Evolution and function of genomic imprinting in plants

Abstract

Genomic imprinting, an inherently epigenetic phenomenon defined by parent of origin-dependent gene expression, is observed in mammals and flowering plants. Genome-scale surveys of imprinted expression and the underlying differential epigenetic marks have led to the discovery of hundreds of imprinted plant genes and confirmed DNA and histone methylation as key regulators of plant imprinting. However, the biological roles of the vast majority of imprinted plant genes are unknown, and the evolutionary forces shaping plant imprinting remain rather opaque. Here, we review the mechanisms of plant genomic imprinting and discuss theories of imprinting evolution and biological significance in light of recent findings.

Keywords: DNA methylation; epigenetics; evolution; genomic imprinting; histone methylation; plant reproduction.

Figure 1.

Imprinted gene expression. Maternally and paternally inherited alleles are epigenetically distinguished (or imprinted), causing differential expression in the fertilization product. Primary imprints are established before fertilization, whereas secondary imprints are guided by primary imprints after fertilization.

Figure 2.

Sexual reproduction in the flowering plant A. thaliana. The gametes are contained within multicellular haploid structures called gametophytes that are derived by mitosis from meiotic spores. The fusion of two haploid polar nuclei forms a diploid central cell in the female gametophyte. At the time of fertilization, the diploid female central cell and a haploid male sperm cell fuse to give rise to the endosperm, while the haploid female egg cell and haploid male sperm cell fuse to give rise to the embryo. The resulting seed is formed of the endosperm, the embryo, and a maternally derived seed coat.

Figure 3.

Mechanisms of imprinting in the endosperm of flowering plants. (A) At the Arabidopsis FWA locus, DEMETER (DME) activity at upstream repeats, presumed to occur in the central cell but not the sperm cells, forms a primary imprint that results in maternal-specific expression. (B) The primary imprint at the Arabidopsis PHERES1 gene is also formed by presumed central cell-specific demethylation of repeats by DME. Loss of methylation at these repeats results in histone 3 Lys27 trimethylation. This secondary imprint laid down by polycomb-repressive complex 2 (PRC2) causes silencing of the maternal loci and paternal-specific expression. (C) Arabidopsis VIM5 is an example of a gene that does not appear to rely on DME-mediated DNA demethylation for the formation of the primary imprint, as both maternal and paternal alleles are deficient in DNA methylation. Instead, histone 3 Lys27 trimethylation may form a primary imprint that results in paternal-specific expression (Hsieh et al. 2011).

Figure 4.

Evolution of imprinted gene expression through genetic mechanism via transposon insertion (A) and epigenetic mechanism via heritable loss of DNA methylation (B).

Figure 5.

Model for the simultaneous evolution of imprinting and endosperm in the ancestor of angiosperms (flowering plants). Angiosperms emerged from a gymnosperm (nonflowering seed plant) lineage, evolving flowers, fruits, and endosperm. Endosperm potentially evolved through the sexualization of a female gamete companion cell, such as the ventral canal cell (Friedman and Floyd 2001; Rudall 2006), via fusion with one of the two sperm cells of pollen. Activity of a DME-like enzyme in the sexualized female gamete companion cell would give rise to an endosperm with DNA methylation-based imprints in the ancestor of modern angiosperms.