Mitochondrial Genome Variation Affects Multiple Respiration and Nonrespiration Phenotypes in Saccharomyces cerevisiae

Mitochondrial genome variation and its effects on phenotypes have been widely analyzed in higher eukaryotes but less so in the model eukaryote Saccharomyces cerevisiae. Here, we describe mitochondrial genome variation in 96 diverse S. cerevisiae strains and assess associations between mitochondrial...

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Published in:Genetics (Austin) Vol. 211; no. 2; pp. 773 - 786
Main Authors: Vijayraghavan, Sriram, Kozmin, Stanislav G, Strope, Pooja K, Skelly, Daniel A, Lin, Zhenguo, Kennell, John, Magwene, Paul M, Dietrich, Fred S, McCusker, John H
Format: Journal Article
Language:English
Published: United States Genetics Society of America 01.02.2019
Subjects:
Antifungal Agents - toxicity
ATP synthase
ATP6 protein
Cell Respiration - genetics
Copper - toxicity
Cycloheximide
Cycloheximide - toxicity
Deoxyribonucleic acid
Disease
DNA
Drug Resistance, Fungal - genetics
Electron transport
Epistasis
Epistasis, Genetic
Eukaryotes
Gene expression
Genetics
Genome, Mitochondrial
Genomes
Genomics
Genotype & phenotype
Genotypes
Hemizygosity
Investigations
Ketoconazole
Ketoconazole - toxicity
Mitochondria
Mitochondrial DNA
Mitochondrial Proton-Translocating ATPases - genetics
Mutation
Oligomycin
Phenotype
Phenotypes
Polymorphism, Genetic
Polymorphism, Single Nucleotide
Proteins
Quantitative genetics
Respiration
Saccharomyces cerevisiae
Saccharomyces cerevisiae - drug effects
Saccharomyces cerevisiae - genetics
Saccharomyces cerevisiae Proteins - genetics
Single-nucleotide polymorphism
Strains (organisms)
Transfer RNA
Variation
Yeast
mitochondrial genome variation
transgression
Introgression
Saccharomyces cerevisiae
phenotypic variation
nuclear-mitochondrial epistasis
ISSN:1943-2631, 0016-6731, 1943-2631
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Summary:Mitochondrial genome variation and its effects on phenotypes have been widely analyzed in higher eukaryotes but less so in the model eukaryote Saccharomyces cerevisiae. Here, we describe mitochondrial genome variation in 96 diverse S. cerevisiae strains and assess associations between mitochondrial genotype and phenotypes as well as nuclear-mitochondrial epistasis. We associate sensitivity to the ATP synthase inhibitor oligomycin with SNPs in the mitochondrially encoded ATP6 gene. We describe the use of iso-nuclear F1 pairs, the mitochondrial genome equivalent of reciprocal hemizygosity analysis, to identify and analyze mitochondrial genotype-dependent phenotypes. Using iso-nuclear F1 pairs, we analyze the oligomycin phenotype-ATP6 association and find extensive nuclear-mitochondrial epistasis. Similarly, in iso-nuclear F1 pairs, we identify many additional mitochondrial genotype-dependent respiration phenotypes, for which there was no association in the 96 strains, and again find extensive nuclear-mitochondrial epistasis that likely contributes to the lack of association in the 96 strains. Finally, in iso-nuclear F1 pairs, we identify novel mitochondrial genotype-dependent nonrespiration phenotypes: resistance to cycloheximide, ketoconazole, and copper. We discuss potential mechanisms and the implications of mitochondrial genotype and of nuclear-mitochondrial epistasis effects on respiratory and nonrespiratory quantitative traits.
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Present address: The Jackson Laboratory, Bar Harbor, ME 04609.
Present address: National Center for Biotechnology Information, National Library of Medicine, National Institutes of Health, Bethesda, MD 20892.
Present address: Department Molecular and Human Genetics, Baylor College of Medicine, Houston, TX 77030-3411.
ISSN:1943-2631
0016-6731
1943-2631
DOI:10.1534/genetics.118.301546