Discordant evolution of mitochondrial and nuclear yeast genomes at population level

Abstract

Background: Mitochondria are essential organelles partially regulated by their own genomes. The mitochondrial genome maintenance and inheritance differ from the nuclear genome, potentially uncoupling their evolutionary trajectories. Here, we analysed mitochondrial sequences obtained from the 1011 Saccharomyces cerevisiae strain collection and identified pronounced differences with their nuclear genome counterparts. Results: In contrast with pre-whole genome duplication fungal species, S. cerevisiae mitochondrial genomes show higher genetic diversity compared to the nuclear genomes. Strikingly, mitochondrial genomes appear to be highly admixed, resulting in a complex interconnected phylogeny with a weak grouping of isolates, whereas interspecies introgressions are very rare. Complete genome assemblies revealed that structural rearrangements are nearly absent with rare inversions detected. We tracked intron variation in COX1 and COB to infer gain and loss events throughout the species evolutionary history. Mitochondrial genome copy number is connected with the nuclear genome and linearly scale up with ploidy. We observed rare cases of naturally occurring mitochondrial DNA loss, petite, with a subset of them that do not suffer the expected growth defect in fermentable rich media. Conclusions: Overall, our results illustrate how differences in the biology of two genomes coexisting in the same cells can lead to discordant evolutionary histories.

Editorial: The Significance of Mitogenomics in Mycology

“…Wolters et al (2015) revealed that the distribution of mitochondrial introns in S. cerevisiae had population-specific profiles. However, further work by De Chiara et al (2020) showed that despite high mtDNA polymorphism, mitochondrial population structure poorly reflects the clustering based on nuclear data, which indicated that in yeasts both nuclear and mitochondrial genomes are affected by outbreeding. The limitations of mitogenomics in population surveys have been recently underlined in studies on plant pathogenic Fusaria.…”

“…Nearly all mechanisms responsible for maintaining the nuclear genome integrity, such as mismatch repair, base excision repair, and double-strand break repair via homologous recombination or the non-homologous end-joining pathway, also occur to maintain mtDNA stability (Kaniak-Golik and Skoneczna, 2015 ). In fungi, the mutation rate in mtDNA is usually lower than in nuclear genomes (De Chiara et al, 2020 ). However, it is worth noting that the mutation rate in mtDNA appears to be dependent upon the fungal group studied.…”

“…Some recent examples of new phylogenetic insights were derived from studies in nematode-trapping fungi ( Zhang et al ), the commercialized edible mushroom Hypsizygus marmoreus (Wang et al, 2019 ), and ectomycorrhizal fungi from the genus Rhizopogon (Li et al, 2019 ). It is worth noting however, that estimating phylogenetic relationships of fungi based on both mitogenome and nuclear phylogenies can be difficult due to their highly discordant evolutionary trajectories (De Chiara et al, 2020 ).…”

Mitochondrial-nuclear coadaptation revealed through mtDNA replacements in Saccharomyces cerevisiae

“…Saccharomyces yeasts have a highly structured population [ 49 , 50 ] with limited outcrossing [ 44 ]. Mitochondrial recombination is an important consequence of yeast matings in nature [ 45 , 46 , 51 , 52 ], indicating that beneficial mitochondrial alleles could be isolated and available for selection. This is most likely to occur when yeasts mate outside their local population, such as when transferred by insect and human vectors [ 53 , 54 ] where hybridization with local yeasts can occur [ 55 ].…”

Genomic Adaptation of Saccharomyces Species to Industrial Environments

“…Compared to the nuclear genomes, the mtDNA in Saccharomyces cerevisiae is more diverted and highly assorted. Structural rearrangements are rare in mtDNA resulting in few cases of DNA loss (De Chiara et al, 2020), however, mitochondrial recombination is common and can lead to phenotypic differentiation if enough divergence is present in the parental species (Leducq et al, 2017). Recent studies showed a strong influence on the different parental mtDNA in S. pastorianus strains related with adaptation to cold temperatures (Baker et al, 2019;Hewitt et al, 2020).…”