Inheritance of two M type mitochondrial DNA from sperm and unfertilized eggs to offspring in <i>Mytilus galloprovincialis</i>

Obata, Masahiro; Sano, Natsumi; Kawamura, Kazuo; Komaru, Akira

doi:10.1111/j.1440-169x.2007.00930.x

Cited by 28 publications

(25 citation statements)

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“…Under DUI, female bivalves transmit their mitochondria (carrying F mtDNA) to both sons and daughters, as in SMI, but males pass on their mitochondria (via sperm carrying M mtDNA) to only sons (e.g., [11] but see [12]). At the organismal level, male bivalves with DUI are thus heteroplasmic and contain both M and F genomes.…”

Section: Introductionmentioning

confidence: 99%

“…In male somatic tissues, the F genome predominates while in male gonadal tissues, the M genome is predominant [13] and it appears to be the exclusive type in sperm [14]. In females, both somatic and gonadal tissues typically contain the F genome, but the occasional presence of a small amount of the M genome has been demonstrated in somatic tissues and ovaries of some species [12-16]. …”

Section: Introductionmentioning

confidence: 99%

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Mitochondrial phylogenomics of the Bivalvia (Mollusca): searching for the origin and mitogenomic correlates of doubly uniparental inheritance of mtDNA

et al. 2010

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BackgroundDoubly uniparental inheritance (DUI) is an atypical system of animal mtDNA inheritance found only in some bivalves. Under DUI, maternally (F genome) and paternally (M genome) transmitted mtDNAs yield two distinct gender-associated mtDNA lineages. The oldest distinct M and F genomes are found in freshwater mussels (order Unionoida). Comparative analyses of unionoid mitochondrial genomes and a robust phylogenetic framework are necessary to elucidate the origin, function and molecular evolutionary consequences of DUI. Herein, F and M genomes from three unionoid species, Venustaconcha ellipsiformis, Pyganodon grandis and Quadrula quadrula have been sequenced. Comparative genomic analyses were carried out on these six genomes along with two F and one M unionoid genomes from GenBank (F and M genomes of Inversidens japanensis and F genome of Lampsilis ornata).ResultsCompared to their unionoid F counterparts, the M genomes contain some unique features including a novel localization of the trnH gene, an inversion of the atp8-trnD genes and a unique 3'coding extension of the cytochrome c oxidase subunit II gene. One or more of these unique M genome features could be causally associated with paternal transmission. Unionoid bivalves are characterized by extreme intraspecific sequence divergences between gender-associated mtDNAs with an average of 50% for V. ellipsiformis, 50% for I. japanensis, 51% for P. grandis and 52% for Q. quadrula (uncorrected amino acid p-distances). Phylogenetic analyses of 12 protein-coding genes from 29 bivalve and five outgroup mt genomes robustly indicate bivalve monophyly and the following branching order within the autolamellibranch bivalves: ((Pteriomorphia, Veneroida) Unionoida).ConclusionThe basal nature of the Unionoida within the autolamellibranch bivalves and the previously hypothesized single origin of DUI suggest that (1) DUI arose in the ancestral autolamellibranch bivalve lineage and was subsequently lost in multiple descendant lineages and (2) the mitochondrial genome characteristics observed in unionoid bivalves could more closely resemble the DUI ancestral condition. Descriptions and comparisons presented in this paper are fundamental to a more complete understanding regarding the origins and consequences of DUI.

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Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Mitochondrial phylogenomics of the Bivalvia (Mollusca): searching for the origin and mitogenomic correlates of doubly uniparental inheritance of mtDNA

et al. 2010

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“…Specifically, DUI is a “mother-to-daughter” and “father-to-son” mtDNA inheritance system where females transmit their mt genomes (F mtDNA) to both sons and daughters, and males transmit their mt genomes (M mtDNA) to their sons [20]–[23]. Female offspring are typically homoplasmic ( = containing one mt genome) and male offspring are heteroplasmic [21], [23] but see [24], [25]. In marine mussels Mytilus spp., male somatic tissue contains predominantly the mtDNA of the mother (F genome) but male gametes contain exclusively the mtDNA of the father (M genome) [26], [27].…”

Section: Introductionmentioning

confidence: 99%

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

et al. 2011

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BackgroundA novel feature for animal mitochondrial genomes has been recently established: i.e., the presence of additional, lineage-specific, mtDNA-encoded proteins with functional significance. This feature has been observed in freshwater mussels with doubly uniparental inheritance of mtDNA (DUI). The latter unique system of mtDNA transmission, which also exists in some marine mussels and marine clams, is characterized by one mt genome inherited from the female parent (F mtDNA) and one mt genome inherited from the male parent (M mtDNA). In freshwater mussels, the novel mtDNA-encoded proteins have been shown to be mt genome-specific (i.e., one novel protein for F genomes and one novel protein for M genomes). It has been hypothesized that these novel, F- and M-specific, mtDNA-encoded proteins (and/or other F- and/or M-specific mtDNA sequences) could be responsible for the different modes of mtDNA transmission in bivalves but this remains to be demonstrated.Methodology/Principal FindingsWe investigated all complete (or nearly complete) female- and male-transmitted marine mussel mtDNAs previously sequenced for the presence of ORFs that could have functional importance in these bivalves. Our results confirm the presence of a novel F genome-specific mt ORF, of significant length (>100aa) and located in the control region, that most likely has functional significance in marine mussels. The identification of this ORF in five Mytilus species suggests that it has been maintained in the mytilid lineage (subfamily Mytilinae) for ∼13 million years. Furthermore, this ORF likely has a homologue in the F mt genome of Musculista senhousia, a DUI-containing mytilid species in the subfamily Crenellinae. We present evidence supporting the functionality of this F-specific ORF at the transcriptional, amino acid and nucleotide levels.Conclusions/SignificanceOur results offer support for the hypothesis that “novel F genome-specific mitochondrial genes” are involved in key biological functions in bivalve species with DUI.

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“…Second, the inference that these individuals are derived from heteroplasmic eggs indicates that the failure to exclude paternal mtDNA by female embryos does not just lead to the inclusion of M haplotypes into the soma but, at least occasionally, into the germ line as well. Obata et al (2006Obata et al ( , 2007 and Sano et al (2007) have both previously shown heteroplasmic (the presence of both F and M haplotypes) unfertilized Mytilus galloprovincialis-spawned eggs. When fertilizing heteroplasmic eggs in the laboratory, Obata et al (2007) found that the M haplotype in the resulting progeny was consistent with the M type of the sperm.…”

Section: Discussionmentioning

confidence: 97%

“…Obata et al (2006Obata et al ( , 2007 and Sano et al (2007) have both previously shown heteroplasmic (the presence of both F and M haplotypes) unfertilized Mytilus galloprovincialis-spawned eggs. When fertilizing heteroplasmic eggs in the laboratory, Obata et al (2007) found that the M haplotype in the resulting progeny was consistent with the M type of the sperm. They also found 30% (n = 6) of the adult mussels that they used contained 2 M haplotypes and an F haplotype ).…”

Section: Discussionmentioning

confidence: 97%

Ubiquitous heteroplasmy in Mytilus spp. resulting from disruption in doubly uniparental inheritance regulation

Brannock¹,

Roberts²,

Hilbish³

2013

Mar. Ecol. Prog. Ser.

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Species within the marine mussel Mytilus edulis complex (M. edulis, M. galloprovincialis, and M. trossulus) have an unusual form of mitochondrial DNA (mtDNA) inheritance commonly referred to as doubly uniparental inheritance (DUI). With DUI, all progeny inherit mtDNA maternally (F), while male progeny also inherit mtDNA paternally (M) through their father's sperm. Therefore, females are normally homoplasmic for the F mtDNA, and males are heteroplasmic for the F and M mtDNA. In this study, we show that the regulation of DUI in populations of blue mussels in northern Japan is severely disrupted; consequently, the majority of individuals (89%) are heteroplasmic for M and F mtDNA. Disruption of DUI is primarily due to the failure of female embryos to exclude the father's M mtDNA from their somatic and germinal tissues. High proportions of heteroplasmic females have only been reported in Japanese mussel populations thus far. We show that this disruption occurs in both parental species (M. trossulus and M. galloprovincialis) as well as hybrids and is independent of geographic location around Hokkaido, Japan. This finding differs from many previous studies, which have shown that disruption in DUI is confined to hybrid zones. In addition, some individuals were heteroplasmic for M or F mtDNA, indicating that DUI disruption is multigenerational. Triplasmic individuals were 3 times more often female and were mostly confined within the hybrid zones; however, a few individuals were found within M. galloprovincialis parental populations.KEY WORDS: Mytilus galloprovincialis · Mytilus trossulus · Doubly uniparental inheritance · Disruption · Heteroplasmy Resale or republication not permitted without written consent of the publisher Editorial responsibility:

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Inheritance of two M type mitochondrial DNA from sperm and unfertilized eggs to offspring in Mytilus galloprovincialis

Cited by 28 publications

References 27 publications

Mitochondrial phylogenomics of the Bivalvia (Mollusca): searching for the origin and mitogenomic correlates of doubly uniparental inheritance of mtDNA

Mitochondrial phylogenomics of the Bivalvia (Mollusca): searching for the origin and mitogenomic correlates of doubly uniparental inheritance of mtDNA

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

Ubiquitous heteroplasmy in Mytilus spp. resulting from disruption in doubly uniparental inheritance regulation

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