H3K36 methylation is critical for brassinosteroid‐regulated plant growth and development in rice

Abstract

SUMMARYMethylation of histone lysine residues plays an essential role in epigenetic regulation of gene expression in eukaryotes. Enzymes involved in establishment of the repressive H3K9 and H3K27 methylation marks have been previously characterized, but the deposition and function of H3K4 and H3K36 methylation remain uncharacterized in rice. Here, we report that rice SDG725 encodes a H3K36 methyltransferase, and its downregulation causes wide-ranging defects, including dwarfism, shortened internodes, erect leaves and small seeds. These defects resemble the phenotypes previously described for some brassinosteroid-knockdown mutants. Consistently, transcriptome analyses revealed that SDG725 depletion results in down-regulation by more than two-fold of over 1000 genes, including D11, BRI1 and BU1, which are known to be involved in brassinosteroid biosynthesis or signaling pathways. Chromatin immunoprecipitation analyses showed that levels of H3K36me2/3 are reduced in chromatin at some regions of these brassinosteroid-related genes in SDG725 knockdown plants, and that SDG725 protein is able to directly bind to these target genes. Taken together, our data indicate that SDG725-mediated H3K36 methylation modulates brassinosteroid-related gene expression, playing an important role in rice plant growth and development.

The Histone Methyltransferase SDG724 Mediates H3K36me2/3 Deposition at MADS50 and RFT1 and Promotes Flowering in Rice

“…SDG724 is a class II SET domain protein and is constitutively expressed in various kinds of tissues (see Supplemental Figure 10 online). Members of this class, including SDG4, SDG8, and SDG25 in Arabidopsis and SDG725 in rice, were shown to have H3K36 methylation activities (Zhao et al, 2005;Cartagena et al, 2008;Dong et al, 2008;Cazzonelli et al, 2009b;Grini et al, 2009;Berr et al, 2010a;Ko et al, 2010;Sui et al, 2012). Our study demonstrated that SDG724 is a major factor for H3K36me3 deposition in rice for the following reasons.…”

“…In the rice genome, at least 35 SET protein coding genes were annotated (Ng et al, 2007), but few have been characterized (Liang et al, 2003;Thakur et al, 2003;B. Ding et al, 2007;Qin et al, 2010;Sui et al, 2012). The plant SET domain-containing (C) Analysis of the global levels of H3K36me1/2/3, H3K4me1/2/3, and H3K9me2 markers in wild-type (WT), lvp1-1, and lvp1-2 plants using H3K methylation tag-specific antibodies.…”

“…Histone Lys methylation in plants functions in biological processes such as flowering transition, floral organ development, carotenoid biosynthesis, shoot and root branching, pollen and macro-trichome development, and the brassinosteroid signaling pathway (Kim et al, 2005;Zhao et al, 2005;Dong et al, 2008;Cazzonelli et al, 2009aCazzonelli et al, , 2009bGrini et al, 2009;Berr et al, 2011;Deal and Henikoff, 2011;Feng and Jacobsen, 2011;Thorstensen et al, 2011;Sui et al, 2012). In Arabidopsis, FLOWERING LOCUS C (FLC) and other flowering time genes are regulated by different kinds of histone Lys methylations (Michaels and Amasino, 1999;He and Amasino, 2005;He, 2009;Berr et al, 2011;Deal and Henikoff, 2011;Feng and Jacobsen, 2011;Thorstensen et al, 2011).…”

The Chromatin-Remodeling Factor PICKLE Integrates Brassinosteroid and Gibberellin Signaling during Skotomorphogenic Growth in Arabidopsis

“…mutant plants but was upregulated in REF6 overexpression plants, in which the H3K27me3 level at this locus was decreased (Lu et al, 2011). Moreover, H3K36 methylation was shown to regulate BR-related gene expression and plant development in rice (Oryza sativa; Sui et al, 2012). In addition, a proteomic study identified several BR-responsive nucleus-enriched proteins, including nucleosome assembly proteins, HISTONE DEACETY-LASE 2B, and VERNALIZATION INDEPENDENCE3, suggesting that BR-induced gene expression is regulated by chromatin remodeling (Shigeta et al, 2011a(Shigeta et al, , 2011b.…”

MORF-RELATED GENE702, a Reader Protein of Trimethylated Histone H3 Lysine 4 and Histone H3 Lysine 36, Is Involved in Brassinosteroid-Regulated Growth and Flowering Time Control in Rice

“…Arabidopsis SDG8, also named ASH1 HOMOLOG2, EARLY FLOWERING IN SHORT DAYS, or CAROTENOID CHLOROPLAST REGULATORY1, is the major H3K36 methyltransferase, and its loss-of-function mutants also show pleiotropic defects, including early flowering, reduced organ size, increased shoot branching, altered carotenoid composition, misformed reproductive organs, reduced fertility, and impaired defenses against pathogens (Kim et al, 2005;Zhao et al, 2005;Dong et al, 2008;Xu et al, 2008;Cazzonelli et al, 2009;Grini et al, 2009;Berr et al, 2010a). Interestingly, SDG725, an H3K36 methyltransferase and the closest homolog of SDG8 in rice (Oryza sativa), is involved in promoting brassinosteroid (BR)-related gene expression and rice flowering (Sui et al, 2012(Sui et al, , 2013. SDG724, another H3K36 methyltransferase in rice, also promotes flowering by affecting H3K36 methylation levels at OsMADS50 and RICE FLOWERING LOCUS T1 (RFT1) chromatin (Sun et al, 2012).…”