The Arabidopsis thaliana MEDEA Polycomb group protein controls expression of PHERES1 by parental imprinting

Abstract

The maternally expressed Arabidopsis thaliana Polycomb group protein MEDEA (MEA) controls expression of the MADS-box gene PHERES1 (PHE1). Here, we show that PHE1 is mainly paternally expressed but maternally repressed and that this maternal repression of PHE1 breaks down in seeds lacking maternal MEA activity. Because Polycomb group proteins control parental imprinting in mammals as well, the independent recruitment of similar protein machineries for the imprinting of genes is a notable example of convergent evolution.

Extensive, clustered parental imprinting of protein-coding and noncoding RNAs in developing maize endosperm

“…Because the previously identified imprinted genes are mostly MEGs, there is no previous report on parental differential methylation for PEGs. Silencing of the maternal allele of a PEG gene (PHE1) in Arabidopsis is reported to require demethylation of the maternal allele and depends on the PRC2 complex (43)(44)(45). All eight PEGs having DMRs are also maternally hypomethylated, suggesting that there could be an additional mechanism for the regulation of PEGs.…”

Mechanisms and evolution of genomic imprinting in plants

“…Thus, silencing of the maternal alleles of PHERES1 (PHE1) and the paternal alleles of MEDEA (MEA) and ARABIDOPSIS FORMIN HOMOLOGUE 5 depend on repressive activity of PcG proteins (Kö hler et al, 2005;Baroux et al, 2006;Gehring et al, 2006;Jullien et al, 2006b;Makarevich et al, 2008;Fitz Gerald et al, 2009). PcG proteins act in complexes that apply H3K27me3 on their target genes, causing gene repression by not well understood mechanisms .…”

“…After this logic, many imprinted genes are likely to have an endosperm-constrained function, or, alternatively, they have no functional role in the endosperm and are on the trajectory to convert to pseudogenes (Figure 2). Although there are exceptions (for example, PHE1 and HDG3 (Kö hler et al, 2005;Gehring et al, 2009)), the majority of imprinted genes is likely to be maternally active and paternally silenced, imposing a strong maternal control over endosperm development, as it could be predicted based on the hypothesis that the endosperm is an extension of the maternal gametophytic life phase (Nowack et al, 2007). To conclude, both hypotheses, the 'defense hypothesis' as well as 'kinship theory' together can explain the origin of genomic imprinting in the endosperm; whereas the first hypothesis explains how imprinting originates, the latter explains how imprinting will be manifested and maintained.…”

Endosperm: an integrator of seed growth and development

“…Small-scale microarray analyses using combinations of fis mutants have to date discovered two genes that are repressed by the FIS-complex, and these genes encode the MADS-box protein PHERES1 (PHE1) and the SKP1-like protein MEIDOS [16]. What functions these proteins have in seed development and growth is not known, but PHE1 has been shown to be expressed exclusively from the paternal genome after fertilization [42 ]. In contrast to the gametophytic maternal effects discussed previously, genes such as PHE1 might thus be responsible for activating paternal-specific gene sets in endosperm.…”