Abstract
The conserved protein kinase Rio1 localizes to the cytoplasm and nucleus of eukaryotic cells. While the roles of Rio1 in the cytoplasm are well characterized, its nuclear function remains unknown. Here we show that nuclear Rio1 promotes rDNA array stability and segregation in Saccharomyces cerevisiae. During rDNA replication in S phase, Rio1 downregulates RNA polymerase I (PolI) and recruits the histone deacetylase Sir2. Both interventions ensure rDNA copy-number homeostasis and prevent the formation of extrachromosomal rDNA circles, which are linked to accelerated ageing in yeast. During anaphase, Rio1 downregulates PolI by targeting its subunit Rpa43, causing PolI to dissociate from the rDNA. By stimulating the processing of PolI-generated transcripts at the rDNA, Rio1 allows for rDNA condensation and segregation in late anaphase. These events finalize the genome transmission process. We identify Rio1 as an essential nucleolar housekeeper that integrates rDNA replication and segregation with ribosome biogenesis.
Highlights
The conserved protein kinase Rio[1] localizes to the cytoplasm and nucleus of eukaryotic cells
The rDNA locus exists as a tandem-repeat array comprising B150 rDNA units containing the 35S and 5S genes, which are transcribed by RNA polymerase I (PolI) and PolIII, respectively
Previous work showed that substituting conserved catalytic residue D244E in the Rio[1] kinase domain provoked plasmid loss in S. cerevisiae[21], suggesting an involvement of Rio[1] in DNA replication and/or segregation
Summary
The conserved protein kinase Rio[1] localizes to the cytoplasm and nucleus of eukaryotic cells. During rDNA replication in S phase, Rio[1] downregulates RNA polymerase I (PolI) and recruits the histone deacetylase Sir[2]. By stimulating the processing of PolI-generated transcripts at the rDNA, Rio[1] allows for rDNA condensation and segregation in late anaphase. These events finalize the genome transmission process. The removal of PolI and the local resolution of its transcripts allow the condensin complex to bind The latter compacts the rDNA array and recruits the DNA decatenating enzyme topoisomerase II (refs 1,3,4,7) resulting in the physical separation and subsequent segregation of the sister rDNA loci. The downregulation of PolI by Rio[1] and its activation of pre-rRNA processing drive rDNA condensation and segregation. We identify Rio[1] as an essential nucleolar housekeeper of rDNA integrity and transmission, and as an upstream regulator of ribosome biogenesis
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