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J. Biol. Chem., Vol. 282, Issue 35, 25588-25596, August 31, 2007

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Novel Plant-specific Cyclin-dependent Kinase Inhibitors Induced by Biotic and Abiotic Stresses^*

Adrian Peres, Michelle L. Churchman, Srivaidehirani Hariharan^¶||, Kristiina Himanen^¶||1, Aurine Verkest^¶||1, Klaas Vandepoele^¶||2, Zoltan Magyar^¶||, Yves Hatzfeld, Els Van Der Schueren^¶||, Gerrit T. S. Beemster^¶||, Valerie Frankard, John C. Larkin, Dirk Inzé^¶||, and Lieven De Veylder^¶||23

From the CropDesign N.V., B-9052 Ghent, Belgium, the Department of Biological Sciences, Louisiana State University, Baton Rouge, Louisiana 70803, the ^¶Department of Plant Systems Biology, Flanders Institute for Biotechnology (VIB), 9052 Gent, Belgium, and the ^||Department of Molecular Genetics, Ghent University, 9052 Gent, Belgium

The EL2 gene of rice (Oryza sativa), previously classified as early response gene against the potent biotic elicitor N-acetylchitoheptaose and encoding a short polypeptide with unknown function, was identified as a novel cell cycle regulatory gene related to the recently reported SIAMESE (SIM) gene of Arabidopsis thaliana. Iterative two-hybrid screens, in vitro pull-down assays, and fluorescence resonance energy transfer analyses showed that Orysa; EL2 binds the cyclin-dependent kinase (CDK) CDKA1;1 and D-type cyclins. No interaction was observed with the plant-specific B-type CDKs. The amino acid motif ELERFL was identified to be essential for cyclin, but not for CDK binding. Orysa;EL2 impaired the ability of Orysa; CYCD5;3 to complement a budding yeast (Saccharomyces cerevisiae) triple CLN mutant, whereas recombinant protein inhibited CDK activity in vitro. Moreover, Orysa;EL2 was able to rescue the multicellular trichome phenotype of sim mutants of Arabidopsis, unequivocally demonstrating that Orysa;EL2 operates as a cell cycle inhibitor. Orysa;EL2 mRNA levels were induced by cold, drought, and propionic acid. Our data suggest that Orysa;EL2 encodes a new type of plant CDK inhibitor that links cell cycle progression with biotic and abiotic stress responses.

Received for publication, April 20, 2007 , and in revised form, June 8, 2007.

^* This work was supported in part by grants from the Institute for the Promotion of Innovation by Science and Technology in Flanders (TraitQuest Grant 000391), the European Research Training Network DAGOLIGN Project HPRN-CT-2002-00267, and National Science Foundation Grant IOB 0444560 (to M. L. C. and J. C. L.). 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 Recipients of a postdoctoral and a predoctoral fellowship from the Institute for the Promotion by Science and Technology in Flanders, respectively.

² Postdoctoral fellows of the Research Foundation-Flanders.

³ To whom correspondence should be addressed: Dept. Plant Systems Biology, VIB, Ghent University, Technologiepark 927, B-9052 Gent, Belgium. Tel.: 32-9-3313800; Fax: 32-9-3313809; E-mail: lieven.deveylder{at}psb.ugent.be.

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