TE-like DNA methylation of highly expressed endosperm genes in maize

ABSTRACT Unlike the stable transcription of plant genes with CG gene body methylation alone, genes with methylation in TE-like CHG and CG contexts are poorly transcribed and often missanotated. In contrast, here we describe a set of TE-like methylated genes that are maternally demethylated and expressed toward the extreme high end of the spectrum in endosperm. They are enriched for short, secreted proteins, and about a third encode zeins, the major seed storage proteins of maize. Consistent with their dynamic expression in endosperm, they acquire either activating or repressive gene regulatory modifications when demethylated but are heterochromatic when methylated in other tissues. The majority are expressed both maternally and paternally, but a subset whose methylation/demethylation extends upstream of gene bodies into promoters are strongly imprinted. These and other data indicate that TE-like methylation and associated heterochromatin can be a signature of broad silencing but exceptionally high and specific gene expression in either pollen or endosperm. Competing Interest Statement The authors have declared no competing interest. Footnotes The revised manuscript contains ChIP and CUT&Tag data showing that TE-like methylated endosperm genes are heterochromatic in sporophyte and euchromatic in endosperm. It also has includes additional evidence for conservation of TE-like methylation of protein storage genes in other cereal crops.