Transcription‐induced chromatin association of RNA surveillance factors mediates facultative heterochromatin formation in fission yeast

Facultative heterochromatin is reversibly established and disrupted during differentiation, but its regulation remains mechanistically unclear. Here, we show that two meiotic gene loci in fission yeast, mei4 and ssm4 , comprise facultative heterochromatin that is regulated in a developmental stage‐dependent manner. This heterochromatin coordinates expression levels by associating with a chromodomain protein C hp1 and an antisilencing factor E pe1. It has been recently shown that an RNA surveillance machinery for eliminating meiotic gene transcripts, which involves a cis ‐element called the determinant of selective removal ( DSR ) and trans acting factors, M mi1 and R ed1, also participates in heterochromatin formation at the meiotic genes, but the molecular mechanism underlying the process is largely unknown. By dissecting the mei4 gene, we identified a region that promotes DSR ‐dependent methylation of histone H 3 lysine 9 ( H 3 K 9). Integration of this mei4 region together with DSR into an unrelated gene results in ectopic H 3 K 9 methylation. Moreover, our results suggest that transcription of these elements induces chromatin association of M mi1, which, in turn, recruits R ed1 interacting with C lr4/ S uv39h H 3 K 9 methyltransferase. M mi1 remains associated in cells lacking R ed1, suggesting that the recruitment of R ed1 follows the chromatin association of M mi1. Overall, we provide detailed insights into the facultative heterochromatin regulation in fission yeast.