DNA polymerase epsilon is required for heterochromatin maintenance in Arabidopsis
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RESEARCH
Open Access
DNA polymerase epsilon is required for heterochromatin maintenance in Arabidopsis Pierre Bourguet1, Leticia López-González1, Ángeles Gómez-Zambrano1,2, Thierry Pélissier1, Amy Hesketh1, Magdalena E. Potok3, Marie-Noëlle Pouch-Pélissier1, Magali Perez4, Olivier Da Ines1, David Latrasse4, Charles I. White1, Steven E. Jacobsen3,5, Moussa Benhamed4 and Olivier Mathieu1* * Correspondence: olivier.mathieu@ uca.fr 1 Institute of Genetics Reproduction and Development (iGReD), Université Clermont Auvergne, CNRS, Inserm, F-63000 Clermont-Ferrand, France Full list of author information is available at the end of the article
Abstract Background: Chromatin organizes DNA and regulates its transcriptional activity through epigenetic modifications. Heterochromatic regions of the genome are generally transcriptionally silent, while euchromatin is more prone to transcription. During DNA replication, both genetic information and chromatin modifications must be faithfully passed on to daughter strands. There is evidence that DNA polymerases play a role in transcriptional silencing, but the extent of their contribution and how it relates to heterochromatin maintenance is unclear. Results: We isolate a strong hypomorphic Arabidopsis thaliana mutant of the POL2A catalytic subunit of DNA polymerase epsilon and show that POL2A is required to stabilize heterochromatin silencing genome-wide, likely by preventing replicative stress. We reveal that POL2A inhibits DNA methylation and histone H3 lysine 9 methylation. Hence, the release of heterochromatin silencing in POL2A-deficient mutants paradoxically occurs in a chromatin context of increased levels of these two repressive epigenetic marks. At the nuclear level, the POL2A defect is associated with fragmentation of heterochromatin. Conclusion: These results indicate that POL2A is critical to heterochromatin structure and function, and that unhindered replisome progression is required for the faithful propagation of DNA methylation throughout the cell cycle. Keywords: DNA polymerase epsilon, Replication stress, DNA methylation, Heterochromatin, Silencing
Background In nearly all eukaryotes, DNA is wrapped around histone proteins to form nucleosomes that allow extensive compaction of the genome while allowing access for important processes such as DNA replication, DNA repair, and transcription. Each nucleosome consists of about 147 bp of DNA wrapped around two molecules of each of four histones H2A, H2B, H3, and H4. Two main states of chromatin organization © The Author(s). 2020 Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise
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