Mitonuclear interplay in yeast: from speciation to phenotypic adaptation

Visinoni, Federico; Delneri, Daniela

doi:10.1016/j.gde.2022.101957

Cited by 8 publications

(4 citation statements)

References 48 publications

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“…Pairing the data with the previously generated nuclear genomes will help elucidate the interplay between these two et al 10.3389/fmicb.2023.1268944 Frontiers in Microbiology 10 frontiersin.org genomes. Mitochondrial-nuclear epistasis has been demonstrated to affect phenotypic variation in yeasts (Paliwal al., 2014;Nguyen T. H. M. et al, 2020;Visinoni and Delneri, 2022;Biot-Pelletier et al, 2023;Nguyen et al, 2023) and a diverse array of model systems (Dowling et al, 2007;Burton and Barreto, 2012;Mossman et al, 2016). For many existing mitochondrial genomes, any analysis of such interactions was previously often complicated by the lack of a corresponding nuclear genome or by mismatches between the strains sequenced for a given species.…”

Section: Discussionmentioning

confidence: 99%

Mitochondrial genome diversity across the subphylum Saccharomycotina

Wolters,

LaBella,

Opulente

et al. 2023

Front. Microbiol.

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IntroductionEukaryotic life depends on the functional elements encoded by both the nuclear genome and organellar genomes, such as those contained within the mitochondria. The content, size, and structure of the mitochondrial genome varies across organisms with potentially large implications for phenotypic variance and resulting evolutionary trajectories. Among yeasts in the subphylum Saccharomycotina, extensive differences have been observed in various species relative to the model yeast Saccharomyces cerevisiae, but mitochondrial genome sampling across many groups has been scarce, even as hundreds of nuclear genomes have become available.MethodsBy extracting mitochondrial assemblies from existing short-read genome sequence datasets, we have greatly expanded both the number of available genomes and the coverage across sparsely sampled clades.ResultsComparison of 353 yeast mitochondrial genomes revealed that, while size and GC content were fairly consistent across species, those in the genera Metschnikowia and Saccharomyces trended larger, while several species in the order Saccharomycetales, which includes S. cerevisiae, exhibited lower GC content. Extreme examples for both size and GC content were scattered throughout the subphylum. All mitochondrial genomes shared a core set of protein-coding genes for Complexes III, IV, and V, but they varied in the presence or absence of mitochondrially-encoded canonical Complex I genes. We traced the loss of Complex I genes to a major event in the ancestor of the orders Saccharomycetales and Saccharomycodales, but we also observed several independent losses in the orders Phaffomycetales, Pichiales, and Dipodascales. In contrast to prior hypotheses based on smaller-scale datasets, comparison of evolutionary rates in protein-coding genes showed no bias towards elevated rates among aerobically fermenting (Crabtree/Warburg-positive) yeasts. Mitochondrial introns were widely distributed, but they were highly enriched in some groups. The majority of mitochondrial introns were poorly conserved within groups, but several were shared within groups, between groups, and even across taxonomic orders, which is consistent with horizontal gene transfer, likely involving homing endonucleases acting as selfish elements.DiscussionAs the number of available fungal nuclear genomes continues to expand, the methods described here to retrieve mitochondrial genome sequences from these datasets will prove invaluable to ensuring that studies of fungal mitochondrial genomes keep pace with their nuclear counterparts.

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Section: Discussionmentioning

confidence: 99%

Mitochondrial genome diversity across the subphylum Saccharomycotina

Wolters,

LaBella,

Opulente

et al. 2023

Front. Microbiol.

View full text Add to dashboard Cite

show abstract

“…Pairing the data with the previously generated nuclear genomes will help elucidate the interplay between these two genomes. Interactions between mitochondrial and nuclear loci (mito-nuclear epistasis) have been demonstrated to affect phenotypic variation in yeasts (Paliwal et al, 2014;Nguyen et al, 2020bNguyen et al, , 2023Visinoni and Delneri, 2022;Biot-Pelletier et al, 2023) and a diverse array of model systems (Dowling et al, 2007;Burton and Barreto, 2012;Mossman et al, 2016). For many existing mitochondrial genomes, any analysis of such interactions was previously often complicated by the lack of a corresponding nuclear genome or by mismatches between the strains sequenced for a given species.…”

Section: Discussionmentioning

confidence: 99%

Mitochondrial Genome Diversity across the Subphylum Saccharomycotina

Wolters,

LaBella,

Opulente

et al. 2023

Preprint

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Eukaryotic life depends on the functional elements encoded by both the nuclear genome and organellar genomes, such as those contained within the mitochondria. The content, size, and structure of the mitochondrial genome varies across organisms with potentially large implications for phenotypic variance and resulting evolutionary trajectories. Among yeasts in the subphylum Saccharomycotina, extensive differences have been observed in various species relative to the model yeast Saccharomyces cerevisiae, but mitochondrial genome sampling across many groups has been scarce, even as hundreds of nuclear genomes have become available. By extracting mitochondrial assemblies from existing short-read genome sequence datasets, we have greatly expanded both the number of available genomes and the coverage across sparsely sampled clades. Comparison of 353 yeast mitochondrial genomes revealed that, while size and GC content were fairly consistent across species, those in the genera Metschnikowia and Saccharomyces trended larger, while several species in the order Saccharomycetales, which includes S. cerevisiae, exhibited lower GC content. Extreme examples for both size and GC content were scattered throughout the subphylum. All mitochondrial genomes shared a core set of protein-coding genes for Complexes III, IV, and V, but they varied in the presence or absence of mitochondrially-encoded canonical Complex I genes. We traced the loss of Complex I genes to a major event in the ancestor of the orders Saccharomycetales and Saccharomycodales, but we also observed several independent losses in the orders Phaffomycetales, Pichiales, and Dipodascales. In contrast to prior hypotheses based on smaller-scale datasets, comparison of evolutionary rates in protein-coding genes showed no bias towards elevated rates among aerobically fermenting (Crabtree/Warburg-positive) yeasts. Mitochondrial introns were widely distributed, but they were highly enriched in some groups. The majority of mitochondrial introns were poorly conserved within groups, but several were shared within groups, between groups, and even across taxonomic orders, which is consistent with horizontal gene transfer, likely involving homing endonucleases acting as selfish elements. As the number of available fungal nuclear genomes continues to expand, the methods described here to retrieve mitochondrial genome sequences from these datasets will prove invaluable to ensuring that studies of fungal mitochondrial genomes keep pace with their nuclear counterparts.

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“…Thus, mutations occurring in one of these interacting genomic regions must be repaired or compensated by the counterpart through a counter-mutation (Hill, 2020). Once the compensation process occurs in a specific lineage, mitochondrial and nuclear mutations can cause incompatibilities with other individuals from the same species (Burton, 2022; Visinoni & Delneri, 2022).…”

Section: Introductionmentioning

confidence: 99%

Rearrangements and accelerated mutation rates on Dendrodorididae mitogenomes rumble their evolution

Galià-Camps,

Schell,

Enguídanos

et al. 2024

Preprint

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The systematics of the family Dendrodorididae poses a challenge to evolutionary biologists, as their mitochondrial and nuclear markers provide contradictory phylogenetic signals. Nuclear pseudogenes or exogenous contamination are hypothesized to cause the molecular discordance. However, these hypotheses have not been tested. We used genomic data from seven Dendrodorididae species to investigate the evolution of this family. Two mitogenomes displayed a novel structural rearrangement in nudibranchs, involving the translocation of three collinear genes and five surrounding tRNAs. Additionally, we found numerous mitogenomic regions with non-synonymous mutations and multiple indels in both coding and ribosomal genes. Protein modeling resulted in similar structures, suggesting that functionality is conserved. Phylogenies using mitogenomic data confirmed a specific clade membership for the rearranged mitogenomes. The incorporation of nuclear data did not fully resolve the systematic relationships of Dendrodorididae, acknowledging the evolutionary complexity of this group. The present study provides novel evidence on sudden molecular changes in mitogenomes, and highlights the relevance of using genomic data to unveil rare evolutionary processes, which is critical for understanding evolution of neglected taxa.

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Mitonuclear interplay in yeast: from speciation to phenotypic adaptation

Cited by 8 publications

References 48 publications

Mitochondrial genome diversity across the subphylum Saccharomycotina

Mitochondrial genome diversity across the subphylum Saccharomycotina

Mitochondrial Genome Diversity across the Subphylum Saccharomycotina

Rearrangements and accelerated mutation rates on Dendrodorididae mitogenomes rumble their evolution

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