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 A naturally heteroplasmic clam provides clues about the effects of genetic bottleneck on paternal mtDNA

2021 ◽  
Author(s):  
Mariangela Iannello ◽  
Stefano Bettinazzi ◽  
Sophie Breton ◽  
Fabrizio Ghiselli ◽  
Liliana Milani
Keyword(s):  
Maternal Inheritance ◽  
Ruditapes Philippinarum ◽  
Uniparental Inheritance ◽  
Single Individual ◽  
Doubly Uniparental Inheritance ◽  
Large Variability ◽  
Unique System ◽  
Multiple Copies ◽  
First Time ◽  
Different Tissues

Abstract Mitochondrial DNA (mtDNA) is present in multiple copies within an organism. Since these copies are not identical, a single individual carries a heterogeneous population of mtDNAs, a condition known as heteroplasmy. Several factors play a role in the dynamics of the within-organism mtDNA population: among them genetic bottlenecks, selection, and strictly maternal inheritance are known to shape the levels of heteroplasmy across mtDNAs. In Metazoa, the only evolutionarily stable exception to the strictly maternal inheritance of mitochondria is the doubly uniparental inheritance (DUI), reported in 100+ bivalve species. In DUI species there are two highly divergent mtDNA lineages, one inherited through oocyte mitochondria (F-type) and the other through sperm mitochondria (M-type). Having both parents contributing to the mtDNA pool of the progeny makes DUI a unique system to study the dynamics of mtDNA populations. Since in bivalves the spermatozoon has few mitochondria (4-5), M-type mtDNA faces a tight bottleneck during embryo segregation, one of the narrowest mitochondrial bottlenecks investigated so far. Here, we analyzed the F- and M-type mtDNA variability within individuals of the DUI species Ruditapes philippinarum, and we investigated for the first time the effects of such a narrow bottleneck affecting mtDNA populations. As a potential consequence of this narrow bottleneck, the M-type mtDNA shows a large variability in different tissues, a condition so pronounced that it leads to genotypes from different tissues of the same individual not to cluster together. We believe such results may help understanding the effect of low population size on mtDNA bottleneck.

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 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 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.

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 Molecular Evolution of CatSper in Mammals and Function of Sperm Hyperactivation in Gray Short-Tailed Opossum

Cells ◽  
2021 ◽  
Vol 10 (5) ◽  
pp. 1047
Author(s):  
Jae Yeon Hwang ◽  
Jamie Maziarz ◽  
Günter P. Wagner ◽  
Jean-Ju Chung
Keyword(s):  
Molecular Evolution ◽  
Reproductive Tract ◽  
Sequence Divergence ◽  
Monodelphis Domestica ◽  
Female Reproductive Tract ◽  
Molecular Characteristics ◽  
High Sequence Divergence ◽  
And Function ◽  
Motility Change ◽  
First Time

Males have evolved species-specifical sperm morphology and swimming patterns to adapt to different fertilization environments. In eutherians, only a small fraction of the sperm overcome the diverse obstacles in the female reproductive tract and successfully migrate to the fertilizing site. Sperm arriving at the fertilizing site show hyperactivated motility, a unique motility pattern displaying asymmetric beating of sperm flagella with increased amplitude. This motility change is triggered by Ca2+ influx through the sperm-specific ion channel, CatSper. However, the current understanding of the CatSper function and its molecular regulation is limited in eutherians. Here, we report molecular evolution and conservation of the CatSper channel in the genome throughout eutherians and marsupials. Sequence analyses reveal that CatSper proteins are slowly evolved in marsupials. Using an American marsupial, gray short-tailed opossum (Monodelphis domestica), we demonstrate the expression of CatSper in testes and its function in hyperactivation and unpairing of sperm. We demonstrate that a conserved IQ-like motif in CatSperζ is required for CatSperζ interaction with the pH-tuned Ca2+ sensor, EFCAB9, for regulating CatSper activity. Recombinant opossum EFCAB9 can interact with mouse CatSperζ despite high sequence divergence of CatSperζ among CatSper subunits in therians. Our finding suggests that molecular characteristics and functions of CatSper are evolutionarily conserved in gray short-tailed opossum, unraveling the significance of sperm hyperactivation and fertilization in marsupials for the first time.

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