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J. Biol. Chem., Vol. 283, Issue 35, 23801-23810, August 29, 2008

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Heteromeric Interactions among Ethylene Receptors Mediate Signaling in Arabidopsis^*

Zhiyong Gao, Chi-Kuang Wen¹, Brad M. Binder^¶, Yi-Feng Chen, Jianhong Chang, Yi-Hsuan Chiang, Robert J. Kerris, III, Caren Chang, and G. Eric Schaller²

From the Department of Biological Sciences, Dartmouth College, Hanover, New Hampshire 03755, the ^¶Department of Horticulture, University of Wisconsin, Madison, Wisconsin 53706, and the Department of Cell Biology and Molecular Genetics, University of Maryland, College Park, Maryland 20742

The gaseous hormone ethylene is perceived in Arabidopsis by a five member receptor family that consists of the subfamily 1 receptors ETR1 and ERS1 and the subfamily 2 receptors ETR2, ERS2, and EIN4. Previous work has demonstrated that the basic functional unit for the ethylene receptor, ETR1, is a disulfide-linked homodimer. We demonstrate here that ethylene receptors isolated from Arabidopsis also interact with each other through noncovalent interactions. Evidence that ETR1 associates with other ethylene receptors was obtained by co-purification of ETR1 with tagged versions of ERS1, ETR2, ERS2, and EIN4 from Arabidopsis membrane extracts. ETR1 preferentially associated with the subfamily 2 receptors compared with the subfamily 1 receptor ERS1, but ethylene treatment affected the interactions and relative composition of the receptor complexes. When transgenically expressed in yeast, ETR1 and ERS2 can form disulfide-linked heterodimers. In plant extracts, however, the association of ETR1 and ERS2 can be largely disrupted by treatment with SDS, supporting a higher order noncovalent interaction between the receptors. Yeast two-hybrid analysis demonstrated that the receptor GAF domains are capable of mediating heteromeric receptor interactions. Kinetic analysis of ethylene-insensitive mutants of ETR1 is consistent with their dominance being due in part to an ability to associate with other ethylene receptors. These data suggest that the ethylene receptors exist in plants as clusters in a manner potentially analogous to that found with the histidine kinase-linked chemoreceptors of bacteria and that interactions among receptors contribute to ethylene signal output.

Received for publication, January 24, 2008 , and in revised form, June 23, 2008.

^* This work was supported, in whole or in part, by National Institutes of Health Grant 1R01GM071855 (to C. C.). This work was also supported by Department of Energy Grants DE-FG02-05ER15704 (to G. E. S.) and DE-FG02-99ER20329 (to C. C.), National Science Foundation Grant MCB-0430191 (to G. E. S.), and the University of Maryland Agricultural Experiment Station. 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.

¹ Current address: National Key Laboratory of Plant Molecular Genetics, Institute of Plant Physiology and Ecology, Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences, Shanghai 200032, China.

² To whom correspondence should be addressed. Tel.: 603-646-2525; Fax: 603-646-1347; E-mail: george.e.schaller{at}dartmouth.edu.

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