Skip to main content
PMC home page
The Plant Cell logoLink to The Plant Cell
. 1996 Feb;8(2):203–212. doi: 10.1105/tpc.8.2.203

Production of Salicylic Acid Precursors Is a Major Function of Phenylalanine Ammonia-Lyase in the Resistance of Arabidopsis to Peronospora parasitica.

B Mauch-Mani 1, A J Slusarenko 1
PMCID: PMC161092  PMID: 12239383

Abstract

Arabidopsis ecotype Columbia (Col-0) seedlings, transformed with a phenylalanine ammonia-lyase 1 promoter (PAL1)-[beta]-glucuronidase (GUS) reporter construct, were inoculated with virulent and avirulent isolates of Peronospora parasitica. The PAL1 promoter was constitutively active in the light in vascular tissue but was induced only in the vicinity of fungal structures in the incompatible interaction. A double-staining procedure was developed to distinguish between GUS activity and fungal structures. The PAL1 promoter was activated in cells undergoing lignification in the incompatible interaction in response to the pathogen. Pretreatment of the seedlings with 2-aminoindan-2-phosphonic acid (AIP), a highly specific PAL inhibitor, made the plants completely susceptible. Lignification was suppressed after AIP treatment, and surprisingly, pathogen-induced PAL1 promoter activity could not be detected. Treatment of the seedlings with 2-hydroxyphenylaminosulphinyl acetic acid (1,1-dimethyl ester) (OH-PAS), a cinnamyl alcohol dehydrogenase inhibitor specific for the lignification pathway, also caused a shift toward susceptibility, but the effect was not as pronounced as it was with AIP. Significantly, although OH-PAS suppressed pathogen-induced lignification, it did not suppress pathogen-induced PAL1 promoter activation. Salicylic acid (SA), supplied to AIP-treated plants, restored resistance and both pathogen-induced lignification and activation of the PAL1 promoter. Endogenous SA levels increased significantly in the incompatible but not in the compatible combination, and this increase was suppressed by AIP but not by OH-PAS. These results provide evidence of the central role of SA in genetically determined plant disease resistance and show that lignification per se, although providing a component of the resistance mechanism, is not the deciding factor between resistance and susceptibility.

Full Text

The Full Text of this article is available as a PDF (1.3 MB).

Selected References

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

  1. 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: 10.1006/abio.1976.9999. [DOI] [PubMed] [Google Scholar]
  2. 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]
  3. 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]
  4. Feuillet C., Lauvergeat V., Deswarte C., Pilate G., Boudet A., Grima-Pettenati J. Tissue- and cell-specific expression of a cinnamyl alcohol dehydrogenase promoter in transgenic poplar plants. Plant Mol Biol. 1995 Feb;27(4):651–667. doi: 10.1007/BF00020220. [DOI] [PubMed] [Google Scholar]
  5. 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]
  6. Grand C., Sarni F., Lamb C. J. Rapid induction by fungal elicitor of the synthesis of cinnamyl-alcohol dehydrogenase, a specific enzyme of lignin synthesis. Eur J Biochem. 1987 Nov 16;169(1):73–77. doi: 10.1111/j.1432-1033.1987.tb13582.x. [DOI] [PubMed] [Google Scholar]
  7. Koch E., Slusarenko A. Arabidopsis is susceptible to infection by a downy mildew fungus. Plant Cell. 1990 May;2(5):437–445. doi: 10.1105/tpc.2.5.437. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. 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]
  9. 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]
  10. Moerschbacher B. M., Noll U., Gorrichon L., Reisener H. J. Specific inhibition of lignification breaks hypersensitive resistance of wheat to stem rust. Plant Physiol. 1990 Jun;93(2):465–470. doi: 10.1104/pp.93.2.465. [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. Ohl S., Hedrick S. A., Chory J., Lamb C. J. Functional properties of a phenylalanine ammonia-lyase promoter from Arabidopsis. Plant Cell. 1990 Sep;2(9):837–848. doi: 10.1105/tpc.2.9.837. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Silverman P., Seskar M., Kanter D., Schweizer P., Metraux J. P., Raskin I. Salicylic Acid in Rice (Biosynthesis, Conjugation, and Possible Role). Plant Physiol. 1995 Jun;108(2):633–639. doi: 10.1104/pp.108.2.633. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Tsuji J., Jackson E. P., Gage D. A., Hammerschmidt R., Somerville S. C. Phytoalexin Accumulation in Arabidopsis thaliana during the Hypersensitive Reaction to Pseudomonas syringae pv syringae. Plant Physiol. 1992 Apr;98(4):1304–1309. doi: 10.1104/pp.98.4.1304. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. 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]
  16. 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]
  17. Ward E. R., Uknes S. J., Williams S. C., Dincher S. S., Wiederhold D. L., Alexander D. C., Ahl-Goy P., Metraux J. P., Ryals J. A. Coordinate Gene Activity in Response to Agents That Induce Systemic Acquired Resistance. Plant Cell. 1991 Oct;3(10):1085–1094. doi: 10.1105/tpc.3.10.1085. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Wyrambik D., Grisebach H. Purification and properties of isoenzymes of cinnamyl-alcohol dehydrogenase from soybean-cell-suspension cultures. Eur J Biochem. 1975 Nov 1;59(1):9–15. doi: 10.1111/j.1432-1033.1975.tb02418.x. [DOI] [PubMed] [Google Scholar]
  19. 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]

Articles from The Plant Cell are provided here courtesy of Oxford University Press

RESOURCES