Linking the mitochondrial genotype to phenotype: a complex endeavour

Ghiselli, Fabrizio; Milani, Liliana

doi:10.1098/rstb.2019.0169

Cited by 30 publications

(16 citation statements)

References 48 publications

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“…While the coevolution of mitochondrial and nuclear genomes does occur, the unique biology of mitochondria complicates our view of a species' evolutionary history [32][33][34][35][36][37][38]. In most metazoans, uniparental inheritance, lack of recombination and high mutation rate of mtDNAs make it difficult to separate the effect of genetic drift from natural selection [39].…”

Section: Introductionmentioning

confidence: 99%

Mitochondrial-nuclear coadaptation revealed through mtDNA replacements in Saccharomyces cerevisiae

et al. 2020

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Background Mitochondrial function requires numerous genetic interactions between mitochondrial- and nuclear- encoded genes. While selection for optimal mitonuclear interactions should result in coevolution between both genomes, evidence for mitonuclear coadaptation is challenging to document. Genetic models where mitonuclear interactions can be explored are needed. Results We systematically exchanged mtDNAs between 15 Saccharomyces cerevisiae isolates from a variety of ecological niches to create 225 unique mitochondrial-nuclear genotypes. Analysis of phenotypic profiles confirmed that environmentally-sensitive interactions between mitochondrial and nuclear genotype contributed to growth differences. Exchanges of mtDNAs between strains of the same or different clades were just as likely to demonstrate mitonuclear epistasis although epistatic effect sizes increased with genetic distances. Strains with their original mtDNAs were more fit than strains with synthetic mitonuclear combinations when grown in media that resembled isolation habitats. Conclusions This study shows that natural variation in mitonuclear interactions contributes to fitness landscapes. Multiple examples of coadapted mitochondrial-nuclear genotypes suggest that selection for mitonuclear interactions may play a role in helping yeasts adapt to novel environments and promote coevolution.

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Section: Introductionmentioning

confidence: 99%

Mitochondrial-nuclear coadaptation revealed through mtDNA replacements in Saccharomyces cerevisiae

et al. 2020

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“…The coevolution between mitochondrial and nuclear genes is one of the oldest and best-studied examples of symbiosis [1][2][3]. Orchestrated interaction between the two genomes is essential for a number of eukaryotic traits, especially metabolism and energy production [4][5][6][7], and this intimate coordination has been taken as evidence for positive selection for cooperative mito-nuclear combinations [8,9]. Moreover, there has also been a well-documented transfer of genes from the mitochondrial to the nuclear genome [10][11][12] and bilaterian animal mitochondrial genomes, with a few exceptions, contain only 37 genes.…”

Section: Introductionmentioning

confidence: 99%

Mitochondrial-Y chromosome epistasis inDrosophila melanogaster

2020

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The coordination between mitochondrial and nuclear genes is crucial to eukaryotic organisms. Predicting the nature of these epistatic interactions can be difficult because of the transmission asymmetry of the genes involved. While autosomes and X-linked genes are transmitted through both sexes, genes on the Y chromosome and in the mitochondrial genome are uniparentally transmitted through males and females, respectively. Here, we generate 36 otherwise isogenic Drosophila melanogaster strains differing only in the geographical origin of their mitochondrial genome and Y chromosome, to experimentally examine the effects of the uniparentally inherited parts of the genome, as well as their interaction, in males. We assay longevity and gene expression through RNA-sequencing. We detect an important role for both mitochondrial and Y-linked genes, as well as extensive mitochondrial-Y chromosome epistasis. In particular, genes involved in male reproduction appear to be especially sensitive to such interactions, and variation on the Y chromosome is associated with differences in longevity. Despite these interactions, we find no evidence that the mitochondrial genome and Y chromosome are co-adapted within a geographical region. Overall, our study demonstrates a key role for the uniparentally inherited parts of the genome for male biology, but also that mito-nuclear interactions are complex and not easily predicted from simple transmission asymmetries.

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“…MtDNA populations are dynamic, and fluctuations in the proportion of mtDNA variants are common throughout the lifetime of individuals because of unequal partitioning of mtDNA molecules during cell division (vegetative segregation), random sampling of mtDNA molecules for replication (relaxed replication), and/or fission/fusion events among mitochondria ( Stewart and Chinnery 2015 ; Aryaman, Johnston, et al. 2019 ; Ghiselli and Milani 2020 ; Heine and Hood 2020 ). In addition to neutral processes such as random genetic drift ( Jenuth et al.…”

Section: Introductionmentioning

confidence: 99%

A Naturally Heteroplasmic Clam Provides Clues about the Effects of Genetic Bottleneck on Paternal mtDNA

Iannello

Bettinazzi

Breton

et al. 2021

Genome Biology and Evolution

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Mitochondrial DNA (mtDNA) is present in multiple copies within an organism. Since these copies are not identical, a single individual carries a heterogeneous population of mtDNAs, a condition known as heteroplasmy. Several factors play a role in the dynamics of the within-organism mtDNA population: among them genetic bottlenecks, selection, and strictly maternal inheritance are known to shape the levels of heteroplasmy across mtDNAs. In Metazoa, the only evolutionarily stable exception to the strictly maternal inheritance of mitochondria is the doubly uniparental inheritance (DUI), reported in 100+ bivalve species. In DUI species there are two highly divergent mtDNA lineages, one inherited through oocyte mitochondria (F-type) and the other through sperm mitochondria (M-type). Having both parents contributing to the mtDNA pool of the progeny makes DUI a unique system to study the dynamics of mtDNA populations. Since in bivalves the spermatozoon has few mitochondria (4-5), M-type mtDNA faces a tight bottleneck during embryo segregation, one of the narrowest mitochondrial bottlenecks investigated so far. Here, we analyzed the F- and M-type mtDNA variability within individuals of the DUI species Ruditapes philippinarum, and we investigated for the first time the effects of such a narrow bottleneck affecting mtDNA populations. As a potential consequence of this narrow bottleneck, the M-type mtDNA shows a large variability in different tissues, a condition so pronounced that it leads to genotypes from different tissues of the same individual not to cluster together. We believe such results may help understanding the effect of low population size on mtDNA bottleneck.

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Linking the mitochondrial genotype to phenotype: a complex endeavour

Cited by 30 publications

References 48 publications

Mitochondrial-nuclear coadaptation revealed through mtDNA replacements in Saccharomyces cerevisiae

Mitochondrial-nuclear coadaptation revealed through mtDNA replacements in Saccharomyces cerevisiae

Mitochondrial-Y chromosome epistasis inDrosophila melanogaster

A Naturally Heteroplasmic Clam Provides Clues about the Effects of Genetic Bottleneck on Paternal mtDNA

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