Control of PHERES1 Imprinting in Arabidopsis by Direct Tandem Repeats

Abstract

Genomic imprinting is an epigenetic phenomenon that causes monoallelic expression of specific genes dependent on the parent-of-origin. Imprinting of the Arabidopsis gene PHERES1 requires the function of the FERTILIZATION INDEPENDENT SEED (FIS) Polycomb group complex as well as a distally located methylated region containing a tandem triple repeat sequence. In this study, we investigated the regulation of the close PHERES1 homolog PHERES2. We found that PHERES2 is also a direct target gene of the FIS Polycomb group complex, but, in contrast to PHERES1, PHERES2 is equally expressed from maternal and paternal alleles. Thus, PHERES2 is not regulated by genomic imprinting, correlating with the lack of tandem repeats at PHERES2. Eliminating tandem repeats from the PHERES1 locus abolishes PHERES1 imprinting, demonstrating that tandem repeats are essential for PHERES1 imprinting. Taking these results together, our study shows that the recently duplicated genes PHERES1 and PHERES2 are both target genes of the FIS Polycomb group complex but only PHERES1 is regulated by genomic imprinting, which is likely caused by the presence of repeat sequences in the proximity of the PHERES1 locus.

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.…”

Regulation of imprinted gene expression in Arabidopsis endosperm

“…Maternal demethylation of tandem repeats downstream of PHE1 is also thought to be required for maternal PHE1 silencing. This idea is supported by the observation that loss of methylation in the paternal genome because of a met1 mutation reduced expression of the paternal PHE1 allele (17,20). Indeed, we detected DME-dependent endosperm hypomethylation of these tandem repeats (33) (Fig.…”

“…3B). Thus, the current model explaining regulation of PHE1 imprinting proposes that maternal DNA demethylation near the gene exposes a PRC2 binding site, thereby allowing PcG-mediated silencing of the maternal allele (17). Supporting this model, Weinhofer et al (40) recently reported that DNA hypomethylation allows targeting by PcG proteins in endosperm.…”

“…Three paternally expressed imprinted transcription factor genes, HDG3, MYB THREE REPEAT 2 (MYB3R2), and PHERES 1 (PHE1), have been identified (16,17). Silencing of the maternal PHE1 allele depends on a functional PRC2 complex, and maternally inherited mutations in PRC2 cause biallelic expression of PHE1 (18,19).…”

“…Silencing of the maternal PHE1 allele depends on a functional PRC2 complex, and maternally inherited mutations in PRC2 cause biallelic expression of PHE1 (18,19). In addition, silencing of the maternal PHE1 allele is thought to require maternal demethylation at the PHE1 gene (17,20).…”