The histone demethylase JMJ27 acts during the UV-induced modulation of H3K9me2 landscape and facilitates photodamage repair

Plants have evolved sophisticated DNA repair mechanisms to cope with the deleterious effects of ultraviolet (UV)-induced DNA damage. Indeed, DNA repair pathways cooperate with epigenetic-related processes to efficiently maintain genome integrity. However, it remains to be deciphered how photodamages are recognized within different chromatin landscapes, especially in compacted genomic regions such as constitutive heterochromatin. Here we combined cytogenetics and epigenomics to identify that UV-C irradiation induces modulation of the main epigenetic mark found in constitutive heterochromatin, H3K9me2. We demonstrated that the histone demethylase, Jumonji27 (JMJ27), contributes to the UV-induced reduction of H3K9me2 content at chromocentres. In addition, we identified that JMJ27 forms a complex with the photodamage recognition factor, DNA Damage Binding protein 2 (DDB2), and that the fine-tuning of H3K9me2 contents orchestrates DDB2 dynamics on chromatin in response to UV-C exposure. Hence, this study uncovers the unexpected existence of an interplay between photodamage repair and H3K9me2 homeostasis. UV exposure modulates H3K9me2 contents at chromocentres via the histone demethylase JMJ27 which interacts with the DNA damage recognition factor, DDB2, and facilitates photodamage repair. The loading or release of DDB2 at nucleosome sites is optimized by the fine-tuning of H3K9me2.