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.
Highlights
Mobile genetic elements frequently compromise host fitness (Werren, 2011), corrupting genetic information or disturbing adaptive gene expression patterns, sometimes to lethal effect
Our results demonstrate that the presence of mitochondrial self-splicing introns has become integral to normal mitochondrial gene expression and that, curiously, normal mitochondrial function in S. cerevisiae has come to require inefficient splicing
There are no significant differences in mitochondrial inner membrane potential, as measured by 3,3’-Dihexyloxacarbocyanine iodide [DiOC6(3)] fluorescence (Figure 1f), suggesting that mitochondria are functional despite grossly altered morphology
Summary
Mobile genetic elements frequently compromise host fitness (Werren, 2011), corrupting genetic information or disturbing adaptive gene expression patterns, sometimes to lethal effect. Mobile genetic elements are ubiquitous in most eukaryotic genomes (Hurst and Werren, 2001). How do these selfish elements persist in a genomic environment where – even in the absence of selection – mutational forces constantly work to erode them? Mobile elements can donate motifs (or domains) that are co-opted into host regulatory pathways (or genic sequence) over time (Feschotte, 2008), deletions usually whittle away all but the core beneficial motif. Functional selfish elements that remain mobile are thought to persist over evolutionary time not by virtue of sporadic beneficial effects for the host, but because they replicate and spread to other sites in the genome faster than they are deleted (Feschotte, 2008). The element survives, not where it originally invaded but as a descendant copy elsewhere in the genome
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