Background: Mitochondrial function requires numerous genetic interactions between mitochondrial- and nuclear- encoded genes. While selection for optimal mitonuclear interactions should result in coevolution between both genomes, evidence for mitonuclear coadaptation is challenging to document. Genetic models where mitonuclear interactions can be explored are needed.
Results: We systematically exchanged mtDNAs between 15 Saccharomyces cerevisiae isolates from a variety of ecological niches to create 225 unique mitochondrial-nuclear genotypes. Analysis of phenotypic profiles confirmed that environmentally-sensitive interactions between mitochondrial and nuclear genotype contributed to growth differences. Exchanges of mtDNAs between strains of the same or different clades were just as likely to demonstrate mitonuclear epistasis although epistatic effect sizes increased with genetic distances. Strains with their original mtDNAs were more fit than strains with synthetic mitonuclear combinations when grown in media emulating their original ecological niches.
Conclusions: This study shows that natural variation in mitonuclear interactions contribute to fitness landscapes and thus provide a platform for natural selection to promote coevolution. Multiple examples of coadapted mitochondrial-nuclear genotypes suggest that selection for mitonuclear interactions is an important evolutionary force that has helped shape the population structure of S. cerevisiae.