Mechanism of PHERES1 imprinting in Arabidopsis

Abstract

Genomic imprinting is a phenomenon where only one of the two alleles of a gene is expressed -either the maternally or the paternally inherited allele. Imprinting of the plant gene PHERES1 requires the function of the FERTILIZATION INDEPENDENT SEED (FIS) Polycomb group (PcG) complex for repression of the maternal PHERES1 allele. In this study we investigated the mechanism of PHERES1 imprinting and found that PcG silencing is necessary but not sufficient for imprinting establishment of PHERES1. We provide evidence that silencing of the maternal PHERES1 allele depends on a distantly located region downstream of the PHERES1 locus. This region needs to be methylated to ensure PHERES1 expression but must not be methylated for PHERES1 repression. This mechanism is analogous to the regulation of several imprinted genes in mammals, suggesting the employment of similar evolutionary mechanisms for the regulation of imprinted genes in mammals and flowering plants. Supplementary material available online at

Mechanisms and evolution of genomic imprinting in plants

“…Whereas HDG8 and HDG9 are predominantly maternally expressed, HDG3 is expressed from the paternal allele. Therefore, in agreement with previous findings (Makarevich et al, 2008, Villar et al, 2009), demethylation of transposons or repeat sequences of the maternally inherited alleles can result in imprinted expression with the paternal allele being expressed. Gehring et al (2009) suggest that the best candidates for imprinted genes are those that are less methylated in the endosperm than in the embryo, show endospermpreferred expression and are transcribed at low levels in other parts of the plant.…”

“…Parent-oforigin-specific expression of genetically identical alleles is achieved by the application of specific epigenetic modifications in the gametes. In particular, DNA methylation and Polycomb group (PcG)-mediated trimethylation of histone H3 at lysine 27 (H3K27me3) have been widely recognized as important epigenetic marks distinguishing maternally and paternally inherited alleles in mammals (Umlauf et al, 2004;Edwards and Ferguson-Smith, 2007) as well as in plants (Kinoshita et al, 2004;Baroux et al, 2006;Gehring et al, 2006;Xiao et al, 2006;Makarevich et al, 2008;Jullien et al, 2006a, b).…”

“…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 .…”

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.…”

Networks controlling seed size in Arabidopsis

“…The FIS-PRC2 mainly represses the expression of 291 maternally inherited (and hypomethylated) alleles. Seeds 292 with mutations in mea, fis2 or fie2 show endosperm pro-293 liferation even in the absence of fertilization, but also 294 prolonged endospermal proliferation and absent or delayed 295 cellularization if fertilization occurs (Grossniklaus et al 296 1998; Kiyosue et al 1999;Makarevich et al 2008). The 297 phenotypes of these mutants imply that PCR2 complexes 298 promote fast endosperm differentiation after fertilization, 299 thus directly acting on a pathway that greatly influences 300 seed size (Fig.…”