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J. Biol. Chem., Vol. 280, Issue 19, 18810-18821, May 13, 2005

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Cullins 3a and 3b Assemble with Members of the Broad Complex/Tramtrack/Bric-a-Brac (BTB) Protein Family to Form Essential Ubiquitin-Protein Ligases (E3s) in Arabidopsis^*

Derek J. Gingerich, Jennifer M. Gagne, Donald W. Salter, Hanjo Hellmann¶||, Mark Estelle¶, Ligeng Ma, and Richard D. Vierstra**

From the Department of Genetics, University of Wisconsin, Madison, Wisconsin 53706, ^¶Department of Biology, Indiana University, Bloomington, Indiana 47405, ^||Institute for Biology and Applied Genetics, Albrecht-Thaer Weg 6, Freie Universität Berlin, 14195 Berlin, Germany, and Department of Molecular, Cellular and Developmental Biology, Yale University, New Haven, Connecticut 06520-8104

Selective modification of proteins by ubiquitination is directed by diverse families of ubiquitin-protein ligases (or E3s). A large collection of E3s use Cullins (CULs) as scaffolds to form multisubunit E3 complexes in which the CUL binds a target recognition subcomplex and the RBX1 docking protein, which delivers the activated ubiquitin moiety. Arabidopsis and rice contain a large collection of CUL isoforms, indicating that multiple CUL-based E3s exist in plants. Here we show that Arabidopsis CUL3a and CUL3b associate with RBX1 and members of the broad complex/tramtrack/bric-a-brac (BTB) protein family to form BTB E3s. Eighty genes encoding BTB domain-containing proteins were identified in the Arabidopsis genome, indicating that a diverse array of BTB E3s is possible. In addition to the BTB domain, the encoded proteins also contain various other interaction motifs that likely serve as target recognition elements. DNA microarray analyses show that BTB genes are expressed widely in the plant and that tissue-specific and isoform-specific patterns exist. Arabidopsis defective in both CUL3a and CUL3b are embryo-lethal, indicating that BTB E3s are essential for plant development.

Received for publication, November 23, 2004 , and in revised form, February 23, 2005.

Note Added in Proof—A complementary study of CUL3a and the BTB gene family in Arabidopsis was recently published by Dieterle et al. (Plant J. 41, 386–399). It demonstrates several BTB-CUL3 interactions by Y2H analysis, including one with At5g13060 that has not been described elsewhere.

^* This work was supported by grants from the National Science Foundation Arabidopsis 2010 Program (Grant MCB-0115870 to R. D. V. and M. E.), the Research Division of the University of Wisconsin College of Agriculture and Life Sciences (to R. D. V.), a National Institutes of Health postdoctoral fellowship (Grant F32-GM68361 to D. J. G.), and a National Science Foundation Research Opportunity Award fellowship (to D. W. S.). 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. 1, 2, 3, 4 and Data Sets 5 and 6.

Present address: Dept. of Environmental and Biological Sciences, 201C Bibb Graves, University of West Alabama, Livingston, AL 35470.

^** To whom correspondence should be addressed: Dept. of Genetics, 425-G Henry Mall, University of Wisconsin, Madison, WI 53706. Tel.: 608-262-8215; Fax: 608-262-2976; E-mail: vierstra{at}wisc.edu.

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