A fission yeast CENP-B homologue Abp1 prevents RNAi-mediated heterochromatin formation at ribosomal DNA repeats.

Abstract

In response to nutritional starvation, living cells sensitively regulate the production rates of molecules required for survival. Under glucose starvation, a facultative heterochromatinization of ribosomal DNA (rDNA) is considered to regulate ribosomal RNA (rRNA) production. However, the molecular mechanism is still unclear. Here, we report a novel function of CENP-B homologue Abp1 in forming facultative heterochromatin at rDNA repeats. We find that loss of Abp1 induces an ectopic nucleosome assembly at rDNA repeats. Interestingly, loss of Abp1 induces two mutually exclusive changes at rDNA repeats: an excess accumulation of methylation of histone H3 at lysine 9 (H3K9me), a hallmark of heterochromatin, and an active RNA polymerase II (RNAPII) transcription. This excess heterochromatin represses rRNA expression and requires RNAi machinery for its formation. Furthermore, we show that the excess heterochromatin does not affect cellular viability under glucose starvation but prevents the return to the proliferation cycle in recovering glucose-rich conditions. Since glucose starvation rapidly induces partial Abp1 disassociation from rDNA repeats, we propose that Abp1 regulates an activity of RNAPII transcription that is paradoxically required for RNAi-mediated heterochromatin formation and controls an appropriate level of heterochromatinization at rDNA repeats under glucose starvation.