Genomic imprinting in plants-revisiting existing models

Abstract

Genomic imprinting is an epigenetic phenomenon leading to parentally biased gene expression. Throughout the years, extensive efforts have been made to characterize the epigenetic marks underlying imprinting in animals and plants. As a result, DNA methylation asymmetries between parental genomes emerged as the primary factor controlling the imprinting status of many genes. Nevertheless, the data accumulated so far suggest that this process cannot solely explain the imprinting of all genes. In this review, we revisit the current models explaining imprinting regulation in plants, and discuss novel regulatory mechanisms that could function independently of parental DNA methylation asymmetries in the establishment of imprinting.

Keywords: DNA methylation; Polycomb group proteins; genomic imprinting; plants.

Figure 1.

Expression of genes belonging to the main epigenetic pathways in the Arabidopsis female gametophyte, male gametophyte, and endosperm. The epigenetic pathways analyzed here are DNA methylation maintenance (A), DNA demethylation (B), Polycomb repressive complexes (C), and RdDM (D). Expression is shown for the vegetative nucleus (vn), the sperm cell (sc), the central cell (cc), and the endosperm. Expression data were retrieved from the sources indicated in each respective square. (a) Calarco et al. (2012); (b) Jullien et al. (2012); (c) Borges et al. (2008); (d) Belmonte et al. (2013); (e) Wuest et al. (2010); (f) Schoft et al. (2011); (g) Choi et al. (2002); (h) Slotkin et al. (2009); (i) Martínez et al. (2016); (j) Luo et al. (2000); (k) Wang et al. (2006). (1) Methyltransferase activity of MET2a, MET2b, and MET3 has not yet been assessed. (*) Genes were described as being expressed in pollen and absent in sperm cells (Borges et al. 2008).

Figure 2.

Models of imprinted gene regulation. Different models for the epigenetic regulation of MEGs (A,B) and PEGs (C–E). Models represent the epigenetic status of maternal and paternal alleles in the central cell, sperm cell, and endosperm. The estimated proportion of genes regulated by each of these scenarios is reported in Supplemental Table 1. (A) In this scenario, MEGs are constitutively marked with DNA methylation and are therefore silenced in sporophytic tissues. Maternal expression in the endosperm requires the removal of maternal DNA methylation, as well as maintenance of paternal methylation, which is achieved by DME and MET1, respectively. (B) MEGs that are expressed both in the endosperm and in sporophytic tissues do not carry any constitutive marks. In this scenario, maternal-specific expression is achieved through silencing of the paternal allele, a process that could possibly be mediated by RdDM activity in pollen. (C) These PEGs are constitutively marked with DNA methylation; however, this mark does not lead to transcriptional silencing, but rather prevents the deposition of H3K27me3 by FIS–PRC2. Maternal-specific demethylation mediated by DME allows deposition of H3K27me3 in these alleles, leading to their transcriptional inactivation in the endosperm. The presence of DNA methylation in paternal alleles prevents deposition of H3K27me3, allowing for the transcription of this allele. (D) PEGs in this scenario do not show any constitutive epigenetic marks and are expressed in the endosperm as well as in sporophytic tissues. Paternal-specific expression in the endosperm can be achieved through silencing of the maternal alleles in the central cell, mediated by FIS–PRC2 and central cell-specific transcription factors. (E) In this scenario, PEGs show constitutive H3K27me3 and are transcriptionally inactive in sporophytic tissues. This silencing mark is faithfully maintained during female sexual lineage differentiation. On the other hand, decreased activity of the PRC2 in sperm cells causes removal of H3K27me3, leading to transcriptional activation of paternal alleles.