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J. Biol. Chem., Vol. 283, Issue 28, 19804-19815, July 11, 2008

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Dimerization Controls the Activity of Fungal Elicitors That Trigger Systemic Resistance in Plants^*

Walter A. Vargas, Slavica Djonovi¹, Serenella A. Sukno, and Charles M. Kenerley²

From the Department of Plant Pathology and Microbiology, Texas A&M University, College Station, Texas 77843 and Centro Hispano-Luso de Investigaciones Agrarias, Departamento de Microbiología y Genética, Universidad de Salamanca, 37007 Salamanca, Spain

The soilborne fungus Trichoderma virens secretes a small protein (Sm1) that induces local and systemic defenses in plants. This protein belongs to the ceratoplatanin protein family and is mainly present as a monomer in culture filtrates. However, Hypocrea atroviride (the telomorph form of Trichoderma atroviride) secretes an Sm1-homologous protein, Epl1, with high levels of dimerization. Nonetheless, the molecular mechanisms involved in recognition and the signaling pathways involved in the induction of systemic resistance in plants are still unclear. In this report, we demonstrate that Sm1 and Epl1 are mainly produced as monomer and a dimer, respectively, in the presence of maize seedlings. The results presented show that the ability to induce plant defenses reside only in the monomeric form of both Sm1 and Epl1, and we demonstrate for the first time that the monomeric form of Epl1, likewise Sm1, induces defenses in maize plants. Biochemical analyses indicate that monomeric Sm1 is produced as a glycoprotein, but the glycosyl moiety is missing from its dimeric form, and Epl1 is produced as a nonglycosylated protein. Moreover, for Sm1 homologues in various fungal strains, there is a negative correlation between the presence of the glycosylation site and their ability to aggregate. We propose a subdivision in the ceratoplatanin protein family according to the presence of the glycosylation site and the ability of the proteins to aggregate. The data presented suggest that the elicitor's aggregation may control the Trichoderma-plant molecular dialogue and block the activation of induced systemic resistance in plants.

Received for publication, April 8, 2008 , and in revised form, May 9, 2008.

^* This work was supported by United States Department of Agriculture National Research Initiative Grant 2003-35316-13861 and National Science Foundation Grant IOB0445650 (to C. M. K.). The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

The on-line version of this article (available at http://www.jbc.org) contains supplemental Figs. S1-S5.

¹ Present address: Dept. of Molecular Biology, Massachusetts General Hospital and Department of Genetics, Harvard Medical School, Boston, MA 02114.

² To whom correspondence should be addressed: 413C LF Peterson, TX A&M University, College Station, TX 77843. Tel.: 979-845-7544; Fax: 979-845-6483; E-mail: c-kenerley{at}tamu.edu.

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