The orir to ori+ mutation in spontaneous yeast petites is accompanied by a drastic change in mitochondrial genome replication

Mangin, Marguerite; Faugeron-Fonty, Godeleine; Bernardi, Giorgio

doi:10.1016/0378-1119(83)90132-4

Cited by 14 publications

(5 citation statements)

References 14 publications

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“…Next, we asked if this non-uniform pattern of excision revealed new rules for mtDNA fragmentation. Besides the potential role of homology of the replication origins, it has been noted that a high density of unperturbed replication origins in Petite structures result in a replication advantage for Petite mtDNAs over wild-type mtDNAs (Blanc & Dujon, 1980;Zamaroczy et al, 1981;Mangin et al, 1983). In concatemer structures, this means that smaller repeated fragments containing replication origins are more fit than wild-type fragments when in competition with each other.…”

Section: Locations Of Excisionsmentioning

confidence: 99%

“…Studies proceeded to investigate the relationship between mtDNA structure and suppressivity, which is a measure of the replication advantage of Petite mtDNA over Grande (wild-type) mtDNA in a cross and was critical to understanding the propagation of Petite mtDNAs. After analyzing a large sample of spontaneous Petites mtDNAs, it was shown that in most cases suppressivity was correlated with origin density and that suppressivity was reduced when canonical replication origins were disrupted or absent (de Zamaroczy et al, 1981;Mangin et al, 1983). Notable exceptions to these rules were described in (Rayko et al, 1988), revealing an even more complex structure-suppressivity relationship.…”

Section: Introductionmentioning

confidence: 99%

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Contingency and selection in mitochondrial genome dynamics

Nunn

Goyal

2021

Preprint

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Eukaryotic cells contain numerous copies of mitochondrial DNA (mtDNA), allowing for the coexistence of mutant and wild-type mtDNA in individual cells. The fate of mutant mtDNA depends on their relative replicative fitness within cells and the resulting cellular fitness within populations of cells. Yet the dynamics of the generation of mutant mtDNA and features that inform their fitness remain unaddressed. Here we utilize long read single-molecule sequencing to track mtDNA mutational trajectories in Saccharomyces cerevisiae. We show a previously unseen pattern that constrains subsequent excision events in mtDNA fragmentation. We also provide evidence for the generation of rare and contentious non-periodic mtDNA structures that lead to persistent diversity within individual cells. Finally, we show that measurements of relative fitness of mtDNA fit a phenomenological model that highlights important biophysical parameters governing mtDNA fitness. Altogether, our study provides techniques and insights into the dynamics of large structural changes in genomes that may be applicable in more complex organisms.

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Section: Locations Of Excisionsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Contingency and selection in mitochondrial genome dynamics

Nunn

Goyal

2021

Preprint

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“…Illustrating this peculiar aspect of mitochondrial evolution is the suppressivity of ρ − mitogenomes in yeast. In these cells, despite a strongly deleterious effect on organismal fitness, copies of the mitochondrial genome deleted at loci essential for respiration may outcompete healthy copies thanks to their higher replication origin density ( de Zamaroczy et al 1981 ; Mangin et al 1983 ; Bernardi 2005 ). Furthermore, deletion screens in yeasts have also repeatedly identified signals of frequent essentiality switching among genes involved in mitochondrial functions, both across ( Kim et al 2010 ) and within species ( Caudal et al 2022 ; Chen et al 2022 ), suggesting enhanced evolvability at these loci.…”

Section: Introductionmentioning

confidence: 99%

Evolutionary Trajectories are Contingent on Mitonuclear Interactions

Biot-Pelletier

Bettinazzi

Gagnon‐Arsenault

et al. 2023

Molecular Biology and Evolution

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Critical mitochondrial functions, including cellular respiration, rely on frequently interacting components expressed from both the mitochondrial and nuclear genomes. The fitness of eukaryotic organisms depends on a tight collaboration between both genomes. In the face of an elevated rate of evolution in mtDNA, current models predict that maintenance of mitonuclear compatibility relies on compensatory evolution of the nuclear genome. Mitonuclear interactions would therefore exert an influence on evolutionary trajectories. One prediction from this model is that the same nuclear genome evolving with different mitochondrial haplotypes would follow distinct molecular paths towards higher fitness. To test this prediction, we submitted 1344 populations derived from seven mitonuclear genotypes of Saccharomyces cerevisiae to more than 300 generations of experimental evolution in conditions that either select for a mitochondrial function, or that do not strictly require respiration for survival. Performing high-throughput phenotyping and whole-genome sequencing on independently evolved individuals, we identified numerous examples of gene-level evolutionary convergence among populations with the same mitonuclear background. Phenotypic and genotypic data on strains derived from this evolution experiment identify the nuclear genome and the environment as the main determinants of evolutionary divergence, but also show a modulating role for the mitochondrial genome exerted both directly and via interactions with the two other components. We finally recapitulated a subset of prominent loss-of-function alleles in the ancestral backgrounds and confirmed a generalized pattern of mitonuclear-specific and highly epistatic fitness effects. Together, these results demonstrate how mitonuclear interactions can dictate evolutionary divergence of populations with identical starting nuclear genotypes.

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“…Illustrating this peculiar aspect of mitochondrial evolution is the suppressivity of ρ − mitogenomes in yeast. In these cells, despite a strongly deleterious effect on organismal fitness, copies of the mitochondrial genome deleted at loci essential for respiration outcompete healthy copies thanks to their higher replication origin density (de Zamaroczy et al 1981; Mangin et al 1983; Bernardi 2005). In summary, because of unique characteristics and selection pressures, the rate of evolution tends to be higher in the mitochondrial genome than in the nuclear genome, with a critical influence on genetic divergence, speciation, reproductive strategies, and morphology (Hill 2015).…”

Section: Introductionmentioning

confidence: 99%

“…Illustrating this peculiar aspect of mitochondrial evolution is the suppressivity of ρ - mitogenomes in yeast. In these cells, despite a strongly deleterious effect on organismal fitness, copies of the mitochondrial genome deleted at loci essential for respiration may outcompete healthy copies thanks to their higher replication origin density (de Zamaroczy et al 1981; Mangin et al 1983; Bernardi 2005). Furthermore, deletion screens in yeasts have also repeatedly identified signals of frequent essentiality switching among genes involved in mitochondrial functions, both across (Kim et al 2010) and within species (Caudal et al 2022; Chen et al 2022), suggesting enhanced evolvability at these loci.…”

Section: Introductionmentioning

confidence: 99%

Evolutionary trajectories are contingent on mitonuclear interactions

Biot-Pelletier

Bettinazzi

Gagnon‐Arsenault

et al. 2022

Preprint

View full text Add to dashboard Cite

Critical mitochondrial functions, including cellular respiration, rely on frequently interacting components expressed from both the mitochondrial and nuclear genomes. The fitness of eukaryotic organisms depends on a tight collaboration between both genomes. In the face of an elevated rate of evolution in the mitochondrial genome, current models predict that maintenance of mitonuclear compatibility relies on compensatory evolution of the nuclear genome. Mitonuclear interactions would therefore exert a strong influence on evolutionary trajectories. One prediction from this model is that the same nuclear genomes but evolving with different mitochondrial haplotypes would follow distinct molecular paths towards higher fitness peaks. To test this prediction, we submitted 1344 populations derived from seven mitonuclear genotypes of Saccharomyces cerevisiae to more than 300 generations of experimental evolution in conditions that either select for a mitochondrial function, or that do not strictly require this organelle for survival. Performing high-throughput phenotyping and whole-genome sequencing on independently evolved individuals isolated from endpoint populations, we identified numerous examples of gene-level evolutionary convergence among populations with the same mitonuclear background. We recapitulated a subset of prominent loss-of-function alleles in the ancestral backgrounds. This confirmed a generalized pattern of mitonuclear-specific and highly epistatic fitness effects. Together, these results demonstrate how mitonuclear interactions can dictate evolutionary divergence of populations with identical starting nuclear genotypes.

show abstract

The orir to ori+ mutation in spontaneous yeast petites is accompanied by a drastic change in mitochondrial genome replication

Cited by 14 publications

References 14 publications

Contingency and selection in mitochondrial genome dynamics

Contingency and selection in mitochondrial genome dynamics

Evolutionary Trajectories are Contingent on Mitonuclear Interactions

Evolutionary trajectories are contingent on mitonuclear interactions

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