1):67–74. doi: 10.1104/pp.104.1.67. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Ernst D., Schraudner M., Langebartels C., Sandermann H., Jr Ozone-induced changes of mRNA levels of beta-1,3-glucanase, chitinase and 'pathogenesis-related' protein 1b in tobacco plants. Plant Mol Biol. 1992 Nov;20(4):673–682. doi: 10.1007/BF00046452. [DOI] [PubMed] [Google Scholar]
- 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]
- Greenberg J. T., Guo A., Klessig D. F., Ausubel F. M. Programmed cell death in plants: a pathogen-triggered response activated coordinately with multiple defense functions. Cell. 1994 May 20;77(4):551–563. doi: 10.1016/0092-8674(94)90217-8. [DOI] [PubMed] [Google Scholar]
- Gundlach H., Müller M. J., Kutchan T. M., Zenk M. H. Jasmonic acid is a signal transducer in elicitor-induced plant cell cultures. Proc Natl Acad Sci U S A. 1992 Mar 15;89(6):2389–2393. doi: 10.1073/pnas.89.6.2389. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kanofsky J. R., Sima P. D. Singlet oxygen generation from the reaction of ozone with plant leaves. J Biol Chem. 1995 Apr 7;270(14):7850–7852. doi: 10.1074/jbc.270.14.7850. [DOI] [PubMed] [Google Scholar]
- Kanofsky J. R., Sima P. Singlet oxygen production from the reactions of ozone with biological molecules. J Biol Chem. 1991 May 15;266(14):9039–9042. [PubMed] [Google Scholar]
- Klessig D. F., Malamy J. The salicylic acid signal in plants. Plant Mol Biol. 1994 Dec;26(5):1439–1458. doi: 10.1007/BF00016484. [DOI] [PubMed] [Google Scholar]
- Krupa S. V., Manning W. J. Atmospheric ozone: formation and effects on vegetation. Environ Pollut. 1988;50(1-2):101–137. doi: 10.1016/0269-7491(88)90187-x. [DOI] [PubMed] [Google Scholar]
- Leon J., Lawton M. A., Raskin I. Hydrogen Peroxide Stimulates Salicylic Acid Biosynthesis in Tobacco. Plant Physiol. 1995 Aug;108(4):1673–1678. doi: 10.1104/pp.108.4.1673. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- 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]
- Mauch-Mani B., Slusarenko A. J. Arabidopsis as a model host for studying plant-pathogen interactions. Trends Microbiol. 1993 Oct;1(7):265–270. doi: 10.1016/0966-842x(93)90049-w. [DOI] [PubMed] [Google Scholar]
- 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]
- Mustafa M. G. Biochemical basis of ozone toxicity. Free Radic Biol Med. 1990;9(3):245–265. doi: 10.1016/0891-5849(90)90035-h. [DOI] [PubMed] [Google Scholar]
- Ryals J., Lawton K. A., Delaney T. P., Friedrich L., Kessmann H., Neuenschwander U., Uknes S., Vernooij B., Weymann K. Signal transduction in systemic acquired resistance. Proc Natl Acad Sci U S A. 1995 May 9;92(10):4202–4205. doi: 10.1073/pnas.92.10.4202. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Schlagnhaufer C. D., Glick R. E., Arteca R. N., Pell E. J. Molecular cloning of an ozone-induced 1-aminocyclopropane-1-carboxylate synthase cDNA and its relationship with a loss of rbcS in potato (Solanum tuberosum L.) plants. Plant Mol Biol. 1995 Apr;28(1):93–103. doi: 10.1007/BF00042041. [DOI] [PubMed] [Google Scholar]
- Schraudner M., Ernst D., Langebartels C., Sandermann H. Biochemical Plant Responses to Ozone : III. Activation of the Defense-Related Proteins beta-1,3-Glucanase and Chitinase in Tobacco Leaves. Plant Physiol. 1992 Aug;99(4):1321–1328. doi: 10.1104/pp.99.4.1321. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Sharma Y. K., Davis K. R. Isolation of a novel Arabidopsis ozone-induced cDNA by differential display. Plant Mol Biol. 1995 Oct;29(1):91–98. doi: 10.1007/BF00019121. [DOI] [PubMed] [Google Scholar]
- Sharma Y. K., Davis K. R. Ozone-Induced Expression of Stress-Related Genes in Arabidopsis thaliana. Plant Physiol. 1994 Aug;105(4):1089–1096. doi: 10.1104/pp.105.4.1089. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Shulaev V., Leon J., Raskin I. Is Salicylic Acid a Translocated Signal of Systemic Acquired Resistance in Tobacco? Plant Cell. 1995 Oct;7(10):1691–1701. doi: 10.1105/tpc.7.10.1691. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Uknes S., Mauch-Mani B., Moyer M., Potter S., Williams S., Dincher S., Chandler D., Slusarenko A., Ward E., Ryals J. Acquired resistance in Arabidopsis. Plant Cell. 1992 Jun;4(6):645–656. doi: 10.1105/tpc.4.6.645. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Wanner L. A., Mittal S., Davis K. R. Recognition of the avirulence gene avrB from Pseudomonas syringae pv. glycinea by Arabidopsis thaliana. Mol Plant Microbe Interact. 1993 Sep-Oct;6(5):582–591. doi: 10.1094/mpmi-6-582. [DOI] [PubMed] [Google Scholar]
- Whalen M. C., Innes R. W., Bent A. F., Staskawicz B. J. Identification of Pseudomonas syringae pathogens of Arabidopsis and a bacterial locus determining avirulence on both Arabidopsis and soybean. Plant Cell. 1991 Jan;3(1):49–59. doi: 10.1105/tpc.3.1.49. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Willekens H., Van Camp W., Van Montagu M., Inze D., Langebartels C., Sandermann H., Jr Ozone, Sulfur Dioxide, and Ultraviolet B Have Similar Effects on mRNA Accumulation of Antioxidant Genes in Nicotiana plumbaginifolia L. Plant Physiol. 1994 Nov;106(3):1007–1014. doi: 10.1104/pp.106.3.1007. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- 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]