Normal mitochondrial function in Saccharomyces cerevisiae has become dependent on inefficient splicing

  1. Marina Rudan
  2. Peter Bou Dib
  3. Marina Musa
  4. Matea Kanunnikau
  5. Sandra Sobočanec
  6. David Rueda
  7. Tobias Warnecke  Is a corresponding author
  8. Anita Kriško  Is a corresponding author
  1. Mediterranean Institute for Life Sciences, Croatia
  2. Universitätsmedizin Göttingen, Germany
  3. Rudjer Boškovic Institute, Croatia
  4. MRC London Institute of Medical Sciences, United Kingdom

Abstract

Self-splicing introns are mobile elements that have invaded a number of highly conserved genes in prokaryotic and organellar genomes. Here, we show that deletion of these selfish elements from the Saccharomyces cerevisiae mitochondrial genome is stressful to the host. A strain without mitochondrial introns displays hallmarks of the retrograde response, with altered mitochondrial morphology, gene expression and metabolism impacting growth and lifespan. Deletion of the complete suite of mitochondrial introns is phenocopied by overexpression of the splicing factor Mss116. We show that, in both cases, abnormally efficient transcript maturation results in excess levels of mature cob and cox1 host mRNA. Thus, inefficient splicing has become an integral part of normal mitochondrial gene expression. We propose that the persistence of S. cerevisiae self-splicing introns has been facilitated by an evolutionary lock-in event, where the host genome adapted to primordial invasion in a way that incidentally rendered subsequent intron loss deleterious.

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Article and author information

Author details

  1. Marina Rudan

    Mediterranean Institute for Life Sciences, Split, Croatia
    Competing interests
    The authors declare that no competing interests exist.
  2. Peter Bou Dib

    Institut für Zellbiochemie, Universitätsmedizin Göttingen, Göttingen, Germany
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-7146-8271
  3. Marina Musa

    Mediterranean Institute for Life Sciences, Split, Croatia
    Competing interests
    The authors declare that no competing interests exist.
  4. Matea Kanunnikau

    Mediterranean Institute for Life Sciences, Split, Croatia
    Competing interests
    The authors declare that no competing interests exist.
  5. Sandra Sobočanec

    Division for Molecular Medicine, Rudjer Boškovic Institute, Zagreb, Croatia
    Competing interests
    The authors declare that no competing interests exist.
  6. David Rueda

    MRC London Institute of Medical Sciences, London, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  7. Tobias Warnecke

    MRC London Institute of Medical Sciences, London, United Kingdom
    For correspondence
    tobias.warnecke@lms.mrc.ac.uk
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-4936-5428
  8. Anita Kriško

    Mediterranean Institute for Life Sciences, Split, Croatia
    For correspondence
    anita.krisko@medils.hr
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-7273-0190

Funding

NAOS Group

  • Marina Rudan
  • Marina Musa
  • Matea Kanunnikau
  • Anita Kriško

Mediterrenean Institute of Life Sciences

  • Marina Rudan
  • Marina Musa
  • Matea Kanunnikau
  • Anita Kriško

Imperial College London (Junior Research Fellowship)

  • Tobias Warnecke

Medical Research Council (Core funding)

  • Tobias Warnecke

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

Reviewing Editor

  1. Timothy W Nilsen, Case Western Reserve University, United States

Version history

  1. Received: January 23, 2018
  2. Accepted: March 19, 2018
  3. Accepted Manuscript published: March 23, 2018 (version 1)
  4. Version of Record published: April 13, 2018 (version 2)

Copyright

© 2018, Rudan 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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  1. Marina Rudan
  2. Peter Bou Dib
  3. Marina Musa
  4. Matea Kanunnikau
  5. Sandra Sobočanec
  6. David Rueda
  7. Tobias Warnecke
  8. Anita Kriško
(2018)
Normal mitochondrial function in Saccharomyces cerevisiae has become dependent on inefficient splicing
eLife 7:e35330.
https://doi.org/10.7554/eLife.35330

Share this article

https://doi.org/10.7554/eLife.35330

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