Local DNA hypomethylation activates genes in rice endosperm

Abstract

Cytosine methylation silences transposable elements in plants, vertebrates, and fungi but also regulates gene expression. Plant methylation is catalyzed by three families of enzymes, each with a preferred sequence context: CG, CHG (H = A, C, or T), and CHH, with CHH methylation targeted by the RNAi pathway. Arabidopsis thaliana endosperm, a placenta-like tissue that nourishes the embryo, is globally hypomethylated in the CG context while retaining high non-CG methylation. Global methylation dynamics in seeds of cereal crops that provide the bulk of human nutrition remain unknown. Here, we show that rice endosperm DNA is hypomethylated in all sequence contexts. Non-CG methylation is reduced evenly across the genome, whereas CG hypomethylation is localized. CHH methylation of small transposable elements is increased in embryos, suggesting that endosperm demethylation enhances transposon silencing. Genes preferentially expressed in endosperm, including those coding for major storage proteins and starch synthesizing enzymes, are frequently hypomethylated in endosperm, indicating that DNA methylation is a crucial regulator of rice endosperm biogenesis. Our data show that genome-wide reshaping of seed DNA methylation is conserved among angiosperms and has a profound effect on gene expression in cereal crops.DNA methylation | embryo | transposable element

Genomic DNA methylation analyses reveal the distinct profiles in castor bean seeds with persistent endosperms

“…The density peaks of CG methylation were found mainly in the gene body regions, but the peaks of both CHG and CHH methylation were found mainly in the TE regions and distributed sparely in the gene body regions. Clearly, these observations showed that DNA methylation occurred mainly in the TE-rich regions, consistent with previous reports from other plants (Gehring et al, 2009;Zemach et al, 2010a), and the global methylation patterns between CG and non-CG contexts were differentiated in castor bean.…”

“…Within the DNA demethylase genes, phylogenetic analysis generated six clades (I-VI). The DME homologs were restricted to dicots and absent in monocots, confirming previous observations (Zemach et al, 2010a;Zhang et al, 2011). The ROS1 genes were clustered into clades II (nested by the homologs from dicots), III, and IV (both nested by the homologs from monocots).…”

“…The ROS1 genes were clustered into clades II (nested by the homologs from dicots), III, and IV (both nested by the homologs from monocots). However, both clade I and clade II were rooted by monkey flower (Mimulus guttatus), a basal dicotyledonous plant (Zemach et al, 2010a), suggesting that the DME may be phylogenetically monophyletic in dicots after gene duplication arising in the early angiosperm. In addition, the DML3 genes were clustered into clades V and VI nested by the homologs from dicots and monocots, respectively.…”

“…In particular, DNA methylation was considered as a major regulator of gene imprinting that mainly manifests itself in the endosperm of angiosperm plants, closely associated with endosperm and seed development, such as the imprinted genes MEA (Grossniklaus et al, 1998;Köhler et al, 2003), FWA (Kinoshita et al, 2004), and FIS2 (Jullien et al, 2006). Investigations of genomic DNA methylation in the seeds of Arabidopsis (Gehring et al, 2009;Hsieh et al, 2009), rice (Oryza sativa; Zemach et al, 2010a), and maize (Zea mays; Zhang et al, 2014;Lu et al, 2015) revealed extensive hypomethylation in the endosperm genome. However, the mechanism of how the extent and pattern of DNA methylation are established and whether the extent and pattern of DNA methylation are conserved in plant seeds is largely unclear.…”

Extensive, clustered parental imprinting of protein-coding and noncoding RNAs in developing maize endosperm

“…Two genes in the maize genome (GRMZM2G422464 and GRMZM2G131756) are highly homologous to DME in Arabidopsis, but their exact functions are still unknown. It is also possible that monocots use a different enzyme to mediate maternal demethylation (42). Because the previously identified imprinted genes are mostly MEGs, there is no previous report on parental differential methylation for PEGs.…”