Photodamage repair pathways contribute to the accurate maintenance of the DNA methylome landscape upon UV exposure

• Published in: PLoS genetics 2019-11, Vol.15 (11), p.e1008476
• Main Authors: Graindorge, Stéfanie, Cognat, Valérie, Johann To Berens, Philippe, Mutterer, Jérôme, Molinier, Jean
• Format: Article
• Language: English
• Subjects: Abiotic stress; Arabidopsis - genetics; Arabidopsis - radiation effects; Biology and life sciences; Chromatin; Chromatin - genetics; Chromatin - radiation effects; Demethylation; Deoxyribonucleic acid; DNA; DNA damage; DNA Damage - genetics; DNA Damage - radiation effects; DNA methylation; DNA Methylation - genetics; DNA Methylation - radiation effects; DNA repair; DNA Repair - genetics; DNA Repair - radiation effects; Engineering and Technology; Enzymes; Epigenome - genetics; Epigenome - radiation effects; Gene expression; Genetic research; Genetics; Genome, Plant - genetics; Genome, Plant - radiation effects; Genomes; Genomics; Life Sciences; Methylation; Physical sciences; Plant evolution; Plants genetics; Research and Analysis Methods; Ribonucleic acid; RNA; RNA polymerase; Ultraviolet radiation; Ultraviolet Rays; Vegetal Biology
• ISSN: 1553-7404; 1553-7390; 1553-7404
• DOI: 10.1371/journal.pgen.1008476

Plants are exposed to the damaging effect of sunlight that induces DNA photolesions. In order to maintain genome integrity, specific DNA repair pathways are mobilized. Upon removal of UV-induced DNA lesions, the accurate re-establishment of epigenome landscape is expected to be a prominent step of these DNA repair pathways. However, it remains poorly documented whether DNA methylation is accurately maintained at photodamaged sites and how photodamage repair pathways contribute to the maintenance of genome/methylome integrities. Using genome wide approaches, we report that UV-C irradiation leads to CHH DNA methylation changes. We identified that the specific DNA repair pathways involved in the repair of UV-induced DNA lesions, Direct Repair (DR), Global Genome Repair (GGR) and small RNA-mediated GGR prevent the excessive alterations of DNA methylation landscape. Moreover, we identified that UV-C irradiation induced chromocenter reorganization and that photodamage repair factors control this dynamics. The methylome changes rely on misregulation of maintenance, de novo and active DNA demethylation pathways highlighting that molecular processes related to genome and methylome integrities are closely interconnected. Importantly, we identified that photolesions are sources of DNA methylation changes in repressive chromatin. This study unveils that DNA repair factors, together with small RNA, act to accurately maintain both genome and methylome integrities at photodamaged silent genomic regions, strengthening the idea that plants have evolved sophisticated interplays between DNA methylation dynamics and DNA repair.