Maternal repression of imprinted genes in endosperm by gene body demethylation

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). Here we report that removal of CG-only gene body methylation also drives imprinting in maize, resulting in maternally repressed PEGs. These CG body methylated PEGs express broadly across cell types and lack H3K27me3 except in endosperm, where maternal copies acquire it. We found that partial gene body demethylation is a widespread feature of endosperm genes, 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 maize and rice but has 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.