Epigenetic reprogramming in plant and animal development

Abstract

Epigenetic modifications of the genome are generally stable in somatic cells of multicellular organisms. In germ cells and early embryos, however, epigenetic reprogramming occurs on a genome-wide scale, which includes demethylation of DNA and remodeling of histones and their modifications. The mechanisms of genome-wide erasure of DNA methylation, which involve modifications to 5-methylcytosine and DNA repair, are being unraveled. Epigenetic reprogramming has important roles in imprinting, the natural as well as experimental acquisition of totipotency and pluripotency, control of transposons, and epigenetic inheritance across generations. Small RNAs and the inheritance of histone marks may also contribute to epigenetic inheritance and reprogramming. Reprogramming occurs in flowering plants and in mammals, and the similarities and differences illuminate developmental and reproductive strategies.

Fig. 1

Model of epigenetic silencing dynamics during Arabidopsis life cycle. In somatic cells, three different mechanisms are responsible for repressing transcription from transposable element (TE), DNA methylation (in all three sequence contexts), histone H3K9 dimethylation (H3K9me2), and histone H3K27 monomethylation (H3K27me1). Methyltransferases and proteins regulating these epigenetic marks are shown in the diagram. See text for details. In the female gametophyte, the central cell is demethylated by DME, which leads to TE activation and upregulation of RdDM. The siRNAs produced from TEs not only direct non-CG methylation in the central cell, but also might travel to egg cell and enhance the silencing of TEs there. In addition, AGO9-associated siRNAs produced in somatic companion cells also contribute to the silencing of TEs in the egg cell. In the male gametophyte, the vegetative nucleus does not express DDM1 and has reduced RdDM, which leads to TE activation and mobilization. A new class of 21-nt siRNAs is produced from TEs in the vegetative nucleus that travels to sperm cells to reinforcing TE silencing. After double fertilization, maternal TEs in the endosperm stay activated and produce PolIV-dependent siRNAs, which could function to silence the paternal TEs in the endosperm. The methylation levels in the embryo are elevated, possibly due to the siRNA signals transmitted from the endosperm. Different shadings indicate the level of DNA methylation, with black being the high, gray being medium, and white being low.

Fig. 2

The two major phases of genome-wide erasure of DNA methylation in the early embryo and in primordial germ cells (PGCs) of the mouse are shown. Thickness of the outer arrows indicates levels of DNA methylation. Red, maternal genome; blue, paternal genome. After fertilization the paternal genome is more rapidly demethylated than the maternal one. During gametogenesis de novo methylation in spermatogenesis occurs earlier than in oogenesis. The inner circle shows factors or candidate factors that are implicated in de novo methylation, the maintenance of methylation, or demethylation, respectively. Solid arrows in the inner circle show at what developmental time these epigenetic regulators are thought to act.