Skip to main content
PMC home page
Plant Physiology logoLink to Plant Physiology
. 1996 Apr;110(4):1381–1394. doi: 10.1104/pp.110.4.1381

Race-Specific Elicitors of Cladosporium fulvum Induce Changes in Cell Morphology and the Synthesis of Ethylene and Salicylic Acid in Tomato Plants Carrying the Corresponding Cf Disease Resistance Gene.

K E Hammond-Kosack 1, P Silverman 1, I Raskin 1, JDG Jones 1
PMCID: PMC160933  PMID: 12226268

Abstract

Defense responses mediated by the genetically unlinked Cf-9 and Cf-2 genes were compared with those involving no Cf gene (Cf0). Compatible tomato (Lycopersicon esculentum)-Cladosporium fulvum intercellular washing fluids were injected into tomato cotyledons, and the kinetics of responses was monitored under conditions of 70 and 98% relative humidity. The latter conditions suppressed the normal macroscopic responses. For the Cf-9-Avr9 interaction, stomatal opening was induced within 3 to 4 h and after 9 h mesophyll cell death commenced. A burst of ethylene production occurred between 9 and 12.5 h and remained elevated. Free salicylic acid levels increased after 12 h, peaked at 24 h, and thereafter declined. For the Cf-2-Avr2 interaction, stomata became plugged after 8 h, and salicylic acid and ethylene levels increased by 12 and 18 h, respectively, and thereafter declined. Host cell death commenced around vascular tissue by 24 h. Cell death in both incompatible interactions was frequently preceded by cell enlargement. For Cf0-injected plants, no significant responses were detected. High humidity delayed and reduced the Cf-Avr-gene-dependent cell death and ethylene synthesis, whereas induced salicylic acid levels were unaffected for Cf-2-Avr2 and reduced in magnitude only for Cf-9-Avr9.

Full Text

The Full Text of this article is available as a PDF (2.4 MB).

Selected References

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

  1. Baggiolini M., Wymann M. P. Turning on the respiratory burst. Trends Biochem Sci. 1990 Feb;15(2):69–72. doi: 10.1016/0968-0004(90)90179-f. [DOI] [PubMed] [Google Scholar]
  2. Bent A. F., Innes R. W., Ecker J. R., Staskawicz B. J. Disease development in ethylene-insensitive Arabidopsis thaliana infected with virulent and avirulent Pseudomonas and Xanthomonas pathogens. Mol Plant Microbe Interact. 1992 Sep-Oct;5(5):372–378. doi: 10.1094/mpmi-5-372. [DOI] [PubMed] [Google Scholar]
  3. Bowles D. J. Defense-related proteins in higher plants. Annu Rev Biochem. 1990;59:873–907. doi: 10.1146/annurev.bi.59.070190.004301. [DOI] [PubMed] [Google Scholar]
  4. Bradley D. J., Kjellbom P., Lamb C. J. Elicitor- and wound-induced oxidative cross-linking of a proline-rich plant cell wall protein: a novel, rapid defense response. Cell. 1992 Jul 10;70(1):21–30. doi: 10.1016/0092-8674(92)90530-p. [DOI] [PubMed] [Google Scholar]
  5. Brisson L. F., Tenhaken R., Lamb C. Function of Oxidative Cross-Linking of Cell Wall Structural Proteins in Plant Disease Resistance. Plant Cell. 1994 Dec;6(12):1703–1712. doi: 10.1105/tpc.6.12.1703. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. 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]
  7. 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]
  8. Croft KPC., Juttner F., Slusarenko A. J. Volatile Products of the Lipoxygenase Pathway Evolved from Phaseolus vulgaris (L.) Leaves Inoculated with Pseudomonas syringae pv phaseolicola. Plant Physiol. 1993 Jan;101(1):13–24. doi: 10.1104/pp.101.1.13. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Dangl J. L. Pièce de Résistance: novel classes of plant disease resistance genes. Cell. 1995 Feb 10;80(3):363–366. doi: 10.1016/0092-8674(95)90485-9. [DOI] [PubMed] [Google Scholar]
  10. 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]
  11. Dickinson M. J., Jones D. A., Jones J. D. Close linkage between the Cf-2/Cf-5 and Mi resistance loci in tomato. Mol Plant Microbe Interact. 1993 May-Jun;6(3):341–347. doi: 10.1094/mpmi-6-341. [DOI] [PubMed] [Google Scholar]
  12. 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]
  13. Godiard L., Grant M. R., Dietrich R. A., Kiedrowski S., Dangl J. L. Perception and response in plant disease resistance. Curr Opin Genet Dev. 1994 Oct;4(5):662–671. doi: 10.1016/0959-437x(94)90132-m. [DOI] [PubMed] [Google Scholar]
  14. Goldsbrough A. P., Albrecht H., Stratford R. Salicylic acid-inducible binding of a tobacco nuclear protein to a 10 bp sequence which is highly conserved amongst stress-inducible genes. Plant J. 1993 Apr;3(4):563–571. doi: 10.1046/j.1365-313x.1993.03040563.x. [DOI] [PubMed] [Google Scholar]
  15. Hammond-Kosack K. E., Harrison K., Jones J. D. Developmentally regulated cell death on expression of the fungal avirulence gene Avr9 in tomato seedlings carrying the disease-resistance gene Cf-9. Proc Natl Acad Sci U S A. 1994 Oct 25;91(22):10445–10449. doi: 10.1073/pnas.91.22.10445. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Henderson L. M., Chappell J. B., Jones O. T. The superoxide-generating NADPH oxidase of human neutrophils is electrogenic and associated with an H+ channel. Biochem J. 1987 Sep 1;246(2):325–329. doi: 10.1042/bj2460325. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Kearns E. V., Assmann S. M. The Guard Cell-Environment Connection. Plant Physiol. 1993 Jul;102(3):711–715. doi: 10.1104/pp.102.3.711. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Lamb C. J. Plant disease resistance genes in signal perception and transduction. Cell. 1994 Feb 11;76(3):419–422. doi: 10.1016/0092-8674(94)90106-6. [DOI] [PubMed] [Google Scholar]
  19. Lawton K. A., Potter S. L., Uknes S., Ryals J. Acquired Resistance Signal Transduction in Arabidopsis Is Ethylene Independent. Plant Cell. 1994 May;6(5):581–588. doi: 10.1105/tpc.6.5.581. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. 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]
  21. 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]
  22. 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]
  23. May M. J., Hammond-Kosack K. E., Jones JDG. Involvement of Reactive Oxygen Species, Glutathione Metabolism, and Lipid Peroxidation in the Cf-Gene-Dependent Defense Response of Tomato Cotyledons Induced by Race-Specific Elicitors of Cladosporium fulvum. Plant Physiol. 1996 Apr;110(4):1367–1379. doi: 10.1104/pp.110.4.1367. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. 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]
  25. Peever T. L., Higgins V. J. Electrolyte Leakage, Lipoxygenase, and Lipid Peroxidation Induced in Tomato Leaf Tissue by Specific and Nonspecific Elicitors from Cladosporium fulvum. Plant Physiol. 1989 Jul;90(3):867–875. doi: 10.1104/pp.90.3.867. [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. Ryals J., Uknes S., Ward E. Systemic Acquired Resistance. Plant Physiol. 1994 Apr;104(4):1109–1112. doi: 10.1104/pp.104.4.1109. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Sanchez-Casas P., Klessig D. F. A Salicylic Acid-Binding Activity and a Salicylic Acid-Inhibitable Catalase Activity Are Present in a Variety of Plant Species. Plant Physiol. 1994 Dec;106(4):1675–1679. doi: 10.1104/pp.106.4.1675. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Van Kan J. A., Cozijnsen T., Danhash N., De Wit P. J. Induction of tomato stress protein mRNAs by ethephon, 2,6-dichloroisonicotinic acid and salicylate. Plant Mol Biol. 1995 Mar;27(6):1205–1213. doi: 10.1007/BF00020894. [DOI] [PubMed] [Google Scholar]
  30. Vera-Estrella R., Barkla B. J., Higgins V. J., Blumwald E. Plant Defense Response to Fungal Pathogens (Activation of Host-Plasma Membrane H+-ATPase by Elicitor-Induced Enzyme Dephosphorylation). Plant Physiol. 1994 Jan;104(1):209–215. doi: 10.1104/pp.104.1.209. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Widholm J. M. The use of fluorescein diacetate and phenosafranine for determining viability of cultured plant cells. Stain Technol. 1972 Jul;47(4):189–194. doi: 10.3109/10520297209116483. [DOI] [PubMed] [Google Scholar]
  32. de Laat A. M., van Loon L. C. Regulation of Ethylene Biosynthesis in Virus-Infected Tobacco Leaves : I. DETERMINATION OF THE ROLE OF METHIONINE AS THE PRECURSOR OF ETHYLENE. Plant Physiol. 1981 Jul;68(1):256–260. doi: 10.1104/pp.68.1.256. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. van Loon L. C. Induction by 2-chloroethylophosphonic acid of viral-like lesions, associated proteins, and systemic resistance in tobacco. Virology. 1977 Jul 15;80(2):417–420. doi: 10.1016/s0042-6822(77)80016-0. [DOI] [PubMed] [Google Scholar]

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

RESOURCES