Epigenetic Maps: Methylation of genomic DNA on cytosine bases provides critical epigenetic regulation of gene expression and is involved in silencing transposable elements (TEs) and repeated sequences, as well as regulating imprinted gene expression. Zemach et al. (p. 916 , published online 15 April; see the Perspective by Jeltsch ) analyzed DNA methylation in the genomes of five plants, five fungi, and seven animals by bisulfite sequencing. The data suggest that land plants and vertebrates, which have extensive DNA methylation, are under strong selective pressure to repress TEs, because of their sexual mode of reproduction. Unicellular animals and fungi that reproduce asexually are more likely to lose TE methylation. Although gene body methylation is evolutionarily ancient, it is also mutagenic, and so loss of this pathway has been relatively common and occurred early in fungal evolution and later in several plant and animal lineages.

Dynamic Imprinting: Gene imprinting—the silencing of either a maternally derived or paternally derived gene allele—is controlled in large part by DNA methylation. In plants, imprinting occurs in the endosperm, which nourishes the embryonic plant. Gehring et al. (p. 1447 ) and Hsieh et al. (p. 1451 ) analyzed the dynamics of DNA methylation in the endosperm and embryo of Arabidopsis and found extensive demethylation in the endosperm, suggesting that many imprinted genes are likely to exist. Gehring et al. characterized five imprinted genes in detail. Four of the 10 known imprinted genes are related homeodomain transcription factors. Furthermore, 5′ sequences demethylated in several of the genes were found to be derived from transposable elements, which supports the idea that imprinting arose as a by-product of silencing invading DNA.

Intergenerational Transposable Shutdown: Transposable elements (TEs) are a potential threat, especially to the germline genome. In many eukaryotes, TEs are shut down by DNA methylation and/or small-RNA–mediated silencing. Therefore, it seems counterintuitive that results obtained by Ibarra et al. (p. 1360 ) on Arabidopsis showed that in the cells of this plant's sexual apparatus, many small TEs are demethylated by DEMETER (DME) DNA glycosylase and become activated. But it turns out that activation of the TEs triggers the formation of small-interfering RNAs, which in these experiments were seen to travel from the surrounding cells to the egg. Thus, activation of TEs in the companion cells “immunizes” the gametes via the interfering RNAs that shutdown the TEs in the gametes permanently.

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.