Evidence for a Fourteenth mtDNA-Encoded Protein in the Female-Transmitted mtDNA of Marine Mussels (Bivalvia: Mytilidae)

Breton, Sophie; Ghiselli, Fabrizio; Passamonti, Marco; Milani, Liliana; Stewart, Donald T.; Hoeh, Walter R.

doi:10.1371/journal.pone.0019365

Cited by 54 publications

(50 citation statements)

References 108 publications

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“…In DUI bivalves, females inherit F-type mtDNA, whereas males inherit both F- and M-types (Skibinski et al 1994a, 1994b; Zouros et al 1994a, 1994b). In DUI bivalves (orders Mytiloida, Unionoida, and Veneroida), two novel lineage-specific ORFs were found, one in the F-mtDNA (fORF) and one in the M-mtDNA (mORF) (Breton et al 2009; Breton et al 2011a, 2011b; Ghiselli et al 2013). These novel ORFs have been hypothesized to be responsible for the different mode of mtDNA transmission and the maintenance of gonochorism in DUI bivalves (Breton et al 2009, 2011a, 2011b).…”

Section: Introductionmentioning

confidence: 99%

“…In all the analyzed DUI Mytilus species, the novel fORF is localized in the Largest Unassigned Region (LUR) and encodes a putative protein of more than 100 amino acids (aa), suggesting its maintenance in the subfamily Mytilinae for more than 10 million years (Breton et al 2011b). A fORF is present also in the F-mtDNA of Musculista senhousia , a DUI mytilid of the subfamily Crenellinae (Breton et al 2011b).…”

Section: Introductionmentioning

confidence: 99%

“…A fORF is present also in the F-mtDNA of Musculista senhousia , a DUI mytilid of the subfamily Crenellinae (Breton et al 2011b). In the venerid R. philippinarum , the fORF is localized in the Female Largest Unassigned Region (FLUR), whereas the mORF in the Male Unassigned Region 21 (Ghiselli et al 2013).…”

Section: Introductionmentioning

confidence: 99%

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A Comparative Analysis of Mitochondrial ORFans: New Clues on Their Origin and Role in Species with Doubly Uniparental Inheritance of Mitochondria

Milani

Ghiselli

Guerra

et al. 2013

Genome Biology and Evolution

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128

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Despite numerous comparative mitochondrial genomics studies revealing that animal mitochondrial genomes are highly conserved in terms of gene content, supplementary genes are sometimes found, often arising from gene duplication. Mitochondrial ORFans (ORFs having no detectable homology and unknown function) were found in bivalve molluscs with Doubly Uniparental Inheritance (DUI) of mitochondria. In DUI animals, two mitochondrial lineages are present: one transmitted through females (F-type) and the other through males (M-type), each showing a specific and conserved ORF. The analysis of 34 mitochondrial major Unassigned Regions of Musculista senhousia F- and M-mtDNA allowed us to verify the presence of novel mitochondrial ORFs in this species and to compare them with ORFs from other species with ascertained DUI, with other bivalves and with animals showing new mitochondrial elements. Overall, 17 ORFans from nine species were analyzed for structure and function. Many clues suggest that the analyzed ORFans arose from endogenization of viral genes. The co-option of such novel genes by viral hosts may have determined some evolutionary aspects of host life cycle, possibly involving mitochondria. The structure similarity of DUI ORFans within evolutionary lineages may also indicate that they originated from independent events. If these novel ORFs are in some way linked to DUI establishment, a multiple origin of DUI has to be considered. These putative proteins may have a role in the maintenance of sperm mitochondria during embryo development, possibly masking them from the degradation processes that normally affect sperm mitochondria in species with strictly maternal inheritance.

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Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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A Comparative Analysis of Mitochondrial ORFans: New Clues on Their Origin and Role in Species with Doubly Uniparental Inheritance of Mitochondria

Milani

Ghiselli

Guerra

et al. 2013

Genome Biology and Evolution

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128

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“…The M-type genome is larger because the protein-coding genes COX2 and M-ORF are also larger. Both haplotypes have the 13 protein-coding genes typically found in metazoan mitochondrial genomes, the gender-specific ORF described for all Unionida mitogenomes with DUI system (Breton et al 2009(Breton et al , 2011, 22 transfer RNA (tRNA), and 2 ribosomal RNA (rRNA) genes. The gene orientation, but not gene order, is the same in both mtDNA haplotypes (genomic details supplied on request).…”

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confidence: 99%

The female and male mitochondrial genomes of Unio delphinus and the phylogeny of freshwater mussels (Bivalvia: Unionida)

Fonseca

Lopes‐Lima

Eackles

et al. 2016

Mitochondrial DNA Part B

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We have sequenced the female and male mtDNA of Unio delphinus and inferred the Unionidae phylogeny using 41 complete mtDNA sequences. Additionally, we compared the concatenated mtDNA trees with those using single or combination of two mtDNA genes to identify the best genes to use in the absence of complete mitogenomes. The gender-specific mtDNAs of U. delphinus contain all Unionida mtDNA specific features. The mtDNA phylogeny supports the reciprocal monophyly of the gender-specific clades but it was inconclusive regarding Unionidae subfamilies relationships. The gene trees topologies using ND5 or 16S-rRNA with ND1 were the closest trees to the mtDNA trees.

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“…The recently described F open reading frame (Breton et al, 2011) is located in the center of the studied region of mtDNA (Figure 2). The presence of a protein coding gene could have an impact on the analyses, as most of them assume that the scored variation is neutral.…”

Section: Phylogeography Of European Mytilus Mitochondria B ś Mietankamentioning

confidence: 99%

Glacial history of the European marine mussels Mytilus, inferred from distribution of mitochondrial DNA lineages

et al. 2014

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Mussels of the genus Mytilus have been used to assess the circumglacial phylogeography of the intertidal zone. These mussels are representative components of the intertidal zone and have rapidly evolving mitochondrial DNA, suitable for high resolution phylogeographic analyses. In Europe, the three Mytilus species currently share mitochondrial haplotypes, owing to the cases of extensive genetic introgression. Genetic diversity of Mytilus edulis, Mytilus trossulus and Mytilus galloprovincialis was studied using a 900-bp long part of the most variable fragment of the control region from one of their two mitochondrial genomes. To this end, 985 specimens were sampled along the European coasts, at sites ranging from the Black Sea to the White Sea. The relevant DNA fragments were amplified, sequenced and analyzed. Contrary to the earlier findings, our coalescence and nested cladistics results show that only a single M. edulis glacial refugium existed in the Atlantic. Despite that, the species survived the glaciation retaining much of its diversity. Unsurprisingly, M. galloprovincialis survived in the Mediterranean Sea. In a relatively short time period, around the climatic optimum at 10 ky ago, the species underwent rapid expansion coupled with population differentiation. Following the expansion, further contemporary gene flow between populations was limited. Heredity (2014) 113, 250-258; doi:10.1038/hdy.2014.23; published online 12 March 2014 INTRODUCTION Sea mussels of the Mytilus edulis species complex, which consists of three subspecies: M. edulis, Mytilus trossulus, and Mytilus galloprovincialis, are widespread in northern and southern hemispheres (Gérard et al., 2008). All three taxa occur in the coastal water ecosystems surrounding Europe (Gosling, 1992). In Europe, M. trossulus prefers lower salinity waters: it has been identified in the Baltic Sea (Väinölä and Hvilsom, 1991), in Norwegian fjords (Ridgway and Naevdal, 2004), in Scotland (Beaumont et al., 2008), and in the Barents Sea (Väinölä and Strelkov, 2011). Single individuals possessing M. trossulus alleles were found in the Netherlands (Śmietanka et al., 2004). M. edulis ranges from the White Sea and the Barents Sea in the north, through the Atlantic coastal waters to southern France in the south. The range of M. galloprovincialis extends from the Azov and the Black Sea to the British Isles. In the areas where two subspecies coexist, hybridization has been observed. Two well-documented hybridization areas between M. edulis and M. trossulus exist in European waters. The first one extends from the Danish Straits into the Baltic Sea up to the Aland Islands, and the second has recently been discovered in Scotland (Beaumont et al., 2008). A strong, unidirectional genetic introgression from M. edulis to M. trossulus has been observed in the Baltic Sea area (Kijewski et al., 2006). The extreme effect is visible at the mitochondrial DNA (mtDNA) level, for the native M. trossulus mtDNA was replaced by M. edulis mitochondrial genome (Rawson and Hilbish, 1998). Wit...

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Evidence for a Fourteenth mtDNA-Encoded Protein in the Female-Transmitted mtDNA of Marine Mussels (Bivalvia: Mytilidae)

Cited by 54 publications

References 108 publications

A Comparative Analysis of Mitochondrial ORFans: New Clues on Their Origin and Role in Species with Doubly Uniparental Inheritance of Mitochondria

A Comparative Analysis of Mitochondrial ORFans: New Clues on Their Origin and Role in Species with Doubly Uniparental Inheritance of Mitochondria

The female and male mitochondrial genomes of Unio delphinus and the phylogeny of freshwater mussels (Bivalvia: Unionida)

Glacial history of the European marine mussels Mytilus, inferred from distribution of mitochondrial DNA lineages

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