Abstract
The methylation of histone H3 lysine 36 (H3K36) plays critical roles in brassinosteroid (BR)-related processes and is involved in controlling flowering time in rice (Oryza sativa). Although enzymes that catalyze this methylation reaction have been described, little is known about the recognition mechanisms to decipher H3K36 methylation information in rice. In this study, biochemical characterizations showed that MORF-RELATED GENE702 (MRG702) binds to trimethylated H3K4 and H3K36 (H3K4me3 and H3K36me3) in vitro. Similar to the loss-of-function mutants of the rice H3K36 methyltransferase gene SET DOMAIN GROUP725 (SDG725), the MRG702 knockdown mutants displayed typical BR-deficient mutant and late-flowering phenotypes. Gene transcription analyses showed that MRG702 knockdown resulted in the down-regulation of BR-related genes, including DWARF11, BRASSINOSTEROD INSENSITIVE1, and BRASSINOSTEROID UPREGULATED1, and several flowering genes, including Early heading date1 (Ehd1), Ehd2, Ehd3, OsMADS50, Heading date 3a, and RICE FLOWERING LOCUS T1. A binding analysis showed that MRG702 directly binds to the chromatin at target gene loci. This binding is dependent on the level of trimethylated H3K36, which is mediated by SDG725. Together, our results demonstrate that MRG702 acts as a reader protein of H3K4me3 and H3K36me3 and deciphers the H3K36 methylation information set by SDG725. Therefore, the role of MRG702 in the BR pathway and in controlling flowering time in rice is to function as a reader protein to decipher methylation information.
Highlights
IntroductionThe different modifications of histone residues ( known as histone codes) are thought to serve as signals that are recognized by effector modules (reader proteins), which might implement the downstream functions of histone codes (Liu et al, 2010; Berr et al, 2011; Yun et al, 2011)
State Key Laboratory of Genetic Engineering, Collaborative Innovation Center of Genetics and Development, Institute of Plant Biology, School of Life Sciences, Fudan University, Shanghai 200433, China (J.J., J.S., B.L., Y.Y., A.D.); and National Center for Protein Science Shanghai, Graduate University of the Chinese Academy of Sciences, State Key Laboratory of Molecular Biology, Institute of Biochemistry and Cell Biology, Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences, Shanghai 200031, China (Y.L., Y.H.)
Our results demonstrate that MORF-RELATED GENE702 (MRG702) acts as a reader protein of H3K4me3 and H3K36me3 and deciphers the H3K36 methylation information set by SET DOMAIN GROUP725 (SDG725)
Summary
The different modifications of histone residues ( known as histone codes) are thought to serve as signals that are recognized by effector modules (reader proteins), which might implement the downstream functions of histone codes (Liu et al, 2010; Berr et al, 2011; Yun et al, 2011) Recent studies on such effector modules have shown that a variety of reader domains, including chromodomain (chromatin organization modifier domain), plant homeodomain (PHD), Tudor, malignant brain tumor, PWWP (named after a conserved Pro-Trp-Trp-Pro motif), Zinc finger-CW (named after conserved Cys and Trp residues), WD40, and ankyrin repeats, bind to different methylated Lys residues of histones (Yun et al, 2011). CHR729 affects many aspects of plant development as a bifunctional chromatin regulator (Hu et al, 2012)
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