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

Author

Listed:
  • Maria G. Iacovella

    (European Institute of Oncology)

  • Cristina Golfieri

    (European Institute of Oncology
    Present addresses: German Center for Neurodegenerative Diseases (DZNE), Arnoldstraβe 18/18b, 01307 Dresden, Germany)

  • Lucia F. Massari

    (European Institute of Oncology)

  • Sara Busnelli

    (European Institute of Oncology)

  • Cinzia Pagliuca

    (European Institute of Oncology)

  • Marianna Dal Maschio

    (European Institute of Oncology)

  • Valentina Infantino

    (European Institute of Oncology)

  • Rosella Visintin

    (European Institute of Oncology)

  • Karl Mechtler

    (The Research Institute of Molecular Pathology
    The IMBA Institute of Molecular Biotechnology of the Austrian Academy of Sciences)

  • Sébastien Ferreira-Cerca

    (Lehrstuhl für Biochemie III, Universität Regensburg)

  • Peter De Wulf

    (European Institute of Oncology)

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.

Suggested Citation

  • Maria G. Iacovella & Cristina Golfieri & Lucia F. Massari & Sara Busnelli & Cinzia Pagliuca & Marianna Dal Maschio & Valentina Infantino & Rosella Visintin & Karl Mechtler & Sébastien Ferreira-Cerca &, 2015. "Rio1 promotes rDNA stability and downregulates RNA polymerase I to ensure rDNA segregation," Nature Communications, Nature, vol. 6(1), pages 1-16, May.
    • Handle: RePEc:nat:natcom:v:6:y:2015:i:1:d:10.1038_ncomms7643
    DOI: 10.1038/ncomms7643
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    Cited by:

    1. Ksenia Smurova & Michela Damizia & Carmela Irene & Stefania Stancari & Giovanna Berto & Giulia Perticari & Maria Giuseppina Iacovella & Ilaria D’Ambrosio & Maria Giubettini & Réginald Philippe & Chiar, 2023. "Rio1 downregulates centromeric RNA levels to promote the timely assembly of structurally fit kinetochores," Nature Communications, Nature, vol. 14(1), pages 1-19, December.

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