Arabidopsis DNA polymerase ϵ recruits components of Polycomb repressor complex to mediate epigenetic gene silencing

Abstract

Arabidopsis ESD7 locus encodes the catalytic subunit of the DNA Pol ϵ involved in the synthesis of the DNA leading strand and is essential for embryo viability. The hypomorphic allele esd7-1 is viable but displays a number of pleiotropic phenotypic alterations including an acceleration of flowering time. Furthermore, Pol ϵ is involved in the epigenetic silencing of the floral integrator genes FT and SOC1, but the molecular nature of the transcriptional gene silencing mechanisms involved remains elusive. Here we reveal that ESD7 interacts with components of the PRC2 such as CLF, EMF2 and MSI1, and that mutations in ESD7 cause a decrease in the levels of the H3K27me3 mark present in the chromatin of FT and SOC1. We also demonstrate that a domain of the C-terminal region of ESD7 mediates the binding to the different PRC2 components and this interaction is necessary for the proper recruitment of PRC2 to FT and SOC1 chromatin. We unveil the existence of interplay between the DNA replication machinery and the PcG complexes in epigenetic transcriptional silencing. These observations provide an insight into the mechanisms ensuring that the epigenetic code at pivotal loci in developmental control is faithfully transmitted to the progeny of eukaryotic cells.

Requirement for flap endonuclease 1 (FEN1) to maintain genomic stability and transcriptional gene silencing in Arabidopsis

“…Previous studies proposed that a mutation in the catalytic subunit of DNA polymerase α altered the binding of like heterochromatin protein 1 (LHP1) (Hyun et al ., ), which was a crucial component of the polycomb repressive complex (PRC) for the maintenance of H3K27me3 in Arabidopsis (Zhang et al ., ; Shen et al ., ). Recently, it was reported that DNA polymerase ε interacts with the components of PRC2, and dysfunction of DNA polymerase ε results in a decrease in the H3K27me3 level and increased expression of H3K27me3‐marked genes (Del Olmo et al ., ). It is likely that dysfunction of FEN1 might perturb the DNA replication machinery and thereby affect epigenetic hallmarks directly or indirectly.…”

Tug of war: adding and removing histone lysine methylation in Arabidopsis

“…The uncovered PRC2 recruitment mechanism, including a role for GA repeats motif and Zinc finger transcription factors as recruiters, is very similar to that in Drosophila [61,79]. In addition to transcription factors, DNA polymerase epsilon (ESD7) interacts with PRC2 and can recruit this complex to the flowering time loci FT and SOC1 to maintain high H3K27me3 levels during mitosis [80].…”

Storing memories: the distinct phases of Polycomb-mediated silencing of Arabidopsis FLC

“…The spreading process is also blocked by the CDK inhibitors that halt cell cycle progression [9,20] and by mutations in the DNA replication primase Pol α [72]. Proteomic studies in Arabidopsis show that several PRC2 components, including CLF, immunoprecipitate with DNA Pol ε, the DNA polymerase responsible for replicating the leading strand [73]. CLF, SWN and LHP1 also interact with the helicase complex at the replication forks via a protein related to the yeast replication factor Ctf4 [74].…”