Doubly Uniparental Inheritance of mtDNA: An Unappreciated Defiance of a General Rule

2019 ◽  
pp. 25-49 ◽  
Author(s):  
Eleftherios Zouros ◽  
George C. Rodakis
Keyword(s):  
General Rule ◽  
Uniparental Inheritance ◽  
Doubly Uniparental Inheritance

scholarly journals Bioenergetic consequences of sex-specific mitochondrial DNA evolution

2021 ◽  
Vol 288 (1957) ◽  
pp. 20211585
Author(s):  
Stefano Bettinazzi ◽  
Liliana Milani ◽  
Pierre U. Blier ◽  
Sophie Breton
Keyword(s):  
Mitochondrial Genome ◽  
Acid Metabolism ◽  
Maternal Inheritance ◽  
Tricarboxylic Acid Cycle ◽  
General Rule ◽  
High Energy ◽  
Uniparental Inheritance ◽  
Doubly Uniparental Inheritance ◽  
Antioxidant Metabolism ◽  
The Impact

Doubly uniparental inheritance (DUI) represents a notable exception to the general rule of strict maternal inheritance (SMI) of mitochondria in metazoans. This system entails the coexistence of two mitochondrial lineages (F- and M-type) transmitted separately through oocytes and sperm, thence providing an unprecedented opportunity for the mitochondrial genome to evolve adaptively for male functions. In this study, we explored the impact of a sex-specific mitochondrial evolution upon gamete bioenergetics of DUI and SMI bivalve species, comparing the activity of key enzymes of glycolysis, fermentation, fatty acid metabolism, tricarboxylic acid cycle, oxidative phosphorylation and antioxidant metabolism. Our findings suggest reorganized bioenergetic pathways in DUI gametes compared to SMI gametes. This generally results in a decreased enzymatic capacity in DUI sperm with respect to DUI oocytes, a limitation especially prominent at the terminus of the electron transport system. This bioenergetic remodelling fits a reproductive strategy that does not require high energy input and could potentially link with the preservation of the paternally transmitted mitochondrial genome in DUI species. Whether this phenotype may derive from positive or relaxed selection acting on DUI sperm is still uncertain.

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.

A proposed method for analyzing molecular signatures to detect hermaphroditism in freshwater mussels: a case study using the Eastern Floater (Pyganodon cataracta)

2021 ◽  
Author(s):  
Donald T. Stewart ◽  
Chloe M. Stephenson ◽  
Ljiljana M. Stanton ◽  
Emily E. Chase ◽  
Brent M. Robicheau ◽  
...  
Keyword(s):  
Freshwater Mussels ◽  
Uniparental Inheritance ◽  
Molecular Signatures ◽  
Doubly Uniparental Inheritance ◽  
Hydrophobic Properties ◽  
Mt Dna ◽  
Reading Frame ◽  
Mt Genome ◽  
Primary Nucleotide Sequence

Many freshwater mussels (Order Unionida) have an unusual system of doubly uniparental inheritance (DUI) of mitochondrial (mt) DNA. In species with DUI, males possess a female-transmitted (F-type) mt genome and a male-transmitted (M-type) mt genome. These genomes contain non-canonical open reading frame (orf) genes referred to as f-orf and m-orf, present in F and M mt genomes, respectively. These genes have been implicated in sexual development in Unionida. When gonochoric species become hermaphroditic, which has happened several times in Unionida, they lose their M-type mt genome, and f-orf genes evolve dramatically. Resulting F-ORF proteins are highly divergent in terms of primary nucleotide sequence, inferred amino acids, and hydrophobic properties; these genes (and proteins) are referred to as hermaphroditic orfs or h-orfs (and H-ORFs). We investigated patterns of hydrophobicity divergence for H-ORF proteins in hermaphrodites versus F-ORF proteins in closely related gonochoric species against cytochrome c oxidase subunit 1 (cox1) divergences. This approach was used to assess whether cryptic hermaphrodites can be detected. Although we did not detect evidence for the recent transition of any populations of Eastern Floaters, Pyganodon cataracta (Say, 1817) to hermaphroditism, our analyses demonstrate that molecular signatures in mtDNA can be used to detect hermaphroditism in freshwater mussels.

scholarly journals Disruption of doubly uniparental inheritance of mitochondrial DNA in hybrid mussels (Mytilus edulis × M. galloprovincialis)

Heredity ◽  
2003 ◽  
Vol 91 (4) ◽  
pp. 354-360 ◽  
Author(s):  
A R Wood ◽  
G Turner ◽  
D O F Skibinski ◽  
A R Beaumont
Keyword(s):  
Mitochondrial Dna ◽  
Mytilus Edulis ◽  
Uniparental Inheritance ◽  
Doubly Uniparental Inheritance

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.

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