Rio1 promotes rDNA stability and downregulates RNA polymerase I to ensure rDNA segregation

Nat Commun. 2015 Apr 8;6:6643. doi: 10.1038/ncomms7643.

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.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Anaphase / genetics
  • Chromosome Segregation / genetics*
  • DNA Replication / genetics
  • DNA, Ribosomal / metabolism*
  • DNA-Binding Proteins / genetics*
  • Down-Regulation
  • Protein-Serine-Threonine Kinases / genetics*
  • RNA Polymerase I / genetics*
  • S Phase / genetics
  • Saccharomyces cerevisiae
  • Saccharomyces cerevisiae Proteins / genetics*
  • Silent Information Regulator Proteins, Saccharomyces cerevisiae / genetics*
  • Sirtuin 2 / genetics*

Substances

  • DNA, Ribosomal
  • DNA-Binding Proteins
  • Rpa43 protein, S cerevisiae
  • Saccharomyces cerevisiae Proteins
  • Silent Information Regulator Proteins, Saccharomyces cerevisiae
  • Protein-Serine-Threonine Kinases
  • Rio1 protein, S cerevisiae
  • RNA Polymerase I
  • SIR2 protein, S cerevisiae
  • Sirtuin 2