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.

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 Sex Determining Mechanisms in Bivalves

2017 ◽  
Author(s):  
Sophie Breton ◽  
Charlotte Capt ◽  
Davide Guerra ◽  
Donald Stewart
Keyword(s):  
Final Section ◽  
Genetic Factors ◽  
Current Knowledge ◽  
Mitochondrial Genes ◽  
Uniparental Inheritance ◽  
Developmental Pathway ◽  
Doubly Uniparental Inheritance ◽  
Sexual Systems ◽  
Determination System ◽  
Sex Determination System

In this review, we provide an overview of the current knowledge on the different sexual systems and sex determining mechanisms in bivalves, with a focus on the various epigenetic and genetic factors that may be involved. The final section of the review provides recent discoveries on sex-specific mitochondrial genes in bivalves possessing the unconventional system of doubly uniparental inheritance of mitochondria (which is found in several members of the orders Mytiloida, Unionoida, Veneroida and Nuculanoida). The genes involved in this developmental pathway could represent the first sex determination system in animals in which mitochondrially-encoded genes are directly involved.

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 Natural Heteroplasmy and Mitochondrial Inheritance in Bivalve Molluscs

2019 ◽  
Vol 59 (4) ◽  
pp. 1016-1032 ◽  
Author(s):  
Fabrizio Ghiselli ◽  
Maria Gabriella Maurizii ◽  
Arkadiy Reunov ◽  
Helena Ariño-Bassols ◽  
Carmine Cifaldi ◽  
...  
Keyword(s):  
Developmental Stages ◽  
Sequence Divergence ◽  
Ruditapes Philippinarum ◽  
Uniparental Inheritance ◽  
Doubly Uniparental Inheritance ◽  
Germline Development ◽  
High Sequence Divergence ◽  
High Amino Acid ◽  
Somatic Tissues ◽  
First Time

Abstract Heteroplasmy is the presence of more than one type of mitochondrial genome within an individual, a condition commonly reported as unfavorable and affecting mitonuclear interactions. So far, no study has investigated heteroplasmy at protein level, and whether it occurs within tissues, cells, or even organelles. The only known evolutionarily stable and natural heteroplasmic system in Metazoa is the Doubly Uniparental Inheritance (DUI)—reported so far in ∼100 bivalve species—in which two mitochondrial lineages are present: one transmitted through eggs (F-type) and the other through sperm (M-type). Because of such segregation, mitochondrial oxidative phosphorylation proteins reach a high amino acid sequence divergence (up to 52%) between the two lineages in the same species. Natural heteroplasmy coupled with high sequence divergence between F- and M-type proteins provides a unique opportunity to study their expression and assess the level and extent of heteroplasmy. Here, for the first time, we immunolocalized F- and M-type variants of three mitochondrially-encoded proteins in the DUI species Ruditapes philippinarum, in germline and somatic tissues at different developmental stages. We found heteroplasmy at organelle level in undifferentiated germ cells of both sexes, and in male soma, whereas gametes were homoplasmic: eggs for the F-type and sperm for the M-type. Thus, during gametogenesis, only the sex-specific mitochondrial variant is maintained, likely due to a process of meiotic drive. We examine the implications of our results for DUI proposing a revised model, and we discuss interactions of mitochondria with germ plasm and their role in germline development. Molecular and phylogenetic evidence suggests that DUI evolved from the common Strictly Maternal Inheritance, so the two systems likely share the same underlying molecular mechanism, making DUI a useful system for studying mitochondrial biology.

scholarly journals Metabolic remodelling associated with mtDNA: insights into the adaptive value of doubly uniparental inheritance of mitochondria

2019 ◽  
Vol 286 (1896) ◽  
pp. 20182708 ◽  
Author(s):  
Stefano Bettinazzi ◽  
Enrique Rodríguez ◽  
Liliana Milani ◽  
Pierre U. Blier ◽  
Sophie Breton
Keyword(s):  
Maternal Inheritance ◽  
Direct Selection ◽  
Uniparental Inheritance ◽  
Doubly Uniparental Inheritance ◽  
Respiration Rates ◽  
Adaptive Value ◽  
Unique System ◽  
Somatic Tissues ◽  
Nucleotide Divergence ◽  
Strong Control

Mitochondria produce energy through oxidative phosphorylation (OXPHOS), which depends on the expression of both nuclear and mitochondrial DNA (mtDNA). In metazoans, a striking exception from strictly maternal inheritance of mitochondria is doubly uniparental inheritance (DUI). This unique system involves the maintenance of two highly divergent mtDNAs (F- and M-type, 8–40% of nucleotide divergence) associated with gametes, and occasionally coexisting in somatic tissues. To address whether metabolic differences underlie this condition, we characterized the OXPHOS activity of oocytes, spermatozoa, and gills of different species through respirometry. DUI species express different gender-linked mitochondrial phenotypes in gametes and partly in somatic tissues. The M-phenotype is specific to sperm and entails (i) low coupled/uncoupled respiration rates, (ii) a limitation by the phosphorylation system, and (iii) a null excess capacity of the final oxidases, supporting a strong control over the upstream complexes. To our knowledge, this is the first example of a phenotype resulting from direct selection on sperm mitochondria. This metabolic remodelling suggests an adaptive value of mtDNA variations and we propose that bearing sex-linked mitochondria could assure the energetic requirements of different gametes, potentially linking male-energetic adaptation, mitotype preservation and inheritance, as well as resistance to both heteroplasmy and ageing.

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.

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