Heteroplasmy and repeat expansion in the plant-like mitochondrial genome of a bivalve mollusc

Calcino, Andrew; Baranyi, Christian; Wanninger, Andreas

doi:10.1101/2020.09.23.310516

Cited by 6 publications

(9 citation statements)

References 53 publications

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“…It may be that duplicates are lost quickly, perhaps responding to selection favouring the maintenance of cytonuclear stoichiometry [114]. Evaluating these various possibilities will require better population-level sampling, especially with the help of long-read sequencing technologies like PacBio or Oxford Nanopore, which can help resolve tandem duplications [115,116].…”

Section: Genome Architecturementioning

confidence: 99%

Molluscan mitochondrial genomes break the rules

Ghiselli

Gomes‐dos‐Santos

Adema

et al. 2021

Phil. Trans. R. Soc. B

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The first animal mitochondrial genomes to be sequenced were of several vertebrates and model organisms, and the consistency of genomic features found has led to a ‘textbook description’. However, a more broad phylogenetic sampling of complete animal mitochondrial genomes has found many cases where these features do not exist, and the phylum Mollusca is especially replete with these exceptions. The characterization of full mollusc mitogenomes required considerable effort involving challenging molecular biology, but has created an enormous catalogue of surprising deviations from that textbook description, including wide variation in size, radical genome rearrangements, gene duplications and losses, the introduction of novel genes, and a complex system of inheritance dubbed ‘doubly uniparental inheritance’. Here, we review the extraordinary variation in architecture, molecular functioning and intergenerational transmission of molluscan mitochondrial genomes. Such features represent a great potential for the discovery of biological history, processes and functions that are novel for animal mitochondrial genomes. This provides a model system for studying the evolution and the manifold roles that mitochondria play in organismal physiology, and many ways that the study of mitochondrial genomes are useful for phylogeny and population biology. This article is part of the Theo Murphy meeting issue ‘Molluscan genomics: broad insights and future directions for a neglected phylum’.

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Section: Genome Architecturementioning

confidence: 99%

Molluscan mitochondrial genomes break the rules

Ghiselli

Gomes‐dos‐Santos

Adema

et al. 2021

Phil. Trans. R. Soc. B

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“…[ 10 , 110 – 112 ] Genomic rearrangements are thus frequently observed within a species (also among closely-related species) for CMS-inducing genomes versus “fertile” ones. These characteristics, that is, recombination, repeats and rearrangements, have also been reported in bivalve mtDNAs, [ 113 , 114 ] including in DUI species. [ 15 ] Furthermore, genomic rearrangements with novel ORFs or chimeric genes have been observed among closely-related DUI and non-DUI species, [ 21 , 40 , 115 ] as well as within DUI species (e.g., Mytilus ).…”

Section: Similarities Between Cms and Duimentioning

confidence: 65%

Did doubly uniparental inheritance (DUI) of mtDNA originate as a cytoplasmic male sterility (CMS) system?

et al. 2022

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Animal and plant species exhibit an astonishing diversity of sexual systems, including environmental and genetic determinants of sex, with the latter including genetic material in the mitochondrial genome. In several hermaphroditic plants for example, sex is determined by an interaction between mitochondrial cytoplasmic male sterility (CMS) genes and nuclear restorer genes. Specifically, CMS involves aberrant mitochondrial genes that prevent pollen development and specific nuclear genes that restore it, leading to a mixture of female (male‐sterile) and hermaphroditic individuals in the population (gynodioecy). Such a mitochondrial‐nuclear sex determination system is thought to be rare outside plants. Here, we present one possible case of CMS in animals. We hypothesize that the only exception to the strict maternal mtDNA inheritance in animals, the doubly uniparental inheritance (DUI) system in bivalves, might have originated as a mitochondrial‐nuclear sex‐determination system. We document and explore similarities that exist between DUI and CMS, and we propose various ways to test our hypothesis.

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“…While the degradation of the mt-genome is typically slower compared to the nugenome [33,34,44], it is not known the purpose of these mtTR regions [36] or if they degrade at similar rates to coding regions within the mt-genome. We tested samples collected from a previous mesocosm experiment for the detection of these repeat regions after six days of degradation.…”

Section: Discussionmentioning

confidence: 99%

“…Unlike the typical structure of other animal mt-genomes, which are ~14-20 kilobases (kb) in length and homoplasmic, dreissenid mt-genomes appear more similar to many plant mt-genomes, which display frequent gene rearrangements, greatly expanded repetitive regions, encode various open reading frames of unknown function, and can be heteroplasmic [35,36]. Of particular interest for eDNA applications, both dreissenid mussels display largely expanded mt-genomes (ZM: ~67 kb and QM: ~46 kb) composed of long extended tandem repeat regions (three repeat regions totaling >50 kb and seven repeat regions totaling > 30 kb, respectively) [35,36]. These extended regions can be repeated hundreds of times per mt-genome, compared to only a single copy for any of the coding mt-genes (e.g., 16S, COI, or Cyt b).…”

Section: Introductionmentioning

confidence: 99%

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Improving Environmental DNA Sensitivity for Dreissenid Mussels by Targeting Tandem Repeat Regions of the Mitochondrial Genome

Marshall

Vanderploeg

Chaganti

2022

Water

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The recent genetic revolution through the analysis of aquatic environmental DNA (eDNA) has become a powerful tool for improving the detection of rare and/or invasive species. For the majority of eDNA studies, genetic assays are designed to target mitochondrial genes commonly referred to as “barcode” regions. However, unlike the typical structure of an animal mitochondrial genome, those for the invasive zebra and quagga mussels are greatly expanded with large extended tandem repeat regions. These sections of repeated DNA can appear hundreds of times within the genome compared to a single copy for the mitochondrial barcode genes. This higher number of target copies per mitochondrial genome presents an opportunity to increase eDNA assay sensitivity for these species. Therefore, we designed and evaluated new eDNA assays to target the extended repeat sections for both zebra and quagga mussels. These assays lower the limit of detection of genomic DNA by 100-fold for zebra mussels and 10-fold for quagga mussels. Additionally, these newly developed assays provided longer durations of detection during degradation mesocosm experiments and greater sensitivity for eDNA detection from water samples collected across western Lake Erie compared to standard assays targeting mitochondrial genes. This work illustrates how understanding the complete genomic structure of an organism can improve eDNA analysis.

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Heteroplasmy and repeat expansion in the plant-like mitochondrial genome of a bivalve mollusc

Cited by 6 publications

References 53 publications

Molluscan mitochondrial genomes break the rules

Molluscan mitochondrial genomes break the rules

Did doubly uniparental inheritance (DUI) of mtDNA originate as a cytoplasmic male sterility (CMS) system?

Improving Environmental DNA Sensitivity for Dreissenid Mussels by Targeting Tandem Repeat Regions of the Mitochondrial Genome

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