Normal mitochondrial function in Saccharomyces cerevisiae has become dependent on inefficient splicing
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
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
- Timothy W Nilsen, Case Western Reserve University, United States
Version history
- Received: January 23, 2018
- Accepted: March 19, 2018
- Accepted Manuscript published: March 23, 2018 (version 1)
- 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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