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

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.

[1]  D. Klessig,et al.  Development of necrosis and activation of disease resistance in transgenic tobacco plants with severely reduced catalase levels. , 1997, The Plant journal : for cell and molecular biology.

[2]  D. Klessig,et al.  Protein dephosphorylation mediates salicylic acid‐induced expression of PR‐1 genes in tobacco , 1997 .

[3]  D. Klessig,et al.  Salicylic Acid Is a Modulator of Tobacco and Mammalian Catalases* , 1996, The Journal of Biological Chemistry.

[4]  D. Inzé,et al.  Transgenic tobacco with a reduced catalase activity develops necrotic lesions and induces pathogenesis‐related expression under high light , 1996 .

[5]  J. Ryals,et al.  A benzothiadiazole derivative induces systemic acquired resistance in tobacco , 1996 .

[6]  G. Vanlerberghe,et al.  Signals Regulating the Expression of the Nuclear Gene Encoding Alternative Oxidase of Plant Mitochondria , 1996, Plant physiology.

[7]  G. Bonnema,et al.  A High-Affinity Binding Site for the AVR9 Peptide Elicitor of Cladosporium fulvum Is Present on Plasma Membranes of Tomato and Other Solanaceous Plants. , 1996, The Plant cell.

[8]  S. Volrath,et al.  Benzothiadiazole, a novel class of inducers of systemic acquired resistance, activates gene expression and disease resistance in wheat. , 1996, The Plant cell.

[9]  D. Klessig,et al.  Dissection of the salicylic acid signaling pathway in tobacco , 1996 .

[10]  D. Klessig,et al.  Salicylic Acid—an Important Signal in Plants , 1996 .

[11]  B. Steipe,et al.  Evidence against specific binding of salicylic acid to plant catalase , 1995, FEBS letters.

[12]  G. Eric Schaller,et al.  Ethylene-Binding Sites Generated in Yeast Expressing the Arabidopsis ETR1 Gene , 1995, Science.

[13]  D. Klessig,et al.  Inhibition of ascorbate peroxidase by salicylic acid and 2,6-dichloroisonicotinic acid, two inducers of plant defense responses. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[14]  J. Ryals,et al.  Is hydrogen peroxide a second messenger of salicylic acid in systemic acquired resistance , 1995 .

[15]  D. Klessig,et al.  Two inducers of plant defense responses, 2,6-dichloroisonicotinec acid and salicylic acid, inhibit catalase activity in tobacco. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[16]  I. Raskin,et al.  Hydrogen Peroxide Stimulates Salicylic Acid Biosynthesis in Tobacco , 1995, Plant physiology.

[17]  J. Draper,et al.  Hydrogen peroxide does not function downstream of salicylic acid in the induction of PR protein expression. , 1995, The Plant journal : for cell and molecular biology.

[18]  A. Wagner.  A role for active oxygen species as second messengers in the induction of alternative oxidase gene expression in Petunia hybrida cells , 1995, FEBS letters.

[19]  J. Ryals,et al.  Arabidopsis signal transduction mutant defective in chemically and biologically induced disease resistance. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[20]  J. Ryals,et al.  2,6-Dichloroisonicotinic acid-induced resistance to pathogens without the accumulation of salicylic acid , 1995 .

[21]  D. Klessig,et al.  A mutation in Arabidopsis that leads to constitutive expression of systemic acquired resistance. , 1994, The Plant cell.

[22]  E. Ward,et al.  A Central Role of Salicylic Acid in Plant Disease Resistance , 1994, Science.

[23]  Xinnian Dong,et al.  Characterization of an Arabidopsis Mutant That Is Nonresponsive to Inducers of Systemic Acquired Resistance. , 1994, The Plant cell.

[24]  T. Jabs,et al.  High affinity binding of a fungal oligopeptide elicitor to parsley plasma membranes triggers multiple defense responses , 1994, Cell.

[25]  T. Boller,et al.  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. , 1994, The Journal of biological chemistry.

[26]  E. Ward,et al.  Salicylic Acid Is Not the Translocated Signal Responsible for Inducing Systemic Acquired Resistance but Is Required in Signal Transduction. , 1994, The Plant cell.

[27]  J. Dangl,et al.  Arabidopsis mutants simulating disease resistance response , 1994, Cell.

[28]  F. Ausubel,et al.  Programmed cell death in plants: A pathogen-triggered response activated coordinately with multiple defense functions , 1994, Cell.

[29]  Alan M. Jones,et al.  Auxin-Binding Proteins , 1994 .

[30]  D. Klessig,et al.  Active oxygen species in the induction of plant systemic acquired resistance by salicylic acid. , 1993, Science.

[31]  E. Meyerowitz,et al.  Arabidopsis ethylene-response gene ETR1: similarity of product to two-component regulators. , 1993, Science.

[32]  D. Klessig,et al.  Purification and characterization of a soluble salicylic acid-binding protein from tobacco. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[33]  Leslie Friedrich,et al.  Requirement of Salicylic Acid for the Induction of Systemic Acquired Resistance , 1993, Science.

[34]  T. Boller,et al.  High affinity binding of a glycopeptide elicitor to tomato cells and microsomal membranes and displacement by specific glycan suppressors. , 1993, The Journal of biological chemistry.

[35]  I. Raskin,et al.  Localization, conjugation, and function of salicylic acid in tobacco during the hypersensitive reaction to tobacco mosaic virus. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[36]  D. Klessig,et al.  Temperature-Dependent Induction of Salicylic Acid and Its Conjugates during the Resistance Response to Tobacco Mosaic Virus Infection. , 1992, The Plant cell.

[37]  R. Hammerschmidt,et al.  Systemic Induction of Salicylic Acid Accumulation in Cucumber after Inoculation with Pseudomonas syringae pv syringae. , 1991, Plant physiology.

[38]  D. Klessig,et al.  Identification of a soluble salicylic acid-binding protein that may function in signal transduction in the plant disease-resistance response. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

[39]  M. Hahn,et al.  A specific, high-affinity binding site for the hepta-beta-glucoside elicitor exists in soybean membranes. , 1991, The Plant cell.

[40]  E. Ward,et al.  Induced Systemic Resistance in Cucumber in Response to 2,6-Dichloro-Isonicotinic Acid and Pathogens , 1991 .

[41]  D F Klessig,et al.  Salicylic Acid: A Likely Endogenous Signal in the Resistance Response of Tobacco to Viral Infection , 1990, Science.

[42]  H. Signer,et al.  Increase in Salicylic Acid at the Onset of Systemic Acquired Resistance in Cucumber , 1990, Science.

[43]  C. Leslie,et al.  Inhibition of ethylene biosynthesis by salicylic Acid. , 1988, Plant physiology.

[44]  M. Ponchet,et al.  The effect of benzoic acid derivatives on Nicotiana tabacum growth in relation to PR-b1 production. , 1988, Antiviral research.

[45]  D. Klämbt,et al.  Auxin-binding protein from coleoptile membranes of corn (Zea mays L.). II. Localization of a putative auxin receptor. , 1985, The Journal of biological chemistry.

[46]  J. Antoniw,et al.  The effects of aspirin and polyacrylic acid on soluble leaf proteins and resistance to virus infection in five cultivars of tobacco. , 1980 .

[47]  R. F. White.  Acetylsalicylic acid (aspirin) induces resistance to tobacco mosaic virus in tobacco. , 1979, Virology.

[48]  M. M. Bradford.  A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. , 1976, Analytical biochemistry.