Discordant evolution of mitochondrial and nuclear yeast genomes at population level

Chiara, Matteo De; Friedrich, Anne; Barré, Benjamin; Breitenbach, Michael; Schacherer, Joseph; Liti, Gianni

doi:10.1101/855858

Cited by 18 publications

(36 citation statements)

References 73 publications

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“…Identifying the exact loci underlying mitonuclear interactions is an obvious future goal. This study highlights that mapping efforts will need to consider that coadapted mitonuclear loci are likely strain and niche speci c. Most analysis of yeast mtDNAs have focused on coding sequences [51,52,74]. We did not nd associations between mitochondrial coding SNPs and growth phenotypes in environments revealing coadapted mitonuclear genotypes.…”

Section: Discussionmentioning

confidence: 64%

“…The mitochondrial genomes from these 15 isolates are highly polymorphic with unique allelic pro les across their coding sequences (Table S2), with the exception of 2 wine/European strains (YJM981 and YJM975) that have identical mitochondrial coding sequences. The nucleotide diversity for these 15 mitochondrial coding sequences is slightly higher than found across a comparison of 353 mtDNAs (0.01 (Table S3) vs. 0.0085 [52] with the majority of sequence differences found in COX1, COX2 and VAR1. These mtDNAs did not present evidence of gene rearrangements or interspeci c introgressions as have been sometimes observed [51,52].…”

Section: A Mitonuclear Strain Collection Allows For Direct Assessmentmentioning

confidence: 64%

“…The nucleotide diversity for these 15 mitochondrial coding sequences is slightly higher than found across a comparison of 353 mtDNAs (0.01 (Table S3) vs. 0.0085 [52] with the majority of sequence differences found in COX1, COX2 and VAR1. These mtDNAs did not present evidence of gene rearrangements or interspeci c introgressions as have been sometimes observed [51,52]. While these selected isolates do not necessarily represent all the genetic diversity that describes S. cerevisiae populations [49,52], they do capture a substantial amount of the genetic complexity leading to trait variation.…”

Section: A Mitonuclear Strain Collection Allows For Direct Assessmentmentioning

confidence: 64%

“…These mtDNAs did not present evidence of gene rearrangements or interspeci c introgressions as have been sometimes observed [51,52]. While these selected isolates do not necessarily represent all the genetic diversity that describes S. cerevisiae populations [49,52], they do capture a substantial amount of the genetic complexity leading to trait variation.…”

Section: A Mitonuclear Strain Collection Allows For Direct Assessmentmentioning

confidence: 77%

“…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 bene cial 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].…”

Section: Introductionmentioning

confidence: 99%

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Mitochondrial-nuclear coadaptation revealed through mtDNA replacements in Saccharomyces cerevisiae

Nguyen

Sondhi

Ziesel

et al. 2020

Preprint

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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 that resembled isolation habitats. Conclusions: This study shows that natural variation in mitonuclear interactions contributes to fitness landscapes. Multiple examples of coadapted mitochondrial-nuclear genotypes suggest that selection for mitonuclear interactions may play a role in helping yeasts adapt to novel environments and promote coevolution.

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Section: Discussionmentioning

confidence: 64%

Section: A Mitonuclear Strain Collection Allows For Direct Assessmentmentioning

confidence: 64%

Section: A Mitonuclear Strain Collection Allows For Direct Assessmentmentioning

confidence: 64%

Section: A Mitonuclear Strain Collection Allows For Direct Assessmentmentioning

confidence: 77%

Section: Introductionmentioning

confidence: 99%

See 3 more Smart Citations

Mitochondrial-nuclear coadaptation revealed through mtDNA replacements in Saccharomyces cerevisiae

Nguyen

Sondhi

Ziesel

et al. 2020

Preprint

View full text Add to dashboard Cite

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Macroevolutionary diversity of traits and genomes in the model yeast genus Saccharomyces

et al. 2023

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Species is the fundamental unit to quantify biodiversity. In recent years, the model yeast Saccharomyces cerevisiae has seen an increased number of studies related to its geographical distribution, population structure, and phenotypic diversity. However, seven additional species from the same genus have been less thoroughly studied, which has limited our understanding of the macroevolutionary events leading to the diversification of this genus over the last 20 million years. Here, we show the geographies, hosts, substrates, and phylogenetic relationships for approximately 1,800 Saccharomyces strains, covering the complete genus with unprecedented breadth and depth. We generated and analyzed complete genome sequences of 163 strains and phenotyped 128 phylogenetically diverse strains. This dataset provides insights about genetic and phenotypic diversity within and between species and populations, quantifies reticulation and incomplete lineage sorting, and demonstrates how gene flow and selection have affected traits, such as galactose metabolism. These findings elevate the genus Saccharomyces as a model to understand biodiversity and evolution in microbial eukaryotes.

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Restoring fertility in yeast hybrids: Breeding and quantitative genetics of beneficial traits

Naseeb

Visinoni

et al. 2021

Proc. Natl. Acad. Sci. U.S.A.

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Hybrids between species can harbor a combination of beneficial traits from each parent and may exhibit hybrid vigor, more readily adapting to new harsher environments. Interspecies hybrids are also sterile and therefore an evolutionary dead end unless fertility is restored, usually via auto-polyploidisation events. In the Saccharomyces genus, hybrids are readily found in nature and in industrial settings, where they have adapted to severe fermentative conditions. Due to their hybrid sterility, the development of new commercial yeast strains has so far been primarily conducted via selection methods rather than via further breeding. In this study, we overcame infertility by creating tetraploid intermediates of Saccharomyces interspecies hybrids to allow continuous multigenerational breeding. We incorporated nuclear and mitochondrial genetic diversity within each parental species, allowing for quantitative genetic analysis of traits exhibited by the hybrids and for nuclear–mitochondrial interactions to be assessed. Using pooled F12 generation segregants of different hybrids with extreme phenotype distributions, we identified quantitative trait loci (QTLs) for tolerance to high and low temperatures, high sugar concentration, high ethanol concentration, and acetic acid levels. We identified QTLs that are species specific, that are shared between species, as well as hybrid specific, in which the variants do not exhibit phenotypic differences in the original parental species. Moreover, we could distinguish between mitochondria-type–dependent and –independent traits. This study tackles the complexity of the genetic interactions and traits in hybrid species, bringing hybrids into the realm of full genetic analysis of diploid species, and paves the road for the biotechnological exploitation of yeast biodiversity.

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Discordant evolution of mitochondrial and nuclear yeast genomes at population level

Cited by 18 publications

References 73 publications

Mitochondrial-nuclear coadaptation revealed through mtDNA replacements in Saccharomyces cerevisiae

Mitochondrial-nuclear coadaptation revealed through mtDNA replacements in Saccharomyces cerevisiae

Macroevolutionary diversity of traits and genomes in the model yeast genus Saccharomyces

Restoring fertility in yeast hybrids: Breeding and quantitative genetics of beneficial traits

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