Mitochondrial Genome Instability in <i>W303-SK1</i> Yeast Cytoplasmic Hybrids
Unlike most animals, some fungi, including baker’s yeast, inherit mitochondrial DNA (mtDNA) from both parents. When haploid yeast cells fuse, they form a heteroplasmic zygote, whose offspring retain one or the other variant of mtDNA. Meanwhile, some mutant mtDNA (<i>rho<sup>−</sup>...
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2024-11-01
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| author | Khoren K. Epremyan Arteom A. Burlaka Olga V. Markova Kseniia V. Galkina Dmitry A. Knorre |
| author_facet | Khoren K. Epremyan Arteom A. Burlaka Olga V. Markova Kseniia V. Galkina Dmitry A. Knorre |
| author_sort | Khoren K. Epremyan |
| collection | DOAJ |
| description | Unlike most animals, some fungi, including baker’s yeast, inherit mitochondrial DNA (mtDNA) from both parents. When haploid yeast cells fuse, they form a heteroplasmic zygote, whose offspring retain one or the other variant of mtDNA. Meanwhile, some mutant mtDNA (<i>rho<sup>−</sup></i>), with large deletions in the nucleotide sequence, can displace wild-type (<i>rho<sup>+</sup></i>) mtDNA. Consequently, offspring of zygotes with such <i>rho<sup>−</sup></i> mtDNA predominantly carry the mutant variant. This phenomenon is called suppressivity. In this study, we investigated how the suppressivity of <i>rho<sup>−</sup></i> mtDNA depends on the mitochondrial and nuclear genomes of the <i>rho<sup>+</sup></i> strain during crossing. Comparing two diverged laboratory strains, <i>SK1</i> and <i>W303</i>, we measured suppressivity in crosses with four <i>rho<sup>−</sup></i> strains. One <i>rho<sup>−</sup></i> strain showed significantly higher suppressivity when crossed with <i>SK1</i> than with <i>W303</i>. We then created cytoplasmic hybrids by swapping mtDNAs between these strains. Surprisingly, we found that the mtDNA of the <i>rho<sup>+</sup></i> strain, rather than its nuclear DNA, determines high suppressivity in crosses of <i>SK1 rho<sup>+</sup></i> with the <i>rho<sup>−</sup></i> strain. Additionally, mtDNA replacement reduced respiration rate and growth rate on non-fermentable substrates while increasing the likelihood of functional mtDNA loss. Our data demonstrate that a mutant mtDNA variant’s ability to displace another mitochondrial DNA variant in a heteroplasmic cell depends more on mtDNA sequences than on the biochemical and structural context created by the nuclear genome background. |
| format | Article |
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| language | English |
| publishDate | 2024-11-01 |
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| spelling | doaj-art-2134aee050a84b109f7f499121cf0c692025-08-20T02:08:02ZengMDPI AGBiology2079-77372024-11-01131192710.3390/biology13110927Mitochondrial Genome Instability in <i>W303-SK1</i> Yeast Cytoplasmic HybridsKhoren K. Epremyan0Arteom A. Burlaka1Olga V. Markova2Kseniia V. Galkina3Dmitry A. Knorre4A.N. Belozersky Institute of Physico-Chemical Biology, Lomonosov Moscow State University, Leninskiye Gory, 1-40, 119234 Moscow, RussiaFaculty of Bioengineering and Bioinformatics, Lomonosov Moscow State University, Leninskiye Gory, 1-73, 119234 Moscow, RussiaA.N. Belozersky Institute of Physico-Chemical Biology, Lomonosov Moscow State University, Leninskiye Gory, 1-40, 119234 Moscow, RussiaA.N. Belozersky Institute of Physico-Chemical Biology, Lomonosov Moscow State University, Leninskiye Gory, 1-40, 119234 Moscow, RussiaA.N. Belozersky Institute of Physico-Chemical Biology, Lomonosov Moscow State University, Leninskiye Gory, 1-40, 119234 Moscow, RussiaUnlike most animals, some fungi, including baker’s yeast, inherit mitochondrial DNA (mtDNA) from both parents. When haploid yeast cells fuse, they form a heteroplasmic zygote, whose offspring retain one or the other variant of mtDNA. Meanwhile, some mutant mtDNA (<i>rho<sup>−</sup></i>), with large deletions in the nucleotide sequence, can displace wild-type (<i>rho<sup>+</sup></i>) mtDNA. Consequently, offspring of zygotes with such <i>rho<sup>−</sup></i> mtDNA predominantly carry the mutant variant. This phenomenon is called suppressivity. In this study, we investigated how the suppressivity of <i>rho<sup>−</sup></i> mtDNA depends on the mitochondrial and nuclear genomes of the <i>rho<sup>+</sup></i> strain during crossing. Comparing two diverged laboratory strains, <i>SK1</i> and <i>W303</i>, we measured suppressivity in crosses with four <i>rho<sup>−</sup></i> strains. One <i>rho<sup>−</sup></i> strain showed significantly higher suppressivity when crossed with <i>SK1</i> than with <i>W303</i>. We then created cytoplasmic hybrids by swapping mtDNAs between these strains. Surprisingly, we found that the mtDNA of the <i>rho<sup>+</sup></i> strain, rather than its nuclear DNA, determines high suppressivity in crosses of <i>SK1 rho<sup>+</sup></i> with the <i>rho<sup>−</sup></i> strain. Additionally, mtDNA replacement reduced respiration rate and growth rate on non-fermentable substrates while increasing the likelihood of functional mtDNA loss. Our data demonstrate that a mutant mtDNA variant’s ability to displace another mitochondrial DNA variant in a heteroplasmic cell depends more on mtDNA sequences than on the biochemical and structural context created by the nuclear genome background.https://www.mdpi.com/2079-7737/13/11/927yeastmtDNAcytoplasmic hybridssuppressivitymito-nuclear incompatibility |
| spellingShingle | Khoren K. Epremyan Arteom A. Burlaka Olga V. Markova Kseniia V. Galkina Dmitry A. Knorre Mitochondrial Genome Instability in <i>W303-SK1</i> Yeast Cytoplasmic Hybrids Biology yeast mtDNA cytoplasmic hybrids suppressivity mito-nuclear incompatibility |
| title | Mitochondrial Genome Instability in <i>W303-SK1</i> Yeast Cytoplasmic Hybrids |
| title_full | Mitochondrial Genome Instability in <i>W303-SK1</i> Yeast Cytoplasmic Hybrids |
| title_fullStr | Mitochondrial Genome Instability in <i>W303-SK1</i> Yeast Cytoplasmic Hybrids |
| title_full_unstemmed | Mitochondrial Genome Instability in <i>W303-SK1</i> Yeast Cytoplasmic Hybrids |
| title_short | Mitochondrial Genome Instability in <i>W303-SK1</i> Yeast Cytoplasmic Hybrids |
| title_sort | mitochondrial genome instability in i w303 sk1 i yeast cytoplasmic hybrids |
| topic | yeast mtDNA cytoplasmic hybrids suppressivity mito-nuclear incompatibility |
| url | https://www.mdpi.com/2079-7737/13/11/927 |
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