Skip to main content
Plant Physiology logoLink to Plant Physiology
. 1997 Apr;113(4):1319–1327. doi: 10.1104/pp.113.4.1319

Identification of a Soluble, High-Affinity Salicylic Acid-Binding Protein in Tobacco.

H Du 1, D F Klessig 1
PMCID: PMC158255  PMID: 12223676

Abstract

Salicylic acid (SA) is a key component in the signal transduction pathway(s), leading to the activation of certain defense responses in plants after pathogen attack. Previous studies have identified several proteins, including catalase and ascorbate peroxidase, through which the SA signal might act. Here we describe a new SA-binding protein. This soluble protein is present in low abundance in tobacco (Nicotiana tabacum) leaves and has an apparent molecular weight of approximately 25,000. It reversibly binds SA with an apparent dissociation constant of 90 nM, an affinity that is 150-fold higher than that between SA and catalase. The ability of most analogs of SA to compete with labeled SA for binding to this protein correlated with their ability to induce defense gene expression and enhanced resistance. Strikingly, benzothiadiazole, a recently described chemical activator that induces plant defenses and disease resistance at very low rates of application, was the strongest competitor, being much more effective than unlabeled SA. The possible role of this SA-binding protein in defense signal transduction is discussed.

Full Text

The Full Text of this article is available as a PDF (1.5 MB).

Selected References

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

  1. Abad P., Marais A., Cardin L., Poupet A., Ponchet M. The effect of benzoic acid derivatives on Nicotiana tabacum growth in relation to PR-b1 production. Antiviral Res. 1988 Aug;9(5):315–327. doi: 10.1016/0166-3542(88)90026-5. [DOI] [PubMed] [Google Scholar]
  2. Basse C. W., Fath A., Boller T. High affinity binding of a glycopeptide elicitor to tomato cells and microsomal membranes and displacement by specific glycan suppressors. J Biol Chem. 1993 Jul 15;268(20):14724–14731. [PubMed] [Google Scholar]
  3. Baureithel K., Felix G., Boller T. Specific, high affinity binding of chitin fragments to tomato cells and membranes. Competitive inhibition of binding by derivatives of chitooligosaccharides and a Nod factor of Rhizobium. J Biol Chem. 1994 Jul 8;269(27):17931–17938. [PubMed] [Google Scholar]
  4. Bi Y. M., Kenton P., Mur L., Darby R., Draper J. Hydrogen peroxide does not function downstream of salicylic acid in the induction of PR protein expression. Plant J. 1995 Aug;8(2):235–245. doi: 10.1046/j.1365-313x.1995.08020235.x. [DOI] [PubMed] [Google Scholar]
  5. 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]
  6. Chang C., Kwok S. F., Bleecker A. B., Meyerowitz E. M. Arabidopsis ethylene-response gene ETR1: similarity of product to two-component regulators. Science. 1993 Oct 22;262(5133):539–544. doi: 10.1126/science.8211181. [DOI] [PubMed] [Google Scholar]
  7. Chen Z., Ricigliano J. W., Klessig D. F. Purification and characterization of a soluble salicylic acid-binding protein from tobacco. Proc Natl Acad Sci U S A. 1993 Oct 15;90(20):9533–9537. doi: 10.1073/pnas.90.20.9533. [DOI] [PMC free article] [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. Cheong J. J., Hahn M. G. A specific, high-affinity binding site for the hepta-beta-glucoside elicitor exists in soybean membranes. Plant Cell. 1991 Feb;3(2):137–147. doi: 10.1105/tpc.3.2.137. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Conrath U., Chen Z., Ricigliano J. R., Klessig D. F. Two inducers of plant defense responses, 2,6-dichloroisonicotinec acid and salicylic acid, inhibit catalase activity in tobacco. Proc Natl Acad Sci U S A. 1995 Aug 1;92(16):7143–7147. doi: 10.1073/pnas.92.16.7143. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Delaney T. P., Friedrich L., Ryals J. A. Arabidopsis signal transduction mutant defective in chemically and biologically induced disease resistance. Proc Natl Acad Sci U S A. 1995 Jul 3;92(14):6602–6606. doi: 10.1073/pnas.92.14.6602. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. 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]
  13. 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]
  14. Durner J., Klessig D. F. Salicylic acid is a modulator of tobacco and mammalian catalases. J Biol Chem. 1996 Nov 8;271(45):28492–28501. doi: 10.1074/jbc.271.45.28492. [DOI] [PubMed] [Google Scholar]
  15. 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]
  16. Görlach J., Volrath S., Knauf-Beiter G., Hengy G., Beckhove U., Kogel K. H., Oostendorp M., Staub T., Ward E., Kessmann H. Benzothiadiazole, a novel class of inducers of systemic acquired resistance, activates gene expression and disease resistance in wheat. Plant Cell. 1996 Apr;8(4):629–643. doi: 10.1105/tpc.8.4.629. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. 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]
  18. Kooman-Gersmann M., Honee G., Bonnema G., De Wit PJGM. A High-Affinity Binding Site for the AVR9 Peptide Elicitor of Cladosporium fulvum Is Present on Plasma Membranes of Tomato and Other Solanaceous Plants. Plant Cell. 1996 May;8(5):929–938. doi: 10.1105/tpc.8.5.929. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Leslie C. A., Romani R. J. Inhibition of ethylene biosynthesis by salicylic Acid. Plant Physiol. 1988 Nov;88(3):833–837. doi: 10.1104/pp.88.3.833. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Löbler M., Klämbt D. Auxin-binding protein from coleoptile membranes of corn (Zea mays L.). I. Purification by immunological methods and characterization. J Biol Chem. 1985 Aug 15;260(17):9848–9853. [PubMed] [Google Scholar]
  21. 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]
  22. 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]
  23. Nürnberger T., Nennstiel D., Jabs T., Sacks W. R., Hahlbrock K., Scheel D. High affinity binding of a fungal oligopeptide elicitor to parsley plasma membranes triggers multiple defense responses. Cell. 1994 Aug 12;78(3):449–460. doi: 10.1016/0092-8674(94)90423-5. [DOI] [PubMed] [Google Scholar]
  24. 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]
  25. Rüffer M., Steipe B., Zenk M. H. Evidence against specific binding of salicylic acid to plant catalase. FEBS Lett. 1995 Dec 18;377(2):175–180. doi: 10.1016/0014-5793(95)01334-2. [DOI] [PubMed] [Google Scholar]
  26. Schaller G. E., Bleecker A. B. Ethylene-binding sites generated in yeast expressing the Arabidopsis ETR1 gene. Science. 1995 Dec 15;270(5243):1809–1811. doi: 10.1126/science.270.5243.1809. [DOI] [PubMed] [Google Scholar]
  27. Shah J., Tsui F., Klessig D. F. Characterization of a salicylic acid-insensitive mutant (sai1) of Arabidopsis thaliana, identified in a selective screen utilizing the SA-inducible expression of the tms2 gene. Mol Plant Microbe Interact. 1997 Jan;10(1):69–78. doi: 10.1094/MPMI.1997.10.1.69. [DOI] [PubMed] [Google Scholar]
  28. Summermatter K., Sticher L., Metraux J. P. Systemic Responses in Arabidopsis thaliana Infected and Challenged with Pseudomonas syringae pv syringae. Plant Physiol. 1995 Aug;108(4):1379–1385. doi: 10.1104/pp.108.4.1379. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. 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]
  30. Wagner A. M. A role for active oxygen species as second messengers in the induction of alternative oxidase gene expression in Petunia hybrida cells. FEBS Lett. 1995 Jul 17;368(2):339–342. doi: 10.1016/0014-5793(95)00688-6. [DOI] [PubMed] [Google Scholar]

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

RESOURCES