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J. Biol. Chem., Vol. 279, Issue 46, 48205-48213, November 12, 2004

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Different Mechanisms Participate in the R-dependent Activity of the R2R3 MYB Transcription Factor C1^*

J. Marcela Hernandez, George F. Heine, Niloufer G. Irani, Antje Feller, Min-Gab Kim, Todd Matulnik, Vicki L. Chandler¶, and Erich Grotewold||

From the Ohio State Biochemistry Program, Department of Plant Cellular and Molecular Biology, and Plant Biotechnology Center, The Ohio State University, Columbus, Ohio 43210 and the ^¶Department of Plant Sciences, University of Arizona, Tucson, Arizona 85721

The R2R3 MYB transcription factor C1 requires the basic helix-loop-helix factor R as an essential co-activator for the transcription of maize anthocyanin genes. In contrast, the R2R3 MYB protein P1 activates a subset of the C1-regulated genes independently of R. Substitution of six amino acids in P1 with the C1 amino acids results in P1^*, whose activity on C1-regulated and P1-regulated genes is R-dependent or R-enhanced, respectively. We have used P1^* in combination with various promoters to uncover two mechanisms for R function. On synthetic promoters that contain only C1/P1 binding sites, R is an essential co-activator of C1. This function of R is unlikely to simply be the result of an increase in the C1 DNA-binding affinity, since transcriptional activity of a C1 mutant that binds DNA at a higher affinity, comparable with P1, remains R-dependent. The differential transcriptional activity of C1 fusions with the yeast Gal4 DNA-binding domain in yeast and maize cells suggests that part of the function of R is to relieve C1 from a plant-specific inhibitor. A second function of R requires cis-regulatory elements in addition to the C1/P1 DNA-binding sites for R-enhanced transcription of a1. We hypothesize that R functions in this mode by binding or recruiting additional factors to the anthocyanin regulatory element conserved in the promoters of several anthocyanin genes. Together, these findings suggest a model in which combinatorial interactions with co-activators enable R2R3 MYB factors with very similar DNA binding preferences to discriminate between target genes in vivo.

Received for publication, July 12, 2004 , and in revised form, August 27, 2004.

^* This work was funded by National Science Foundation Grants MCB-9896111 and MCB-9974474 and US Dept. of Agriculture Grant NRICGP 2003-02158 (to E. G) and National Science Foundation Grant MCB-9304687 (to V. L. C.). 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.

^|| To whom all correspondence should be addressed: Dept. of Plant Cellular and Molecular Biology and Plant Biotechnology Center, 206 Rightmire Hall, 1060 Carmack Rd., Columbus, OH 43210. Tel.: 614-292-2483; Fax: 614-292-5379; E-mail: grotewold.1{at}osu.edu.

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