The extremely divergent maternally- and paternally-transmitted mitochondrial genomes are co-expressed in somatic tissues of two freshwater mussel species with doubly uniparental inheritance of mtDNA

Abstract In Mytilus, females carry predominantly maternal mitochondrial DNA (mtDNA) but males carry maternal mtDNA in their somatic tissues and paternal mtDNA in their gonads. This phenomenon, known as doubly uniparental inheritance (DUI) of mtDNA, presents a major departure from the uniparental transmission of organelle genomes. Eggs of Mytilus edulis from females that produce exclusively daughters and from females that produce mostly sons were fertilized with sperm stained with MitoTracker Green FM, allowing observation of sperm mitochondria in the embryo by epifluorescent and confocal microscopy. In embryos from females that produce only daughters, sperm mitochondria are randomly dispersed among blastomeres. In embryos from females that produce mostly sons, sperm mitochondria tend to aggregate and end up in one blastomere in the two- and four-cell stages. We postulate that the aggregate eventually ends up in the first germ cells, thus accounting for the presence of paternal mtDNA in the male gonad. This is the first evidence for different behaviors of sperm mitochondria in developing embryos that may explain the tight linkage between gender and inheritance of paternal mitochondrial DNA in species with DUI.

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Doubly Uniparental Inheritance: Two Mitochondrial Genomes, One Precious Model for Organelle DNA Inheritance and Evolution

DNA and Cell Biology ◽

10.1089/dna.2008.0807 ◽

2009 ◽

Vol 28 (2) ◽

pp. 79-89 ◽

Cited By ~ 81

Author(s):

Marco Passamonti ◽

Fabrizio Ghiselli

Keyword(s):

Mitochondrial Genomes ◽

Uniparental Inheritance ◽

Doubly Uniparental Inheritance ◽

Organelle Dna

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The distribution of male-transmitted and female-transmitted mitochondrial DNA types in somatic tissues of blue mussels: Implications for the operation of doubly uniparental inheritance of mitochondrial DNA

Genome ◽

10.1139/g98-081 ◽

1998 ◽

Vol 41 (6) ◽

pp. 818-824 ◽

Cited By ~ 74

Author(s):

Manuel A Garrido-Ramos ◽

Donald T Stewart ◽

Brent W Sutherland ◽

Eleftherios Zouros

Keyword(s):

Mitochondrial Dna ◽

Blue Mussel ◽

Uniparental Inheritance ◽

Doubly Uniparental Inheritance ◽

Dominant Type ◽

Blue Mussels ◽

Somatic Tissues ◽

Dna Types ◽

M Genome

We have examined the mitochondrial DNA (mtDNA) content of several somatic tissues from male and female individuals of the blue mussel, Mytilus edulis. As expected from the mode of doubly uniparental inheritance (DUI) of mtDNA that is characteristic of this genus, the dominant type of mtDNA in male gonads was the male-transmitted M type. In contrast, all male somatic tissues were dominated by the female-transmitted F type. The M type could occasionally be detected in one or another tissue of a few female individuals. The findings have several implications for the operation of doubly uniparental inheritance of mitochondrial DNA, among which the most important are (i) the M genome does not have an unconditional replicative advantage over the F genome, and (ii) in contrast to "masculinization" (the process by which an F molecule assumes the role of the M genome) "feminization" (the process by which an M molecule assumes the role of the F genome) might be a rare but not impossible phenomenon.Key words: mitochondrial DNA inheritance, mitochondrial DNA tissue distribution, blue mussels, gender-specific mtDNA, doubly uniparental inheritance of mtDNA, Mytilus.

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Presence of male mitochondria in somatic tissues and their functional importance at the whole animal level in the marine bivalve Arctica islandica

Communications Biology ◽

10.1038/s42003-021-02593-1 ◽

2021 ◽

Vol 4 (1) ◽

Author(s):

Cyril Dégletagne ◽

Doris Abele ◽

Gernot Glöckner ◽

Benjamin Alric ◽

Heike Gruber ◽

...

Keyword(s):

Mitochondrial Genes ◽

Marine Bivalve ◽

Uniparental Inheritance ◽

Natural Occurrence ◽

Doubly Uniparental Inheritance ◽

Arctica Islandica ◽

Sharp Drop ◽

Respiratory Capacity ◽

Icelandic Population ◽

Somatic Tissues

AbstractMetazoans normally possess a single lineage of mitochondria inherited from the mother (♀-type mitochondria) while paternal mitochondria are absent or eliminated in fertilized eggs. In doubly uniparental inheritance (DUI), which is specific to the bivalve clade including the ocean quahog, Arctica islandica, ♂-type mitochondria are retained in male gonads and, in a few species, small proportions of ♂-type mitochondria co-exist with ♀-type in somatic tissues. To the best of our knowledge, we report, for the first time in metazoan, the natural occurrence of male and female individuals with exclusively ♂-type mitochondria in somatic tissues of the bivalve A. islandica. Mitochondrial genomes differ by ~5.5% at DNA sequence level. Exclusive presence of ♂-type mitochondria affects mitochondrial complexes partially encoded by mitochondrial genes and leads to a sharp drop in respiratory capacity. Through a combination of whole mitochondrial genome sequencing and molecular assays (gene presence and expression), we demonstrate that 1) 11% of individuals of an Icelandic population appear homoplasmic for ♂-type mitochondria in somatic tissues, 2) ♂-type mitochondrial genes are transcribed and 3) individuals with ♂-type mitochondria in somatic cells lose 30% of their wild-type respiratory capacity. This mitochondrial pattern in A. islandica is a special case of DUI, highlighted in individuals from both sexes with functional consequences at cellular and conceivably whole animal level.

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Molecular Evolution and Recombination in Gender-Associated Mitochondrial DNAs of the Manila Clam Tapes philippinarum

Genetics ◽

10.1093/genetics/164.2.603 ◽

2003 ◽

Vol 164 (2) ◽

pp. 603-611 ◽

Cited By ~ 1

Author(s):

Marco Passamonti ◽

Jeffrey L Boore ◽

Valerio Scali

Keyword(s):

Mitochondrial Dna ◽

Molecular Evolution ◽

Single Gene ◽

Mitochondrial Genomes ◽

Uniparental Inheritance ◽

Doubly Uniparental Inheritance ◽

Tapes Philippinarum ◽

Mitochondrial Dnas ◽

History Of ◽

Mitochondrial Dna Heteroplasmy

Abstract Doubly uniparental inheritance (DUI) provides an intriguing system for addressing aspects of molecular evolution and intermolecular recombination of mitochondrial DNA. For this reason, a large sequence analysis has been performed on Tapes philippinarum (Bivalvia, Veneridae), which has mitochondrial DNA heteroplasmy that is consistent with a DUI. The sequences of a 9.2-kb region (containing 29 genes) from 9 individuals and the sequences of a single gene from another 44 individuals are analyzed. Comparisons suggest that the two sex-related mitochondrial genomes do not experience a neutral pattern of divergence and that selection may act with varying strength on different genes. This pattern of evolution may be related to the long, separate history of M and F genomes within their tissue-specific “arenas.” Moreover, our data suggest that recombinants, although occurring in soma, may seldom be transmitted to progeny in T. philippinarum.

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Variability of mitochondrial ORFans hints at possible differences in the system of doubly uniparental inheritance of mitochondria among families of freshwater mussels (Bivalvia: Unionida)

BMC Evolutionary Biology ◽

10.1186/s12862-019-1554-5 ◽

2019 ◽

Vol 19 (1) ◽

Cited By ~ 1

Author(s):

Davide Guerra ◽

Manuel Lopes-Lima ◽

Elsa Froufe ◽

Han Ming Gan ◽

Paz Ondina ◽

...

Keyword(s):

Freshwater Mussels ◽

Complete Mitochondrial Genome ◽

Physiological Role ◽

Freshwater Mussel ◽

Single Species ◽

Open Reading Frames ◽

Uniparental Inheritance ◽

Doubly Uniparental Inheritance ◽

Sexual Systems ◽

Mitogenome Sequence

Abstract Background Supernumerary ORFan genes (i.e., open reading frames without obvious homology to other genes) are present in the mitochondrial genomes of gonochoric freshwater mussels (Bivalvia: Unionida) showing doubly uniparental inheritance (DUI) of mitochondria. DUI is a system in which distinct female-transmitted and male-transmitted mitotypes coexist in a single species. In families Unionidae and Margaritiferidae, the transition from dioecy to hermaphroditism and the loss of DUI appear to be linked, and this event seems to affect the integrity of the ORFan genes. These observations led to the hypothesis that the ORFans have a role in DUI and/or sex determination. Complete mitochondrial genome sequences are however scarce for most families of freshwater mussels, therefore hindering a clear localization of DUI in the various lineages and a comprehensive understanding of the influence of the ORFans on DUI and sexual systems. Therefore, we sequenced and characterized eleven new mitogenomes from poorly sampled freshwater mussel families to gather information on the evolution and variability of the ORFan genes and their protein products. Results We obtained ten complete plus one almost complete mitogenome sequence from ten representative species (gonochoric and hermaphroditic) of families Margaritiferidae, Hyriidae, Mulleriidae, and Iridinidae. ORFan genes are present only in DUI species from Margaritiferidae and Hyriidae, while non-DUI species from Hyriidae, Iridinidae, and Mulleriidae lack them completely, independently of their sexual system. Comparisons among the proteins translated from the newly characterized ORFans and already known ones provide evidence of conserved structures, as well as family-specific features. Conclusions The ORFan proteins show a comparable organization of secondary structures among different families of freshwater mussels, which supports a conserved physiological role, but also have distinctive family-specific features. Given this latter observation and the fact that the ORFans can be either highly mutated or completely absent in species that secondarily lost DUI depending on their respective family, we hypothesize that some aspects of the connection among ORFans, sexual systems, and DUI may differ in the various lineages of unionids.

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A high-quality reference genome for a parasitic bivalve with doubly uniparental inheritance (Bivalvia: Unionida)

Genome Biology and Evolution ◽

10.1093/gbe/evab029 ◽

2021 ◽

Author(s):

Chase H Smith

Keyword(s):

Single Molecule ◽

Reference Genome ◽

Economic Value ◽

Freshwater Mussel ◽

Uniparental Inheritance ◽

Doubly Uniparental Inheritance ◽

High Quality ◽

Long Reads ◽

A Genome ◽

Genomic Studies

Abstract From a genomics perspective, bivalves (Mollusca: Bivalvia) have been poorly explored with the exception for those of high economic value. The bivalve order Unionida, or freshwater mussels, has been of interest in recent genomic studies due to their unique mitochondrial biology and peculiar life cycle. However, genomic studies have been hindered by the lack of a high-quality reference genome. Here, I present a genome assembly of Potamilus streckersoni using Pacific Bioscience single-molecule real-time long reads and 10X Genomics linked read sequencing. Further, I use RNA sequencing from multiple tissue types and life stages to annotate the reference genome. The final assembly was far superior to any previously published freshwater mussel genome and was represented by 2,368 scaffolds (2,472 contigs) and 1,776,755,624 bp, with a scaffold N50 of 2,051,244 bp. A high proportion of the assembly was comprised of repetitive elements (51.03%), aligning with genomic characteristics of other bivalves. The functional annotation returned 52,407 gene models (41,065 protein, 11,342 tRNAs), which was concordant with the estimated number of genes in other freshwater mussel species. This genetic resource, along with future studies developing high-quality genome assemblies and annotations, will be integral toward unraveling the genomic bases of ecologically and evolutionarily important traits in this hyper-diverse group.

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Mitogenomics of Perumytilus purpuratus (Bivalvia: Mytilidae) and its implications for doubly uniparental inheritance of mitochondria

PeerJ ◽

10.7717/peerj.5593 ◽

2018 ◽

Vol 6 ◽

pp. e5593 ◽

Cited By ~ 4

Author(s):

Beata Śmietanka ◽

Marek Lubośny ◽

Aleksandra Przyłucka ◽

Karin Gérard ◽

Artur Burzyński

Keyword(s):

Purifying Selection ◽

Mitochondrial Genomes ◽

Uniparental Inheritance ◽

Maternal Lineage ◽

Doubly Uniparental Inheritance ◽

Reading Frame ◽

Musculista Senhousia ◽

Perumytilus Purpuratus ◽

First Time ◽

Complete Mitochondrial Genomes

Animal mitochondria are usually inherited through the maternal lineage. The exceptional system allowing fathers to transmit their mitochondria to the offspring exists in some bivalves. Its taxonomic spread is poorly understood and new mitogenomic data are needed to fill the gap. Here, we present for the first time the two divergent mitogenomes from Chilean mussel Perumytilus purpuratus. The existence of these sex-specific mitogenomes confirms that this species has the doubly uniparental inheritance (DUI) of mitochondria. The genetic distance between the two mitochondrial lineages in P. purpuratus is not only much bigger than in the Mytilus edulis species complex but also greater than the distance observed in Musculista senhousia, the only other DUI-positive member of the Mytilidae family for which both complete mitochondrial genomes were published to date. One additional, long ORF (open reading frame) is present exclusively in the maternal mitogenome of P. purpuratus. This ORF evolves under purifying selection, and will likely be a target for future DUI research.

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Tissue-specific expression of male-transmitted mitochondrial DNA and its implications for rates of molecular evolution in Mytilus mussels (Bivalvia: Mytilidae)

Genome ◽

10.1139/g01-159 ◽

2002 ◽

Vol 45 (2) ◽

pp. 348-355 ◽

Cited By ~ 50

Author(s):

Anne C Dalziel ◽

Donald T Stewart

Keyword(s):

Mitochondrial Dna ◽

Molecular Evolution ◽

Uniparental Inheritance ◽

Rt Pcr ◽

Male Gonad ◽

Doubly Uniparental Inheritance ◽

Specific Expression ◽

Somatic Tissues ◽

Selective Forces ◽

Rates Of Molecular Evolution

Mytilus and other bivalves exhibit an unusual system of mitochondrial DNA (mtDNA) transmission termed doubly uniparental inheritance (DUI). Specifically, males transmit the mtDNA they have received from their fathers to their sons. Females transmit their mother's mtDNA to both sons and daughters. Males are normally heteroplasmic and females are normally homoplasmic, but not exclusively. This system is associated with an unusual pattern of molecular evolution. Male-transmitted mtDNA (M type) evolves faster than female-transmitted (F type) mtDNA. Relatively relaxed selection on the M type has been proposed as an explanation for this phenomenon. To further evaluate the selective forces acting upon the M-type genome, we used RT-PCR to determine where it is expressed. M-type mtDNA expression was detected in all gonad samples and in 50% of somatic tissues of males, and in a single female tissue. F-type mtDNA expression was detected in all female tissues, all male somatic tissues, and all but one male gonad sample. We argue that the expression of M-type mtDNA in male somatic and male gonad tissues has implications for the strength of selection acting upon it.Key words: gender-associated mitochondrial DNA, doubly uniparental inheritance of mtDNA, Mytilus edulis, molecular evolution.

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