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J. Biol. Chem., Vol. 283, Issue 33, 22637-22648, August 15, 2008

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The CHD3 Remodeler PICKLE Promotes Trimethylation of Histone H3 Lysine 27^*

Heng Zhang¹, Stanley Dean Rider, Jr.², James T. Henderson, Matthew Fountain, King Chuang, Vasundhara Kandachar, Alexis Simons, Howard J. Edenberg, Jeanne Romero-Severson^¶, William M. Muir^||, and Joe Ogas³

From the Department of Biochemistry, Purdue University, West Lafayette, Indiana 47907-2063, the Department of Biochemistry and Molecular Biology and Center for Medical Genomics, Indiana University School of Medicine, Indianapolis, Indiana 46202, the ^¶Department of Biological Sciences, University of Notre Dame, Notre Dame, Indiana 46556-5645, and the ^||Department of Animal Sciences, Purdue University, West Lafayette, Indiana 47907-2054

CHD3 proteins are ATP-dependent chromatin remodelers that contribute to repression of developmentally regulated genes in both animal and plant systems. In animals, this repression has been linked to a multiple subunit complex, Mi-2/NuRD, whose constituents include a CHD3 protein, a histone deacetylase, and a methyl-CpG-binding domain protein. In Arabidopsis, PICKLE (PKL) codes for a CHD3 protein that acts during germination to repress expression of seed-associated genes. Repression of seed-associated traits is promoted in pkl seedlings by the plant growth regulator gibberellin (GA). We undertook a microarray analysis to determine how PKL and GA act to promote the transition from seed to seedling. We found that PKL and GA act in separate pathways to repress expression of seed-specific genes. Comparison of genomic datasets revealed that PKL-dependent genes are enriched for trimethylation of histone H3 lysine 27 (H3K27me3), a repressive epigenetic mark. Chromatin immunoprecipitation studies demonstrate that PKL promotes H3K27me3 in both germinating seedlings and in adult plants but do not identify a connection between PKL-dependent expression and acetylation levels. Taken together, our analyses illuminate a new pathway by which CHD3 remodelers contribute to repression in eukaryotes.

Received for publication, March 17, 2008 , and in revised form, June 3, 2008.

The amino acid sequence of this protein can be accessed through NCBI Protein Database under NCBI accession number GSE11852 [NCBI GEO] .

^* This work was supported, in whole or in part, by National Institutes of Health Grants R01GM059770-01A1 and 5R01GM59770-02. This work was also supported by a grant from the Indiana 21st Century Research and Development Fund (to J. R. S.). This is journal paper number 2008-18351 of the Purdue University 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.

The on-line version of this article (available at http://www.jbc.org) contains supplemental text, additional references, Fig. S1, and Tables S1–S17.

¹ Supported by funds from the Purdue Research Foundation.

² Supported by funds from BASF.

³ To whom correspondence should be addressed: Dept. of Biochemistry, Purdue University, 175 S. University Ave., West Lafayette, IN 47907-2063. Tel.: 765-496-3969; Fax: 765-494-7897; E-mail: ogas{at}purdue.edu.

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