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The Mitochondrial Genome Impacts Respiration but Not Fermentation in Interspecific Saccharomyces Hybrids

In eukaryotes, mitochondrial DNA (mtDNA) has high rate of nucleotide substitution leading to different mitochondrial haplotypes called mitotypes. However, the impact of mitochondrial genetic variant on phenotypic variation has been poorly considered in microorganisms because mtDNA encodes very few g...

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Autores principales: Albertin, Warren, da Silva, Telma, Rigoulet, Michel, Salin, Benedicte, Masneuf-Pomarede, Isabelle, de Vienne, Dominique, Sicard, Delphine, Bely, Marina, Marullo, Philippe
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2013
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3781082/
https://www.ncbi.nlm.nih.gov/pubmed/24086452
http://dx.doi.org/10.1371/journal.pone.0075121
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author Albertin, Warren
da Silva, Telma
Rigoulet, Michel
Salin, Benedicte
Masneuf-Pomarede, Isabelle
de Vienne, Dominique
Sicard, Delphine
Bely, Marina
Marullo, Philippe
author_facet Albertin, Warren
da Silva, Telma
Rigoulet, Michel
Salin, Benedicte
Masneuf-Pomarede, Isabelle
de Vienne, Dominique
Sicard, Delphine
Bely, Marina
Marullo, Philippe
author_sort Albertin, Warren
collection PubMed
description In eukaryotes, mitochondrial DNA (mtDNA) has high rate of nucleotide substitution leading to different mitochondrial haplotypes called mitotypes. However, the impact of mitochondrial genetic variant on phenotypic variation has been poorly considered in microorganisms because mtDNA encodes very few genes compared to nuclear DNA, and also because mitochondrial inheritance is not uniparental. Here we propose original material to unravel mitotype impact on phenotype: we produced interspecific hybrids between S. cerevisiae and S. uvarum species, using fully homozygous diploid parental strains. For two different interspecific crosses involving different parental strains, we recovered 10 independent hybrids per cross, and allowed mtDNA fixation after around 80 generations. We developed PCR-based markers for the rapid discrimination of S. cerevisiae and S. uvarum mitochondrial DNA. For both crosses, we were able to isolate fully isogenic hybrids at the nuclear level, yet possessing either S. cerevisiae mtDNA (Sc-mtDNA) or S. uvarum mtDNA (Su-mtDNA). Under fermentative conditions, the mitotype has no phenotypic impact on fermentation kinetics and products, which was expected since mtDNA are not necessary for fermentative metabolism. Alternatively, under respiratory conditions, hybrids with Sc-mtDNA have higher population growth performance, associated with higher respiratory rate. Indeed, far from the hypothesis that mtDNA variation is neutral, our work shows that mitochondrial polymorphism can have a strong impact on fitness components and hence on the evolutionary fate of the yeast populations. We hypothesize that under fermentative conditions, hybrids may fix stochastically one or the other mt-DNA, while respiratory environments may increase the probability to fix Sc-mtDNA.
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spelling pubmed-37810822013-10-01 The Mitochondrial Genome Impacts Respiration but Not Fermentation in Interspecific Saccharomyces Hybrids Albertin, Warren da Silva, Telma Rigoulet, Michel Salin, Benedicte Masneuf-Pomarede, Isabelle de Vienne, Dominique Sicard, Delphine Bely, Marina Marullo, Philippe PLoS One Research Article In eukaryotes, mitochondrial DNA (mtDNA) has high rate of nucleotide substitution leading to different mitochondrial haplotypes called mitotypes. However, the impact of mitochondrial genetic variant on phenotypic variation has been poorly considered in microorganisms because mtDNA encodes very few genes compared to nuclear DNA, and also because mitochondrial inheritance is not uniparental. Here we propose original material to unravel mitotype impact on phenotype: we produced interspecific hybrids between S. cerevisiae and S. uvarum species, using fully homozygous diploid parental strains. For two different interspecific crosses involving different parental strains, we recovered 10 independent hybrids per cross, and allowed mtDNA fixation after around 80 generations. We developed PCR-based markers for the rapid discrimination of S. cerevisiae and S. uvarum mitochondrial DNA. For both crosses, we were able to isolate fully isogenic hybrids at the nuclear level, yet possessing either S. cerevisiae mtDNA (Sc-mtDNA) or S. uvarum mtDNA (Su-mtDNA). Under fermentative conditions, the mitotype has no phenotypic impact on fermentation kinetics and products, which was expected since mtDNA are not necessary for fermentative metabolism. Alternatively, under respiratory conditions, hybrids with Sc-mtDNA have higher population growth performance, associated with higher respiratory rate. Indeed, far from the hypothesis that mtDNA variation is neutral, our work shows that mitochondrial polymorphism can have a strong impact on fitness components and hence on the evolutionary fate of the yeast populations. We hypothesize that under fermentative conditions, hybrids may fix stochastically one or the other mt-DNA, while respiratory environments may increase the probability to fix Sc-mtDNA. Public Library of Science 2013-09-23 /pmc/articles/PMC3781082/ /pubmed/24086452 http://dx.doi.org/10.1371/journal.pone.0075121 Text en © 2013 Albertin et al http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are properly credited.
spellingShingle Research Article
Albertin, Warren
da Silva, Telma
Rigoulet, Michel
Salin, Benedicte
Masneuf-Pomarede, Isabelle
de Vienne, Dominique
Sicard, Delphine
Bely, Marina
Marullo, Philippe
The Mitochondrial Genome Impacts Respiration but Not Fermentation in Interspecific Saccharomyces Hybrids
title The Mitochondrial Genome Impacts Respiration but Not Fermentation in Interspecific Saccharomyces Hybrids
title_full The Mitochondrial Genome Impacts Respiration but Not Fermentation in Interspecific Saccharomyces Hybrids
title_fullStr The Mitochondrial Genome Impacts Respiration but Not Fermentation in Interspecific Saccharomyces Hybrids
title_full_unstemmed The Mitochondrial Genome Impacts Respiration but Not Fermentation in Interspecific Saccharomyces Hybrids
title_short The Mitochondrial Genome Impacts Respiration but Not Fermentation in Interspecific Saccharomyces Hybrids
title_sort mitochondrial genome impacts respiration but not fermentation in interspecific saccharomyces hybrids
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3781082/
https://www.ncbi.nlm.nih.gov/pubmed/24086452
http://dx.doi.org/10.1371/journal.pone.0075121
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