1. Chromosomes and Gene Expression
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The dynamic assembly of distinct RNA polymerase I complexes modulates rDNA transcription

  1. Eva Torreira
  2. Jaime Alegrio Louro
  3. Irene Pazos
  4. Noelia González-Polo
  5. David Gil-Carton
  6. Ana Garcia Duran
  7. Sébastien Tosi
  8. Oriol Gallego  Is a corresponding author
  9. Olga Calvo
  10. Carlos Fernández-Tornero  Is a corresponding author
  1. Centro de Investigaciones Biológicas, Spain
  2. The Barcelona Institute of Science and Technology, Spain
  3. Instituto de Biología Funcional y Genómica, Spain
  4. Cooperative Center for Research in Biosciences CIC bioGUNE, Spain
Research Article
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Cite this article as: eLife 2017;6:e20832 doi: 10.7554/eLife.20832

Abstract

Cell growth requires synthesis of ribosomal RNA by RNA polymerase I (Pol I). Binding of initiation factor Rrn3 activates Pol I, fostering recruitment to ribosomal DNA promoters. This fundamental process must be precisely regulated to satisfy cell needs at any time. We present in vivo evidence that, when growth is arrested by nutrient deprivation, cells induce rapid clearance of Pol I-Rrn3 complexes, followed by the assembly of inactive Pol I homodimers. This dual repressive mechanism reverts upon nutrient addition, thus restoring cell growth. Moreover, Pol I dimers also form after inhibition of either ribosome biogenesis or protein synthesis. Our mutational analysis, based on the electron cryomicroscopy structures of monomeric Pol I alone and in complex with Rrn3, underscores the central role of subunits A43 and A14 in the regulation of differential Pol I complexes assembly and subsequent promoter association.

Article and author information

Author details

  1. Eva Torreira

    Centro de Investigaciones Biológicas, Madrid, Spain
    Competing interests
    The authors declare that no competing interests exist.
  2. Jaime Alegrio Louro

    Centro de Investigaciones Biológicas, Madrid, Spain
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-2800-923X
  3. Irene Pazos

    Institute for Research in Biomedicine, The Barcelona Institute of Science and Technology, Barcelona, Spain
    Competing interests
    The authors declare that no competing interests exist.
  4. Noelia González-Polo

    Instituto de Biología Funcional y Genómica, Salamanca, Spain
    Competing interests
    The authors declare that no competing interests exist.
  5. David Gil-Carton

    Structural Biology Unit, Cooperative Center for Research in Biosciences CIC bioGUNE, Derio, Spain
    Competing interests
    The authors declare that no competing interests exist.
  6. Ana Garcia Duran

    Institute for Research in Biomedicine, The Barcelona Institute of Science and Technology, Barcelona, Spain
    Competing interests
    The authors declare that no competing interests exist.
  7. Sébastien Tosi

    Institute for Research in Biomedicine, The Barcelona Institute of Science and Technology, Barcelona, Spain
    Competing interests
    The authors declare that no competing interests exist.
  8. Oriol Gallego

    Institute for Research in Biomedicine, The Barcelona Institute of Science and Technology, Barcelona, Spain
    For correspondence
    oriol.gallego@irbbarcelona.org
    Competing interests
    The authors declare that no competing interests exist.
  9. Olga Calvo

    Instituto de Biología Funcional y Genómica, Salamanca, Spain
    Competing interests
    The authors declare that no competing interests exist.
  10. Carlos Fernández-Tornero

    Centro de Investigaciones Biológicas, Madrid, Spain
    For correspondence
    cftornero@cib.csic.es
    Competing interests
    The authors declare that no competing interests exist.

Funding

Ministerio de Economía y Competitividad (BFU2013-48374-P)

  • Carlos Fernández-Tornero

Fundación Ramón Areces (-)

  • Carlos Fernández-Tornero

Ministerio de Economía y Competitividad (RYC-2011-07967)

  • Oriol Gallego

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Reviewing Editor

  1. Alan G Hinnebusch, National Institutes of Health, United States

Publication history

  1. Received: August 21, 2016
  2. Accepted: March 6, 2017
  3. Accepted Manuscript published: March 6, 2017 (version 1)
  4. Accepted Manuscript updated: March 8, 2017 (version 2)
  5. Version of Record published: March 22, 2017 (version 3)
  6. Version of Record updated: March 24, 2017 (version 4)

Copyright

© 2017, Torreira et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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