A composite DNA element that functions as a maintainer required for epigenetic inheritance of heterochromatin

Epigenetic inheritance of heterochromatin requires DNA-sequence-independent propagation mechanisms, coupling to RNAi, or input from DNA sequence, but how DNA contributes to inheritance is not understood. Here, we identify a DNA element (termed maintainer) that is sufficient for epigenetic inheritance of pre-existing histone H3 lysine 9 methylation (H3K9me) and heterochromatin in Schizosaccharomyces pombe but cannot establish de novo gene silencing in wild-type cells. This maintainer is a composite DNA element with binding sites for the Atf1/Pcr1 and Deb1 transcription factors and the origin recognition complex (ORC), located within a 130-bp region, and can be converted to a silencer in cells with lower rates of H3K9me turnover, suggesting that it participates in recruiting the H3K9 methyltransferase Clr4/Suv39h. These results suggest that, in the absence of RNAi, histone H3K9me is only heritable when it can collaborate with maintainer-associated DNA-binding proteins that help recruit the enzyme responsible for its epigenetic deposition.

Automated summary

Epigenetic inheritance of heterochromatin requires mechanisms independent of DNA sequence, RNAi coupling, or input from DNA sequence. A DNA element termed maintainer has been identified that is sufficient for the epigenetic inheritance of pre-existing histone H3 lysine 9 methylation and heterochromatin in Schizosaccharomyces pombe. This maintainer is a composite DNA element with binding sites for specific transcription factors and ORC, and can be converted to a silencer in cells with lower rates of H3K9me turnover.