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

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 is considered to regulate ribosomal RNA production. However, the molecular mechanism is still unclear. Here, we report a novel function of CENP-B homolog Abp1 in forming facultative heterochromatin at ribosomal DNA repeats. We find that the loss of Abp1 induces an ectopic nucleosome assembly at rDNA repeats. Interestingly, the loss of Abp1 induces two mutually exclusive changes at ribosomal DNA repeats: an excess accumulation of methylation of histone H3 at lysine 9, a hallmark of heterochromatin, and an active RNA polymerase II transcription. This excess heterochromatin represses ribosomal RNA expression and requires RNA interference 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 ribosomal DNA repeats, we propose that Abp1 regulates activity of RNA polymerase II transcription that is paradoxically required for RNA interference-mediated heterochromatin formation and controls an appropriate level of heterochromatinization at ribosomal DNA repeats under glucose starvation.