DNA demethylation is initiated in the central cells of Arabidopsis and rice

Abstract

Cytosine methylation is a DNA modification with important regulatory functions in eukaryotes. In flowering plants, sexual reproduction is accompanied by extensive DNA demethylation, which is required for proper gene expression in the endosperm, a nutritive extraembryonic seed tissue. Endosperm arises from a fusion of a sperm cell carried in the pollen and a female central cell. Endosperm DNA demethylation is observed specifically on the chromosomes inherited from the central cell in Arabidopsis thaliana, rice, and maize, and requires the DEMETER DNA demethylase in Arabidopsis. DEMETER is expressed in the central cell before fertilization, suggesting that endosperm demethylation patterns are inherited from the central cell. Down-regulation of the MET1 DNA methyltransferase has also been proposed to contribute to central cell demethylation. However, with the exception of three maize genes, central cell DNA methylation has not been directly measured, leaving the origin and mechanism of endosperm demethylation uncertain. Here, we report genome-wide analysis of DNA methylation in the central cells of Arabidopsis and rice-species that diverged 150 million years agoas well as in rice egg cells. We find that DNA demethylation in both species is initiated in central cells, which requires DEMETER in Arabidopsis. However, we do not observe a global reduction of CG methylation that would be indicative of lowered MET1 activity; on the contrary, CG methylation efficiency is elevated in female gametes compared with nonsexual tissues. Our results demonstrate that locus-specific, active DNA demethylation in the central cell is the origin of maternal chromosome hypomethylation in the endosperm.

Arabidopsis male sexual lineage exhibits more robust maintenance of CG methylation than somatic tissues

“…5). The semiconservative model of CG methylation inheritance (1), and the considerable genetic evidence in support of this model (31)(32)(33), is more compatible with the higher efficiency of CG methylation in the male germ line (microspores and sperm), and with the similarly high efficiency observed in female plant gametes (34), than with that observed in somatic tissues (28). In heterochromatic TEs, much or all of the increased efficiency might be accounted by reduced levels of histone H1 (Fig.…”

Parental DNA Methylation States Are Associated with Heterosis in Epigenetic Hybrids

“…Heterosis was observed in a parent-of-origin manner; the reciprocal cross did not result in heterosis (Dapp et al, 2015). This suggests a maternal effect (Park et al, 2016). In our design, we used Col-wt as the female parent and various ddm1-derived epiRILs as the male parent.…”

Live-cell analysis of DNA methylation during sexual reproduction in Arabidopsis reveals context and sex-specific dynamics controlled by noncanonical RdDM

“…The egg cell seems to be the exception, as we observed a significant decrease of signal upon its maturation, which might be due to either demethylation or loss of symmetrical methylation resulting from lack of MET1 activity . The methylome of the egg cell in rice was published recently (Park et al 2016) and revealed a CG methylation pattern typical of somatic cells. Assuming that these results are also valid in the Arabidopsis egg cell, this might suggest significant hemimethylation rather than demethylation in the egg cell.…”