Mitochondrial genotype modulates mtDNA copy number and organismal phenotype in Drosophila

Salminen, Tiina S.; Oliveira, Marcos T.; Cannino, Giuseppe; Lillsunde, Päivi; Jacobs, Howard T.; Kaguni, Laurie S.

doi:10.1016/j.mito.2017.02.001

Cited by 40 publications

(102 citation statements)

References 55 publications

(60 reference statements)

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“…This advantage is likely the primary driver of the evolution of HGII mtDNA, enabling HGII to outcompete HGI by “selfish” replication at the cytoplasm level (Rand, ). Recent studies suggest that point mutations in the mitogenome may alter mtDNA copy number and mitochondrial abundance (Camus et al, ; Salminen et al, ; Zhu, Ingelmo, & Rand, ). We suspect that the three nonsynonymous changes are probably associated with mtDNA copy number variation.…”

Section: Discussionmentioning

confidence: 99%

Mitochondrial variation in small brown planthoppers linked to multiple traits and probably reflecting a complex evolutionary trajectory

et al. 2019

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While it has been proposed in several taxa that the mitochondrial genome is associated with adaptive evolution to different climatic conditions, making links between mitochondrial haplotypes and organismal phenotypes remains a challenge. Mitonuclear discordance occurs in the small brown planthopper (SBPH), Laodelphax striatellus, with one mitochondrial haplogroup (HGI) more common in the cold climate region of China relative to another form (HGII) despite strong nuclear gene flow, providing a promising model to investigate climatic adaptation of mitochondrial genomes. We hypothesized that cold adaptation through HGI may be involved, and considered mitogenome evolution, population genetic analyses, and bioassays to test this hypothesis. In contrast to our hypothesis, chill‐coma recovery tests and population genetic tests of selection both pointed to HGII being involved in cold adaptation. Phylogenetic analyses revealed that HGII is nested within HGI, and has three nonsynonymous changes in ND2, ND5 and CYTB in comparison to HGI. These molecular changes likely increased mtDNA copy number, cold tolerance and fecundity of SBPH, particularly through a function‐altering amino acid change involving M114T in ND2. Nuclear background also influenced fecundity and chill recovery (i.e., mitonuclear epistasis) and protein modelling indicates possible nuclear interactions for the two nonsynonymous changes in ND2 and CYTB. The high occurrence frequency of HGI in the cold climate region of China remains unexplained, but several possible reasons are discussed. Overall, our study points to a link between mtDNA variation and organismal‐level evolution and suggests a possible role of mitonuclear interactions in maintaining mtDNA diversity.

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Section: Discussionmentioning

confidence: 99%

Mitochondrial variation in small brown planthoppers linked to multiple traits and probably reflecting a complex evolutionary trajectory

et al. 2019

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“…For example, in plants, cytonuclear interactions (interactions involving polymorphisms within the mitochondrial and/or chloroplast genome and those in the nuclear genome) were shown to affect 23 of 28 phenotypes measured in Arabidopsis thaliana, with pervasive effects on traits involved in germination, resource acquisition, phenology, height, fecundity and survival [18], and also on regulation of the metabolome [19]. In bilaterian animals, from flies to mice and humans, genetic polymorphisms that delineate distinct mitochondrial haplotypes have been linked to the expression of traits tied to reproductive success, development and longevity [3,[20][21][22][23][24][25][26].…”

Section: Introductionmentioning

confidence: 99%

Mitochondrial genetic effects on reproductive success: signatures of positive intrasexual, but negative intersexual pleiotropy

Camus

Dowling

2018

Proc. R. Soc. B.

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Theory predicts that maternal inheritance of mitochondria will facilitate the accumulation of mtDNA mutations that are male biased, or even sexually antagonistic, in effect. While there are many reported cases of mtDNA mutations conferring cytoplasmic male sterility in plants, historically it was assumed such mutations would not persist in the streamlined mitochondrial genomes of bilaterian metazoans. Intriguingly, recent cases of mitochondrial variants exerting male biases in effect have come to light in bilaterians. These cases aside, it remains unknown whether the mitochondrial genetic variation affecting phenotypic expression, and in particular reproductive performance, in bilaterians is routinely composed of sex-biased or sex-specific variation. If selection consistently favours mtDNA variants that augment female fitness, but at cost to males, this could shape patterns of pleiotropy and lead to negative intersexual correlations across mtDNA haplotypes. Here, we show that genetic variation across naturally occurring mitochondrial haplotypes affects components of reproductive success in both sexes, in the fruit fly We find that intrasexual correlations across mitochondrial haplotypes, for components of reproductive success, are generally positive, while intersexual correlations are negative. These results accord with theoretical predictions, suggesting that maternal inheritance has led to the fixation of numerous mutations of sexually antagonistic effect.

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“…Mitochondria vary little in structure and function, and they contain genomes of uniform size and gene composition across taxa. However, mitochondria differ in their abundance between cell types and between taxa, and mitochondrial abundance can vary with the energy needs of a cell (Okie, Smith, & Martin‐Cereceda, ), while mitogenome copy number also has been shown to vary with metabolically important traits (e.g., Salminen et al., ). Mitogenomic approaches to species diversity and abundance at the community level therefore may be able to incorporate metabolic rates in the study of biodiversity patterns.…”

Section: Introductionmentioning

confidence: 99%

Shotgun mitogenomics across body size classes in a local assemblage of tropical Diptera: Phylogeny, species diversity and mitochondrial abundance spectrum

2017

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Abstract. Mitochondrial genomes can be assembled readily from shotgun sequenced DNA mixtures of mass-trapped arthropods ('mitochondrial metagenomics'), speeding up the taxonomic characterization. Bulk sequencing was conducted on some 800 individuals of Diptera obtained by canopy-fogging of a single tree in Borneo dominated by small (<1.5 mm) individuals. Specimens were split into five body-size classes for DNA extraction, to equalize read numbers across specimens and to study how body size, a key ecological trait, interacts with species and phylogenetic diversity. Genome assembly produced 304 orthologous Accepted ArticleThis article is protected by copyright. All rights reserved.mitochondrial contigs presumed to each represent a different species. The small-bodied fraction was the by far most species-rich (187 contigs). Identification of contigs was through phylogenetic analysis together with 56 reference mitogenomes, which placed most of the Bornean community into seven clades of small-bodied species, indicating phylogenetic conservation of body size. Mapping of shotgun reads against the mitogenomes showed wide ranges of read abundances within each size class. Ranked read-abundance plots were largely log-linear, indicating a uniformly filled abundance spectrum, especially for smallbodied species. Small-bodied species differed greatly from other size classes in neutral metacommunity parameters, exhibiting greater levels of immigration, besides greater total community size. We suggest that the established uses of mitochondrial metagenomics for analysis of species and phylogenetic diversity can be extended to parameterise recent theories of community ecology and biodiversity, and by focusing on the number mitochondria, rather than individuals, a new theoretical framework for analysis of mitochondrial abundance spectra can be developed that incorporates metabolic activity approximated by the count of mitochondria.

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Mitochondrial genotype modulates mtDNA copy number and organismal phenotype in Drosophila

Cited by 40 publications

References 55 publications

Mitochondrial variation in small brown planthoppers linked to multiple traits and probably reflecting a complex evolutionary trajectory

Mitochondrial variation in small brown planthoppers linked to multiple traits and probably reflecting a complex evolutionary trajectory

Mitochondrial genetic effects on reproductive success: signatures of positive intrasexual, but negative intersexual pleiotropy

Shotgun mitogenomics across body size classes in a local assemblage of tropical Diptera: Phylogeny, species diversity and mitochondrial abundance spectrum

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