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

Genome ◽  
2002 ◽  
Vol 45 (2) ◽  
pp. 348-355 ◽  
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.

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.

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.

scholarly journals Male-Dependent Doubly Uniparental Inheritance of Mitochondrial DNA and Female-Dependent Sex-Ratio in the Mussel Mytilus galloprovincialis

Genetics ◽  
1997 ◽  
Vol 145 (4) ◽  
pp. 1073-1082 ◽  
Author(s):  
Carlos Saavedra ◽  
María-Isabel Reyero ◽  
Eleftherios Zouros
Keyword(s):  
Mitochondrial Dna ◽  
Sex Ratio ◽  
Mytilus Galloprovincialis ◽  
Germ Line ◽  
Female Parent ◽  
Female Gonad ◽  
Uniparental Inheritance ◽  
Male Gonad ◽  
Doubly Uniparental Inheritance ◽  
Male Progeny

We have investigated sex ratio and mitochondrial DNA inheritance in pair-matings involving five female and five male individuals of the Mediterranean mussel Mytilus galloprovincialis. The percentage of male progeny varied widely among families and was found to be a characteristic of the female parent and independent of the male to which it was mated. Thus sex-ratio in Mytilus appears to be independent of the nuclear genotype of the sperm. With a few exceptions, doubly uniparental inheritance (DUI) of mtDNA was observed in all families fathered by four of the five males: female and male progeny contained the mother's mtDNA (the F genome), but males contained also the father's paternal mtDNA (the M genome). Two hermaphrodite individuals found among the progeny of these crosses contained the F mitochondrial genome in the female gonad and both the F and M genomes in the male gonad. All four families fathered by the fifth male showed the standard maternal inheritance (SMI) of animal mtDNA: both female and male progeny contained only the maternal mtDNA. These observations illustrate the intimate linkage between sex and mtDNA inheritance in species with DUI and suggest different major roles for each gender. We propose a model according to which development of a male gonad requires the presence in the early germ cells of an agent associated with sperm-derived mitochondria, these mitochondria are endowed with a paternally encoded replicative advantage through which they overcome their original minority in the fertilized egg and this advantage (and, therefore, the chance of an early entrance into the germ line) is countered by a maternally encoded egg factor.

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

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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