Segregation of sperm mitochondria in two- and four-cell embryos of the blue mussel Mytilus edulis: implications for the mechanism of doubly uniparental inheritance of mitochondrial DNA

Genome ◽  
2006 ◽  
Vol 49 (7) ◽  
pp. 799-807 ◽  
Author(s):  
Andrew T Cogswell ◽  
Ellen L.R Kenchington ◽  
Eleftherios Zouros
Keyword(s):  
Mytilus Edulis ◽  
Blue Mussel ◽  
Mitochondrial Genomes ◽  
Uniparental Inheritance ◽  
Cleavage Furrow ◽  
Doubly Uniparental Inheritance ◽  
Developmental Mechanism ◽  
Sex Ratio Bias ◽  
The Family ◽  
Early Developmental

Species of the family Mytilidae have 2 mitochondrial genomes, one that is transmitted through the egg and one that is transmitted through the sperm. In the Mytilus edulis species complex (M. edulis, M. galloprovincialis, and M. trossulus) there is also a strong mother-dependent sex-ratio bias in favor of one or the other sex among progeny from pair matings. In a previous study, we have shown that sperm mitochondria enter the egg and that their behavior during cell division is different depending on whether the egg originated from a female- or male-biased mother. Specifically, in eggs from females that produce mostly or exclusively daughters, sperm mitochondria disperse randomly among cells after egg division. In eggs from females that produce predominantly sons, sperm mitochondria tend to stay together in the same cell. Here, we extend these observations and show that in 2- and 4-cell embryos from male-biased mothers most sperm mitochondria are located near or at the cleavage furrow of the major cell, in contrast to embryos from female-biased mothers where there is no preferential association of sperm mitochondria with the cleavage furrow. This observation provides evidence for an early developmental mechanism through which sperm mitochondria are preferentially channeled into the primordial cells of male embryos, thus making the paternal mitochondrial genome the dominant mtDNA component of the male germ line.Key words: mussels, doubly uniparental inheritance of mtDNA, sperm mitochondria.

scholarly journals Differential Segregation Patterns of Sperm Mitochondria in Embryos of the Blue Mussel (Mytilus edulis)

Genetics ◽  
2004 ◽  
Vol 166 (2) ◽  
pp. 883-894
Author(s):  
Liqin Cao ◽  
Ellen Kenchington ◽  
Eleftherios Zouros
Keyword(s):  
Mitochondrial Dna ◽  
Mytilus Edulis ◽  
Blue Mussel ◽  
Uniparental Inheritance ◽  
Male Gonad ◽  
Doubly Uniparental Inheritance ◽  
Organelle Genomes ◽  
Somatic Tissues ◽  
Tight Linkage ◽  
Mitotracker Green

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.

scholarly journals Distribution and frequency of mitochondrial DNA polymorphisms in blue mussel (Mytilus edulis) populations of southwestern Nova Scotia (Canada)

2018 ◽  
Vol 96 (6) ◽  
pp. 608-613 ◽  
Author(s):  
Donald T. Stewart ◽  
Marion Sinclair-Waters ◽  
Alexandra Rice ◽  
Ryan A. Bunker ◽  
Brent M. Robicheau ◽  
...  
Keyword(s):  
Nova Scotia ◽  
Mytilus Edulis ◽  
Blue Mussel ◽  
Phylogenetic Analyses ◽  
Role Reversal ◽  
Dna Polymorphisms ◽  
Swimming Velocity ◽  
Uniparental Inheritance ◽  
Doubly Uniparental Inheritance ◽  
Mt Genome

The Atlantic blue mussel (Mytilus edulis Linnaeus, 1758) exhibits doubly uniparental inheritance of mitochondrial (mt) DNA. Females are usually homoplasmic for a female-transmitted mt genome (the F type) and males are heteroplasmic for an F type and a male-transmitted mt genome (the M type). F types can undergo “role-reversal” events, resulting in new male-transmitted mtDNA genomes known as recently masculinized (RM) types that co-occur in populations with evolutionarily older standard-male (SM) types. Phylogenetic analyses have shown that RM types periodically replace SM types. It has also been shown that sperm with RM mtDNA have greater swimming velocity and more efficient components of the electron transport chain compared to sperm with SM mtDNA, thus leading to the hypothesis that RM sperm may have a selective advantage over SM sperm. The present study examines the distribution of RM and SM mitotypes in male M. edulis (n = 225) from 13 localities in southwestern Nova Scotia (Canada). The SM type was more common in all populations, with the proportion of RM types ranging from 0% to 24.1%. The highest proportion of RM types was observed in an aquaculture operation. Analyses of additional populations are required to evaluate the selective pressures affecting the geographic distribution of RM and SM mitotypes in M. edulis.

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 ◽  
1998 ◽  
Vol 41 (6) ◽  
pp. 818-824 ◽  
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.

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

Genetics ◽  
2003 ◽  
Vol 164 (2) ◽  
pp. 603-611 ◽  
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.

Genetics of Mother-Dependent Sex Ratio in Blue Mussels (Mytilus spp.) and Implications for Doubly Uniparental Inheritance of Mitochondrial DNA

Genetics ◽  
2002 ◽  
Vol 161 (4) ◽  
pp. 1579-1588 ◽  
Author(s):  
Ellen Kenchington ◽  
Barry MacDonald ◽  
Liqin Cao ◽  
Defkalion Tsagkarakis ◽  
Eleftherios Zouros
Keyword(s):  
Mitochondrial Dna ◽  
Sex Ratio ◽  
Female Parent ◽  
Population Level ◽  
Uniparental Inheritance ◽  
Doubly Uniparental Inheritance ◽  
Ratio Bias ◽  
Sex Ratio Bias ◽  
Mitochondrial Genotype ◽  
Ratio Determination

Abstract Previous studies have shown that in most pair matings of Mytilus edulis, M. trossulus, and M. galloprovincialis there is a large sex-ratio bias in favor of either males or females. The degree of bias is a characteristic property of the female parent, as matings of the same female with different males produce the same sex ratio, but matings of the same male with different females produce different sex ratios. All three species possess the unusual feature of doubly uniparental inheritance of mitochondrial DNA (mtDNA); i.e., they contain two distinct types of mtDNA, one that is transmitted matrilinearly and one that is transmitted patrilinearly. This coupling of sex and mtDNA transmission raises the possibility that the mechanism of sex-ratio determination in mussels might be under the control of the mtDNA of the female parent. Here we present data from pedigreed crosses that confirm the previous observations that in mussel matings there is a strong sex-ratio bias and that the bias is under the control of the female parent. In addition, these data strongly suggest that this control is exercised by the mother's nuclear rather than mitochondrial genotype. Making use of these findings we develop a model of mother-dependent sex determination and use data from crosses involving wild females to test the model's predictions at the population level.

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

PeerJ ◽  
2018 ◽  
Vol 6 ◽  
pp. e5593 ◽  
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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