Maternal repression of imprinted genes in endosperm by gene body demethylation

Abstract

Removal of TE-like DNA methylation from regulatory elements drives canonical genomic imprinting of both maternally and paternally expressed genes in endosperm (MEGs and PEGs). In both cases, the maternal copies are demethylated, allowing binding of either activating or repressing factors. Here we report that removal of CG-only gene body methylation also drives imprinting, resulting in maternally repressed PEGs as the most common form of imprinting in maize. These body methylated PEGs express broadly across tissues and lack H3K27me3 except in endosperm, where maternal copies acquire it in domains extending through and beyond genes. We also found that partial gene body demethylation is widespread in endosperm, usually does not result in imprinted expression, and is mediated by DNA glycosylases/lyases (DNGs). These and other data indicate that gene body methylation can shield select genes from PRC2 repression, and its maternal removal by DNGs explains the majority of PEGs in both maize and rice but has a weak impact in Arabidopsis thaliana. We hypothesize that increased gene expression noise arising from gene body demethylation--both with and without imprinting--is beneficial in endosperm.