Mitochondrial Recombination Reveals Mito–Mito Epistasis in Yeast

Wolters, John F.; Charron, Guillaume; Gaspary, Alec; Landry, Christian R.; Fiumera, Anthony C.; Fiumera, Heather L.

doi:10.1534/genetics.117.300660

Cited by 38 publications

(73 citation statements)

References 67 publications

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“…Has adaptation played a role in driving these incompatibilities? Although no direct links are proven, evolution of the mitochondrial genome and mito-nuclear epistasis has been linked to multiple phenotypes (Solieri et al 2008;Albertin et al 2013;Picazo et al 2014), including 37°C growth (Paliwal et al 2014, Wolters et al 2018, Leducq et al 2017, and deficiencies in mitochondrial DNA cause heat sensitivity (Zubko and Zubko 2014). Here, we show that mtDNA is important for evolution of heat and cold tolerance in distantly related species, caused by the accumulation of multiple small-to-medium effect changes and potentially mito-nuclear epistasis.…”

Section: Mitochondrial Dna and Yeast Evolutionmentioning

confidence: 79%

“…These two species are capable of forming hybrids, but the hybrids are sterile owing to both mitochondrial-nuclear incompatibilities (Lee et al 2008;Chou et al 2010) and defects in recombination due to high levels of sequence divergence (Hunter et al 1996;Liti et al 2006). Of relevance, mitochondrial genome variation has been associated with temperature-dependent growth differences among S. cerevisiae strains (Paliwal et al 2014;Wolters et al 2018) and S. paradoxus populations (Leducq et al 2017).…”

Section: Introductionmentioning

confidence: 99%

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Mitochondria-encoded genes contribute to the evolution of heat and cold tolerance amongSaccharomycesspecies

Peris

et al. 2018

Preprint

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Over time, species evolve substantial phenotype differences. Yet, genetic analysis of these traits is limited by reproductive barriers to those phenotypes that distinguish closely related species. Here, we conduct a genome-wide non-complementation screen to identify genes that contribute to a major difference in thermal growth profile between two Saccharomyces species. S. cerevisiae is capable of growing at temperatures exceeding 40C, whereas S. uvarum cannot grow above 33C but outperforms S. cerevisiae at 4C. The screen revealed only a single nuclear-encoded gene with a modest contribution to heat tolerance, but a large effect of the species' mitochondrial DNA (mitotype). Furthermore, we found that, while the S. cerevisiae mitotype confers heat tolerance, the S. uvarum mitotype confers cold tolerance. Recombinant mitotypes indicate multiple genes contribute to thermal divergence. Mitochondrial allele replacements showed that divergence in the coding sequence of COX1 has a moderate effect on both heat and cold tolerance, but it does not explain the entire difference between the two mitochondrial genomes. Our results highlight a polygenic architecture for interspecific phenotypic divergence and point to the mitochondrial genome as an evolutionary hotspot for not only reproductive incompatibilities, but also thermal divergence in yeast.

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Section: Mitochondrial Dna and Yeast Evolutionmentioning

confidence: 79%

Section: Introductionmentioning

confidence: 99%

Mitochondria-encoded genes contribute to the evolution of heat and cold tolerance amongSaccharomycesspecies

Peris

et al. 2018

Preprint

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“…Recent work has suggested that mitotype can also play a role in temperature tolerance in the model budding yeast genus Saccharomyces (6)(7)(8). The eight known Saccharomyces species are broadly divided between cryotolerant and thermotolerant species (9)(10)(11).…”

mentioning

confidence: 99%

“…Thermotolerant strains (maximum growth temperature ≥36˚C) form a clade that includes the model organism Saccharomyces cerevisiae (12), while the rest of the genus is more cryotolerant. Most prior research has focused on thermotolerance or the function of mitochondria under heat stress (~37˚C), on mitotype differences within S. cerevisiae (6,8), or on interspecies differences between S. cerevisiae and its thermotolerant sister species, Saccharomyces paradoxus (13). The genetic basis of cryotolerance in Saccharomyces has been difficult to determine using conventional crosses focused on the nuclear genome (14)(15)(16).…”

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confidence: 99%

Mitochondrial DNA and temperature tolerance in lager yeasts

Baker

Peris

Moriarty

et al. 2018

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A growing body of research suggests that the mitochondrial genome (mtDNA) is important for temperature adaptation. In the yeast genus Saccharomyces, species have diverged in temperature tolerance, driving their use in high or low temperature fermentations. Here we experimentally test the role of mtDNA in temperature tolerance in synthetic and industrial hybrids (Saccharomyces cerevisiae x Saccharomyces eubayanus, or Saccharomyces pastorianus), which cold-brew lager beer. We find that the relative temperature tolerances of hybrids correspond to the parent donating mtDNA, allowing us to modulate lager strain temperature preferences. The strong influence of mitotype on the temperature tolerance of otherwise identical hybrid strains provides support for the mitochondrial climactic adaptation 2 hypothesis in yeasts and demonstrates how mitotype has influenced the world's most commonly fermented beverage.One Sentence Summary: Mitochondrial genome origin affects the temperature tolerance of synthetic and industrial lager-brewing yeast hybrids.

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“…With mitochondria, previous studies have indicated that the mitochondrial genome plays an important role in yeast thermal adaptation [47][48][49] . We found that out of the 9 unstable enzymes identified with the Posterior etcGEMs (with a Tm lower than 42 °C, Fig S7), three (ATP1, HEM1 and PDB1) belonged to the mitochondrial energy metabolism.…”

Section: Discussionmentioning

confidence: 99%

Bayesian genome scale modelling identifies thermal determinants of yeast metabolism

Wang

et al. 2020

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The molecular basis of how temperature affects cell metabolism has been a long-standing question in biology, where the main obstacles are the lack of high-quality data and methods to associate temperature effects on the function of individual proteins as well as to combine them at a systems level. Here we develop and apply a Bayesian modeling approach to resolve the temperature effects in genome scale metabolic models (GEM). The approach minimizes uncertainties in enzymatic thermal parameters and greatly improves the predictive strength of the GEMs. The resulting temperature constrained yeast GEM uncovered enzymes that limit growth at superoptimal temperatures, and squalene epoxidase (ERG1) was predicted to be the most rate limiting. By replacing this single key enzyme with an ortholog from a thermotolerant yeast strain, we obtained a thermotolerant strain that outgrew the wild type, demonstrating the critical role of sterol metabolism in yeast thermosensitivity. Therefore, apart from identifying thermal determinants of cell metabolism and enabling the design of thermotolerant strains, our Bayesian GEM approach facilitates modelling of complex biological systems in the absence of high-quality data and therefore shows promise for becoming a standard tool for genome scale modeling.Temperature is the most common environmental and evolutionary factor that shapes the physiology of living cells. Organisms have successfully adapted to survive in diverse temperature ranges 1-3 , where minor deviations from the optimal temperature by merely a few degrees can dramatically impair cell growth. For instance, the model eukaryotic organism Saccharomyces cerevisiae has an optimal growth temperature of ~30°C, whereas a temperature of 42°C is already lethal to the organism 4,5 . Since cell growth fundamentally requires all cellular components to be functional in the temperature window of cell growth, proteins, the most abundant group of biomolecules that carry out the majority of catalytic functions and are also the most sensitive to changes in temperature 5-7 , are considered to have the largest effect on cell physiology in relation to temperature. However, despite all our knowledge of temperature effects at both the cellular and molecular levels, including recent breakthroughs in temperature-dependent protein folding 7-10 and enzyme kinetics 11,12 , the temperature association between proteins and cell physiology is still poorly understood.Multiple studies have attempted to model the temperature effects on cell growth with very few proteome wide parameters. For instance, the dominant activation barrier and the number of essential proteins to cell growth 13 , activation energy of the growth process and the free energy change of protein denaturation 14 and others (reviewed in 15 ). These models showed excellent performance when describing the general cell growth rate at various temperatures, however, they could not pinpoint the specific rate-limiting enzymes, nor predict the amount of improvement in growth rate by replacing these ...

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Mitochondrial Recombination Reveals Mito–Mito Epistasis in Yeast

Cited by 38 publications

References 67 publications

Mitochondria-encoded genes contribute to the evolution of heat and cold tolerance amongSaccharomycesspecies

Mitochondria-encoded genes contribute to the evolution of heat and cold tolerance amongSaccharomycesspecies

Mitochondrial DNA and temperature tolerance in lager yeasts

Bayesian genome scale modelling identifies thermal determinants of yeast metabolism

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