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Sophie Breton - One of the best experts on this subject based on the ideXlab platform.
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An Unusual Evolutionary Strategy: The Origins, Genetic Repertoire, and Implications of Doubly Uniparental Inheritance of Mitochondrial DNA in Bivalves
Evolutionary Biology—A Transdisciplinary Approach, 2020Co-Authors: Donald T. Stewart, Sophie Breton, Brent M. Robicheau, Eric Pante, Stefano Bettinazzi, Emily E. Chase, Noor Youssef, Manuel A. Garrido-ramosAbstract:Mitochondrial DNA (mtDNA) is typically passed on to progeny only by the female parent. The phenomenon of “doubly Uniparental Inheritance” (DUI) of mtDNA in many bivalve species is a fascinating exception to the paradigm of strict maternal Inheritance of mtDNA. In this review, we survey the current state of knowledge of DUI and discuss several active areas of research in this field. Topics/questions covered include: the number of times DUI evolved (once or multiple origins), the link between DUI and sex determination, the role(s) of mtDNA-encoded non-oxidative phosphorylation genes (i.e. ORFan/orf genes) in freshwater mussels, the function of conserved sequence motifs and sperm transmission elements in mtDNA of marine mussels, the challenges of annotating mtDNA genomes of DUI species, the presence of unorthodox features in venerid mtDNA, whether or not orf DNA sequences are useful in species-level identification of freshwater mussel, and finally, whether or not there are obvious benefits of DUI. For each topic, we also highlight important avenues for future research within this fascinating field of mitochondrial evolutionary biology.
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Unorthodox features in two venerid bivalves with doubly Uniparental Inheritance of mitochondria.
Scientific Reports, 2020Co-Authors: Charlotte Capt, Donald T. Stewart, Karim Bouvet, Davide Guerra, Brent M. Robicheau, Eric Pante, Sophie BretonAbstract:In animals, strictly maternal Inheritance (SMI) of mitochondria is the rule, but one exception (doubly Uniparental Inheritance or DUI), marked by the transmission of sex-specific mitogenomes, has been reported in bivalves. Associated with DUI is a frequent modification of the mitochondrial cox2 gene, as well as additional sex-specific mitochondrial genes not involved in oxidative phosphorylation. With the exception of freshwater mussels (for 3 families of the order Unionida), these DUI-associated features have only been shown in few species [within Mytilidae (order Mytilida) and Veneridae (order Venerida)] because of the few complete sex-specific mitogenomes published for these orders. Here, we present the complete sex-specific mtDNAs of two recently-discovered DUI species in two families of the order Venerida, Scrobicularia plana (Semelidae) and Limecola balthica (Tellinidae). These species display the largest differences in genome size between sex-specific mitotypes in DUI species (>10 kb), as well as the highest mtDNA divergences (sometimes reaching >50%). An important in-frame insertion (>3.5 kb) in the male cox2 gene is partly responsible for the differences in genome size. The S. plana cox2 gene is the largest reported so far in the Kingdom Animalia. The mitogenomes may be carrying sex-specific genes, indicating that general mitochondrial features are shared among DUI species.
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Unorthodox features in two venerid bivalves with doubly Uniparental Inheritance of mitochondria
Scientific Reports, 2020Co-Authors: Charlotte Capt, Karim Bouvet, Davide Guerra, Brent M. Robicheau, Eric Pante, Donald Stewart, Sophie BretonAbstract:in animals, strictly maternal Inheritance (SMi) of mitochondria is the rule, but one exception (doubly Uniparental Inheritance or DUI), marked by the transmission of sex-specific mitogenomes, has been reported in bivalves. Associated with DUI is a frequent modification of the mitochondrial cox2 gene, as well as additional sex-specific mitochondrial genes not involved in oxidative phosphorylation. With the exception of freshwater mussels (for 3 families of the order Unionida), these DUI-associated features have only been shown in few species [within Mytilidae (order Mytilida) and Veneridae (order Venerida)] because of the few complete sex-specific mitogenomes published for these orders. Here, we present the complete sex-specific mtDNAs of two recently-discovered DUI species in two families of the order Venerida, Scrobicularia plana (Semelidae) and Limecola balthica (tellinidae). these species display the largest differences in genome size between sex-specific mitotypes in DUI species (>10 kb), as well as the highest mtDNA divergences (sometimes reaching >50%). An important in-frame insertion (>3.5 kb) in the male cox2 gene is partly responsible for the differences in genome size. The S. plana cox2 gene is the largest reported so far in the Kingdom Animalia. The mitogenomes may be carrying sex-specific genes, indicating that general mitochondrial features are shared among DUI species. Animal mitochondrial DNA (mtDNA) is typically depicted as a strictly maternally inherited (SMI) circular DNA molecule that is relatively small (~16 kb) and genomically streamlined with almost invariant gene content (13 protein-coding genes and 24 structural RNAs) 1,2. However, important deviations do occur in the mtD-NAs of bivalve molluscs, which not only display dramatic variation in size (67 kb) 3,4 and gene arrangement 5 , but also the presence of additional protein-coding genes not associated with oxidative phospho-rylation 6-9. An even more extreme departure from the norm in bivalve mitochondrial genomes is their mode of doubly Uniparental Inheritance (DUI)-both egg and sperm mitochondria are transmitted from generation to generation in several bivalve species, but only male offspring retain paternally-transmitted mitochondria (with male or M mtDNA) in their gametes 10-12. Adult females of DUI-exhibiting species usually possess only the female-transmitted mtDNA (F mtDNA) in their soma and gametes whereas males possess F mtDNA in their soma and M mtDNA in their gametes 10-13. The DNA divergence between F and M mtDNAs usually vary from about 8% to 40% depending on the species 12,14. Genetic analyses suggested that both F and M mtDNAs in DUI bivalves evolve at a faster rate than typical metazoan mtDNA, and that M mtDNA evolves faster than F mtDNA 15-17. One factor explaining this observation may be that the M genome is subject to weaker selective pressures than the F genome due to an unequal "division of labor" in the DUI system 16. Typical animal mtDNA functions in gonads and somatic tissues of both sexes whereas under DUI, F mtDNA functions in female gonads and the soma of both sexes, while M mtDNAs functions primarily in spermatozoa of male gonads and only partially in the male soma 13,16,18. As opposed to SMI that promotes homoplasmy, a state in which all mtDNA copies are typically genetically identical in each cell, thus preventing potentially harmful genomic conflicts, DUI is a naturally heter-oplasmic system in which two highly divergent mitochondrial lineages coexist in the same nuclear background, enabling the analysis of the consequences of tissue heteroplamy 13 .
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Metabolic remodelling associated with mtDNA: insights into the adaptive value of doubly Uniparental Inheritance of mitochondria.
Proceedings of the Royal Society B: Biological Sciences, 2019Co-Authors: Stefano Bettinazzi, Liliana Milani, Pierre U. Blier, Enrique Rodríguez, Sophie BretonAbstract: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.
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The complete male-type mitochondrial genomes of the Fatmucket, Lampsilis siliquoidea, and the endangered Arkansas Fatmucket, Lampsilis powellii
Mitochondrial DNA Part B, 2018Co-Authors: E. E. Chase, Donald T. Stewart, Walter R. Hoeh, Brent M. Robicheau, John L. Harris, Sophie BretonAbstract:Doubly Uniparental Inheritance (DUI) is a unique mode of mitochondrial (mt) Inheritance found only in some bivalve molluscs. Under DUI, both maternal (i.e. female-transmitted or F-type) and paterna...
Marco Passamonti - One of the best experts on this subject based on the ideXlab platform.
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Pursuing the quest for better understanding the taxonomic distribution of the system of doubly Uniparental Inheritance of mtDNA
PeerJ, 2016Co-Authors: Arthur Gusman, Marco Passamonti, Donald T. Stewart, Sophia Lecomte, Sophie BretonAbstract:There is only one exception to strict maternal Inheritance of mitochondrial DNA (mtDNA) in the animal kingdom: a system named doubly Uniparental Inheritance (DUI), which is found in several bivalve species. Why and how such a radically different system of mitochondrial transmission evolved in bivalve remains obscure. Obtaining a more complete taxonomic distribution of DUI in the Bivalvia may help to better understand its origin and function. In this study we provide evidence for the presence of sex-linked heteroplasmy (thus the possible presence of DUI) in two bivalve species, i.e., the nuculanoid Yoldia hyperborea(Gould, 1841)and the veneroid Scrobicularia plana(Da Costa,1778), increasing the number of families in which DUI has been found by two. An update on the taxonomic distribution of DUI in the Bivalvia is also presented.
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Early replication dynamics of sex-linked mitochondrial DNAs in the doubly Uniparental Inheritance species Ruditapes philippinarum (Bivalvia Veneridae)
Heredity, 2016Co-Authors: D Guerra, Fabrizio Ghiselli, L Milani, S Breton, Marco PassamontiAbstract:Mitochondrial homoplasmy, which is maintained by strictly maternal Inheritance and a series of bottlenecks, is thought to be an adaptive condition for metazoans. Doubly Uniparental Inheritance (DUI) is a unique mode of mitochondrial transmission found in bivalve species, in which two distinct mitochondrial genome (mtDNA) lines are present, one inherited through eggs (F) and one through sperm (M). During development, the two lines segregate in a sex- and tissue-specific manner: females lose M during embryogenesis, whereas males actively segregate it in the germ line. These two pivotal events are still poorly characterized. Here we investigated mtDNA replication dynamics during embryogenesis and pre-adulthood of the venerid Ruditapes philippinarum using real-time quantitative PCR. We found that both mtDNAs do not detectably replicate during early embryogenesis, and that the M line might be lost from females around 24 h of age. A rise in mtDNA copy number was observed before the first reproductive season in both sexes, with the M mitochondrial genome replicating more than the F in males, and we associate these boosts to the early phase of gonad production. As evidence indicates that DUI relies on the same molecular machine of mitochondrial maternal Inheritance that is common in most animals, our data are relevant not only to DUI but also to shed light on how differential segregations of mtDNA variants, in the same nuclear background, may be controlled during development.
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The quest for Doubly Uniparental Inheritance in heterodont bivalves and its detection in Meretrix lamarckii (Veneridae: Meretricinae)
Journal of Zoological Systematics and Evolutionary Research, 2014Co-Authors: Federico Plazzi, Antonello Cassano, Marco PassamontiAbstract:Doubly Uniparental Inheritance (DUI) is possibly the most striking exception to the well-known maternal Inheritance of mitochondria. It poses several stimulating questions concerning among others the function of these organelles, sex determination, embryonic development, and evolutionary consequences. At present, DUI has been found in few species of bivalve molluscs, but more research is necessary to obtain a clearer picture of its distribution within the group, a picture that is mandatory to make any reasonable inference about its origin and evolutionary meaning. The debate about a single evolutionary origin of DUI versus multiple origins is still open. In this manuscript, we investigated seven species of heterodont bivalves and provide evidence for the presence of DUI in the venerid Meretrix lamarckii.
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A comparative analysis of mitochondrial ORFans: new clues on their origin and role in species with doubly Uniparental Inheritance of mitochondria.
Genome Biology and Evolution, 2013Co-Authors: Liliana Milani, Fabrizio Ghiselli, Sophie Breton, Davide Guerra, Marco PassamontiAbstract:Despite numerous comparative mitochondrial genomics studies revealing that animal mitochondrial genomes are highly conserved in terms of gene content, supplementary genes are sometimes found, often arising from gene duplication. Mitochondrial ORFans (ORFs having no detectable homology and unknown function) were found in bivalve molluscs with Doubly Uniparental Inheritance (DUI) of mitochondria. In DUI animals, two mitochondrial lineages are present: one transmitted through females (F-type) and the other through males (M-type), each showing a specific and conserved ORF. The analysis of 34 mitochondrial major Unassigned Regions of Musculista senhousia F- and M-mtDNA allowed us to verify the presence of novel mitochondrial ORFs in this species and to compare them with ORFs from other species with ascertained DUI, with other bivalves and with animals showing new mitochondrial elements. Overall, 17 ORFans from nine species were analyzed for structure and function. Many clues suggest that the analyzed ORFans arose from endogenization of viral genes. The co-option of such novel genes by viral hosts may have determined some evolutionary aspects of host life cycle, possibly involving mitochondria. The structure similarity of DUI ORFans within evolutionary lineages may also indicate that they originated from independent events. If these novel ORFs are in some way linked to DUI establishment, a multiple origin of DUI has to be considered. These putative proteins may have a role in the maintenance of sperm mitochondria during embryo development, possibly masking them from the degradation processes that normally affect sperm mitochondria in species with strictly maternal Inheritance.
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Sex-Linked Mitochondrial Behavior During Early Embryo Development in Ruditapes philippinarum (Bivalvia Veneridae) a Species with the Doubly Uniparental Inheritance (DUI) of Mitochondria
Journal of Experimental Zoology Part B: Molecular and Developmental Evolution, 2012Co-Authors: Liliana Milani, Fabrizio Ghiselli, Marco PassamontiAbstract:In most metazoans mitochondria are inherited maternally. However, in some bivalve molluscs, two mitochondrial lineages are present: one transmitted through females (F-type), the other through males (M-type). This unique system is called Doubly Uniparental Inheritance (DUI) of mitochondria. In DUI species, M-type mitochondria have to invade the germ line of male embryos during development, otherwise sperm would transmit F-type mtDNA and DUI would fail. The mechanisms by which sperm mitochondria enter the germ line are still unknown. To address this question, we traced the movement of spermatozoon mitochondria (M-type) in embryos of the DUI species Ruditapes philippinarum by fertilizing eggs with sperm stained with the mitochondrial-specific vital dye MitoTracker Green. As in Mytilus DUI species, in R. philippinarum the distribution of sperm mitochondria follows two different patterns: an aggregated one in which these organelles locate near the first cleavage furrow, and a dispersed one in which sperm mitochondria are scattered. The presence of the two mitochondrial patterns in these taxa, together with their absence in species with Strictly Maternal Inheritance (SMI), confirms that their occurrence is related to DUI. Moreover, a Real-Time qPCR analysis showed that neither M-type nor F-type mitochondria undergo replication boosts in the earliest embryo development. This is the first study on sex-linked mtDNA copy number carried out by qPCR analysis on embryos of a DUI species and the first time the segregation patterns of sperm mitochondria are described in a DUI system other than Mytilus. J. Exp. Zool. (Mol. Dev. Evol.) 318:182–189, 2012. © 2012 Wiley Periodicals, Inc.
Fabrizio Ghiselli - One of the best experts on this subject based on the ideXlab platform.
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mitochondrial activity in gametes and Uniparental Inheritance a comment on what can we infer about the origin of sex in early eukaryotes
Philosophical Transactions of the Royal Society B, 2018Co-Authors: Fabrizio Ghiselli, Sophie Breton, Liliana MilaniAbstract:In his insightful article, Speijer [1] discussed the origin of sex under multiple points of view, providing a comprehensive and balanced overview of different theories and hypotheses. However, we think that the section ‘Higher mutational loads in one gamete type and retention of Uniparental mitochondrial Inheritance’ (§9) needs some clarification. Speijer [1] elaborates on the correlation between gamete metabolic and physiological differences and their organellar contribution across generations. Specifically, he quotes the ‘division of labour’ hypothesis, which postulates that male gametes maximize energy production for motility by sacrificing mitochondrial DNA (mtDNA) to oxidative phosphorylation (OXPHOS) and its mutagenic by-products, while non-motile female gametes repress OXPHOS, thus being somewhat inactive [2]. Basically, we clarify two discussion points: (i) the exceptions to the strictly maternal Inheritance (SMI) of mitochondria and (ii) the claim that mtDNA is highly mutated in sperm and the supposed causal relationship between such damage and OXPHOS. Exceptions to SMI by which bioenergetically active mitochondria are stably inherited through generations might represent a challenge for the division of labour hypothesis. Doubly Uniparental Inheritance (DUI) is the only known evolutionarily stable exception to the SMI typical of Metazoa. In DUI animals (approx. 100 species of gonochoric bivalve molluscs identified so far [3]), two mitochondrial lineages are inherited, one through eggs (F-type) and the other through sperm (M-type). Eggs are homoplasmic for the F-type, while spermatozoa are homoplasmic for the M-type. These ‘mother-to-daughter’ and ‘father-to-son’ mitochondrial lineages have evolved independently for millions of years (e.g. more than 200 Myr in unionids), accumulating up to 40% of DNA sequence divergence. Since eggs do not transmit the M-type, germ line mitochondria of DUI males are apportioned from the four/five mitochondria of the fertilizing spermatozoon, which carry mtDNA that must be functional and successfully inherited [ …
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Deciphering the Link between Doubly Uniparental Inheritance of mtDNA and Sex Determination in Bivalves: Clues from Comparative Transcriptomics.
Genome Biology and Evolution, 2018Co-Authors: Charlotte Capt, Fabrizio Ghiselli, Liliana Milani, Donald T. Stewart, Sébastien Renaut, Nathan A. Johnson, Bernard E. Sietman, Sophie BretonAbstract:Bivalves exhibit an astonishing diversity of sexual systems and sex-determining mechanisms. They can be gonochoric, hermaphroditic or androgenetic, with both genetic and environmental factors known to determine or influence sex. One unique sex-determining system involving the mitochondrial genome has also been hypothesized to exist in bivalves with doubly Uniparental Inheritance (DUI) of mtDNA. However, the link between DUI and sex determination remains obscure. In this study, we performed a comparative gonad transcriptomics analysis for two DUI-possessing freshwater mussel species to better understand the mechanisms underlying sex determination and DUI in these bivalves. We used a BLAST reciprocal analysis to identify orthologs between Venustaconcha ellipsiformis and Utterbackia peninsularis and compared our results with previously published sex-specific bivalve transcriptomes to identify conserved sex-determining genes. We also compared our data with other DUI species to identify candidate genes possibly involved in the regulation of DUI. A total of ∼12,000 orthologous relationships were found, with 2,583 genes differentially expressed in both species. Among these genes, key sex-determining factors previously reported in vertebrates and in bivalves (e.g., Sry, Dmrt1, Foxl2) were identified, suggesting that some steps of the sex-determination pathway may be deeply conserved in metazoans. Our results also support the hypothesis that a modified ubiquitination mechanism could be responsible for the retention of the paternal mtDNA in male bivalves, and revealed that DNA methylation could also be involved in the regulation of DUI. Globally, our results suggest that sets of genes associated with sex determination and DUI are similar in distantly-related DUI species.
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Mitochondrial activity in gametes and Uniparental Inheritance: a comment on ‘What can we infer about the origin of sex in early eukaryotes?’
Philosophical Transactions of the Royal Society B: Biological Sciences, 2018Co-Authors: Fabrizio Ghiselli, Sophie Breton, Liliana MilaniAbstract:In his insightful article, Speijer [1] discussed the origin of sex under multiple points of view, providing a comprehensive and balanced overview of different theories and hypotheses. However, we think that the section ‘Higher mutational loads in one gamete type and retention of Uniparental mitochondrial Inheritance’ (§9) needs some clarification. Speijer [1] elaborates on the correlation between gamete metabolic and physiological differences and their organellar contribution across generations. Specifically, he quotes the ‘division of labour’ hypothesis, which postulates that male gametes maximize energy production for motility by sacrificing mitochondrial DNA (mtDNA) to oxidative phosphorylation (OXPHOS) and its mutagenic by-products, while non-motile female gametes repress OXPHOS, thus being somewhat inactive [2]. Basically, we clarify two discussion points: (i) the exceptions to the strictly maternal Inheritance (SMI) of mitochondria and (ii) the claim that mtDNA is highly mutated in sperm and the supposed causal relationship between such damage and OXPHOS. Exceptions to SMI by which bioenergetically active mitochondria are stably inherited through generations might represent a challenge for the division of labour hypothesis. Doubly Uniparental Inheritance (DUI) is the only known evolutionarily stable exception to the SMI typical of Metazoa. In DUI animals (approx. 100 species of gonochoric bivalve molluscs identified so far [3]), two mitochondrial lineages are inherited, one through eggs (F-type) and the other through sperm (M-type). Eggs are homoplasmic for the F-type, while spermatozoa are homoplasmic for the M-type. These ‘mother-to-daughter’ and ‘father-to-son’ mitochondrial lineages have evolved independently for millions of years (e.g. more than 200 Myr in unionids), accumulating up to 40% of DNA sequence divergence. Since eggs do not transmit the M-type, germ line mitochondria of DUI males are apportioned from the four/five mitochondria of the fertilizing spermatozoon, which carry mtDNA that must be functional and successfully inherited [ …
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Early replication dynamics of sex-linked mitochondrial DNAs in the doubly Uniparental Inheritance species Ruditapes philippinarum (Bivalvia Veneridae)
Heredity, 2016Co-Authors: D Guerra, Fabrizio Ghiselli, L Milani, S Breton, Marco PassamontiAbstract:Mitochondrial homoplasmy, which is maintained by strictly maternal Inheritance and a series of bottlenecks, is thought to be an adaptive condition for metazoans. Doubly Uniparental Inheritance (DUI) is a unique mode of mitochondrial transmission found in bivalve species, in which two distinct mitochondrial genome (mtDNA) lines are present, one inherited through eggs (F) and one through sperm (M). During development, the two lines segregate in a sex- and tissue-specific manner: females lose M during embryogenesis, whereas males actively segregate it in the germ line. These two pivotal events are still poorly characterized. Here we investigated mtDNA replication dynamics during embryogenesis and pre-adulthood of the venerid Ruditapes philippinarum using real-time quantitative PCR. We found that both mtDNAs do not detectably replicate during early embryogenesis, and that the M line might be lost from females around 24 h of age. A rise in mtDNA copy number was observed before the first reproductive season in both sexes, with the M mitochondrial genome replicating more than the F in males, and we associate these boosts to the early phase of gonad production. As evidence indicates that DUI relies on the same molecular machine of mitochondrial maternal Inheritance that is common in most animals, our data are relevant not only to DUI but also to shed light on how differential segregations of mtDNA variants, in the same nuclear background, may be controlled during development.
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A comparative analysis of mitochondrial ORFans: new clues on their origin and role in species with doubly Uniparental Inheritance of mitochondria.
Genome Biology and Evolution, 2013Co-Authors: Liliana Milani, Fabrizio Ghiselli, Sophie Breton, Davide Guerra, Marco PassamontiAbstract:Despite numerous comparative mitochondrial genomics studies revealing that animal mitochondrial genomes are highly conserved in terms of gene content, supplementary genes are sometimes found, often arising from gene duplication. Mitochondrial ORFans (ORFs having no detectable homology and unknown function) were found in bivalve molluscs with Doubly Uniparental Inheritance (DUI) of mitochondria. In DUI animals, two mitochondrial lineages are present: one transmitted through females (F-type) and the other through males (M-type), each showing a specific and conserved ORF. The analysis of 34 mitochondrial major Unassigned Regions of Musculista senhousia F- and M-mtDNA allowed us to verify the presence of novel mitochondrial ORFs in this species and to compare them with ORFs from other species with ascertained DUI, with other bivalves and with animals showing new mitochondrial elements. Overall, 17 ORFans from nine species were analyzed for structure and function. Many clues suggest that the analyzed ORFans arose from endogenization of viral genes. The co-option of such novel genes by viral hosts may have determined some evolutionary aspects of host life cycle, possibly involving mitochondria. The structure similarity of DUI ORFans within evolutionary lineages may also indicate that they originated from independent events. If these novel ORFs are in some way linked to DUI establishment, a multiple origin of DUI has to be considered. These putative proteins may have a role in the maintenance of sperm mitochondria during embryo development, possibly masking them from the degradation processes that normally affect sperm mitochondria in species with strictly maternal Inheritance.
Eleftherios Zouros - One of the best experts on this subject based on the ideXlab platform.
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Doubly Uniparental Inheritance of mtDNA: An Unappreciated Defiance of a General Rule.
Cellular and Molecular Basis of Mitochondrial Inheritance, 2019Co-Authors: Eleftherios Zouros, George C. RodakisAbstract:We recount the basic observations about doubly Uniparental Inheritance (DUI) of mtDNA in bivalvian mollusks with an emphasis on those that were obtained from work in Mytilus and appeared after the review by Zouros (Evol Biol 40:1–31, 2013). Using this information, we present a new model about DUI that is a revised version of previously suggested models. The model can be summarized as follows. A Mytilus female either provides its eggs with the “masculinizing” factor S and the “sperm mitochondria binding” factor Z, or it does not. This property of the female is determined by two nuclear genes, S and Z, that are always in the on/on or the off/off phase. In fertilized eggs without factors S and Z the embryo develops into a female and the sperm mitochondria are randomly dispersed among cells following development. In fertilized eggs with factors S and Z, the first factor causes the cell to become eventually sperm and the second causes the sperm mitochondria to aggregate and anchor to the nuclear membrane by binding to a specific motif of the sperm-derived mtDNA. Factors S and Z are continuously co-synthesized and co-localized in the cell line from the egg to the sperm. The sperm mitochondria of the aggregate escape the mechanism that eliminates the cell’s mitochondria before the formation of the sperm. The rescued mitochondria are subsequently packed into five mega-mitochondria in the sperm and are delivered in the egg.
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Female‐dependent transmission of paternal mtDNA is a shared feature of bivalve species with doubly Uniparental Inheritance (DUI) of mitochondrial DNA
Journal of Zoological Systematics and Evolutionary Research, 2015Co-Authors: Annie Machordom, Eleftherios Zouros, Rafael Araujo, Carlos Toledo, Emmanuel D. LadoukakisAbstract:Several species from a number of bivalve molluscan families are known to have a paternally transmitted mitochondrial genome, along with the standard maternally transmitted one. The main characteristic of the phenomenon, known as doubly Uniparental Inheritance (DUI), is the coupling of sex and mtDNA Inheritance: males receive both genomes but transmit only the paternal to their progeny; females either do not have the paternal genome or, if they do, they do not transmit it to their progeny. In the families Mytilidae and Veneridae, both of which have DUI, a female individual is either female-biased (it produces only, or nearly so, female progeny), male-biased (it produces mainly male progeny) or non-biased (it produces both genders in intermediate frequencies). Here we present evidence for a same pattern in the freshwater mussel, Unio delphinus (Unionidae). These results suggest that the maternal control of whether a fertilized egg will develop into a male or a female individual (and the associated feature of whether it will inherited or not inherit the paternal mtDNA) is a general characteristic of species with DUI.
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Biparental Inheritance Through Uniparental Transmission: The Doubly Uniparental Inheritance (DUI) of Mitochondrial DNA
Evolutionary Biology, 2013Co-Authors: Eleftherios ZourosAbstract:Many bivalvian mollusks have a sperm-transmitted mitochondrial genome (M), along with the standard egg-transmitted one (F). The phenomenon, known as doubly Uniparental Inheritance (DUI) of mtDNA, is the only known case in which biparental Inheritance of a cytoplasmic genome is the rule rather than the exception. In the mussel Mytilus sperm mitochondria disperse randomly among blastomeres in female embryos, but form an aggregate and stay in the same blastomere in male embryos. In adults, somatic tissues of both sexes are dominated by the F genome. Sperm contains only the M genome and eggs the F (and perhaps traces of M). A female produces mostly daughters, mostly sons, or both sexes in about equal numbers, irrespective of its mate. Thus maleness and M mtDNA fate are tightly linked and under maternal control. Hybridization and triploidization affect the former but not the latter, which suggests that the two are not causally linked. Gene content and arrangement are the same in conspecific F and M genomes, but primary sequence has diverged from 20 % to 40 %, depending on species. The two genomes differ at the control region (CR). Synonymous substitutions accumulate faster in the M than the F genome and non-synonymous even faster. Expression studies indicate that the M genome is active only at spermatogenesis. These observations suggest that the M genome is under a more relaxed selective constraint than the F. Some mytilid species carry, in low frequencies, sperm-transmitted mtDNAs whose primary sequence is of the F type and the CR is an F/M mosaic (“masculinized” genomes). In venerids sperm mitochondria behavior, M genome fate and sex determination are as in mytilids. In unionids the M genome also evolves faster than the F and F/M sequence divergence reaches 50 %. The identification of F-specific and M-specific open reading frames in non-coding regions of unionids and mytilids, in conjunction with the CR’s mosaic structure of masculinized genomes, suggest that the mitochondrial genomes of species with DUI carry sequences that affect their transmission route. A model that incorporates these findings is presented in this review.
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Biparental Inheritance Through Uniparental Transmission: The Doubly Uniparental Inheritance (DUI) of Mitochondrial DNA
Evolutionary Biology, 2013Co-Authors: Eleftherios ZourosAbstract:Many bivalvian mollusks have a sperm-transmitted mitochondrial genome (M), along with the standard egg-transmitted one (F). The phenomenon, known as doubly Uniparental Inheritance (DUI) of mtDNA, is the only known case in which biparental Inheritance of a cytoplasmic genome is the rule rather than the exception. In the mussel Mytilus sperm mitochondria disperse randomly among blastomeres in female embryos, but form an aggregate and stay in the same blastomere in male embryos. In adults, somatic tissues of both sexes are dominated by the F genome. Sperm contains only the M genome and eggs the F (and perhaps traces of M). A female produces mostly daughters, mostly sons, or both sexes in about equal numbers, irrespective of its mate. Thus maleness and M mtDNA fate are tightly linked and under maternal control. Hybridization and triploidization affect the former but not the latter, which suggests that the two are not causally linked. Gene content and arrangement are the same in conspecific F and M genomes, but primary sequence has diverged from 20 % to 40 %, depending on species. The two genomes differ at the control region (CR). Synonymous substitutions accumulate faster in the M than the F genome and non-synonymous even faster. Expression studies indicate that the M genome is active only at spermatogenesis. These observations suggest that the M genome is under a more relaxed selective constraint than the F. Some mytilid species carry, in low frequencies, sperm-transmitted mtDNAs whose primary sequence is of the F type and the CR is an F/M mosaic (“masculinized” genomes). In venerids sperm mitochondria behavior, M genome fate and sex determination are as in mytilids. In unionids the M genome also evolves faster than the F and F/M sequence divergence reaches 50 %. The identification of F-specific and M-specific open reading frames in non-coding regions of unionids and mytilids, in conjunction with the CR’s mosaic structure of masculinized genomes, suggest that the mitochondrial genomes of species with DUI carry sequences that affect their transmission route. A model that incorporates these findings is presented in this review.
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Doubly Uniparental Inheritance (DUI) of mitochondrial DNA in Donax trunculus (Bivalvia: Donacidae) and the problem of its sporadic detection in Bivalvia.
Evolution, 2008Co-Authors: Ioannis Theologidis, Stilianos Fodelianakis, Miguel B. Gaspar, Eleftherios ZourosAbstract:Mitochondrial DNA is transmitted maternally in metazoan species. This rule does not hold in several species of bivalves that have two mtDNA types, one that is transmitted maternally and the other paternally. This system of mitochondrial DNA transmission is known as doubly Uniparental Inheritance (DUI). Here we present evidence of DUI in the clam Donax trunculus making Donacidae the sixth bivalve family in which the phenomenon has been found. In addition, we present the taxonomic affiliation of all species in which DUI is currently known to occur and construct a phylogeny of the maternal and paternal genomes of these species. We use this information to address the question of a single or multiple origins of DUI and to discuss whether failed attempts to demonstrate the presence of DUI in several bivalve species might be due to problems of detection or to genuine absence of the phenomenon.
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Metabolic remodelling associated with mtDNA: insights into the adaptive value of doubly Uniparental Inheritance of mitochondria.
Proceedings of the Royal Society B: Biological Sciences, 2019Co-Authors: Stefano Bettinazzi, Liliana Milani, Pierre U. Blier, Enrique Rodríguez, Sophie BretonAbstract: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.
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mitochondrial activity in gametes and Uniparental Inheritance a comment on what can we infer about the origin of sex in early eukaryotes
Philosophical Transactions of the Royal Society B, 2018Co-Authors: Fabrizio Ghiselli, Sophie Breton, Liliana MilaniAbstract:In his insightful article, Speijer [1] discussed the origin of sex under multiple points of view, providing a comprehensive and balanced overview of different theories and hypotheses. However, we think that the section ‘Higher mutational loads in one gamete type and retention of Uniparental mitochondrial Inheritance’ (§9) needs some clarification. Speijer [1] elaborates on the correlation between gamete metabolic and physiological differences and their organellar contribution across generations. Specifically, he quotes the ‘division of labour’ hypothesis, which postulates that male gametes maximize energy production for motility by sacrificing mitochondrial DNA (mtDNA) to oxidative phosphorylation (OXPHOS) and its mutagenic by-products, while non-motile female gametes repress OXPHOS, thus being somewhat inactive [2]. Basically, we clarify two discussion points: (i) the exceptions to the strictly maternal Inheritance (SMI) of mitochondria and (ii) the claim that mtDNA is highly mutated in sperm and the supposed causal relationship between such damage and OXPHOS. Exceptions to SMI by which bioenergetically active mitochondria are stably inherited through generations might represent a challenge for the division of labour hypothesis. Doubly Uniparental Inheritance (DUI) is the only known evolutionarily stable exception to the SMI typical of Metazoa. In DUI animals (approx. 100 species of gonochoric bivalve molluscs identified so far [3]), two mitochondrial lineages are inherited, one through eggs (F-type) and the other through sperm (M-type). Eggs are homoplasmic for the F-type, while spermatozoa are homoplasmic for the M-type. These ‘mother-to-daughter’ and ‘father-to-son’ mitochondrial lineages have evolved independently for millions of years (e.g. more than 200 Myr in unionids), accumulating up to 40% of DNA sequence divergence. Since eggs do not transmit the M-type, germ line mitochondria of DUI males are apportioned from the four/five mitochondria of the fertilizing spermatozoon, which carry mtDNA that must be functional and successfully inherited [ …
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Deciphering the Link between Doubly Uniparental Inheritance of mtDNA and Sex Determination in Bivalves: Clues from Comparative Transcriptomics.
Genome Biology and Evolution, 2018Co-Authors: Charlotte Capt, Fabrizio Ghiselli, Liliana Milani, Donald T. Stewart, Sébastien Renaut, Nathan A. Johnson, Bernard E. Sietman, Sophie BretonAbstract:Bivalves exhibit an astonishing diversity of sexual systems and sex-determining mechanisms. They can be gonochoric, hermaphroditic or androgenetic, with both genetic and environmental factors known to determine or influence sex. One unique sex-determining system involving the mitochondrial genome has also been hypothesized to exist in bivalves with doubly Uniparental Inheritance (DUI) of mtDNA. However, the link between DUI and sex determination remains obscure. In this study, we performed a comparative gonad transcriptomics analysis for two DUI-possessing freshwater mussel species to better understand the mechanisms underlying sex determination and DUI in these bivalves. We used a BLAST reciprocal analysis to identify orthologs between Venustaconcha ellipsiformis and Utterbackia peninsularis and compared our results with previously published sex-specific bivalve transcriptomes to identify conserved sex-determining genes. We also compared our data with other DUI species to identify candidate genes possibly involved in the regulation of DUI. A total of ∼12,000 orthologous relationships were found, with 2,583 genes differentially expressed in both species. Among these genes, key sex-determining factors previously reported in vertebrates and in bivalves (e.g., Sry, Dmrt1, Foxl2) were identified, suggesting that some steps of the sex-determination pathway may be deeply conserved in metazoans. Our results also support the hypothesis that a modified ubiquitination mechanism could be responsible for the retention of the paternal mtDNA in male bivalves, and revealed that DNA methylation could also be involved in the regulation of DUI. Globally, our results suggest that sets of genes associated with sex determination and DUI are similar in distantly-related DUI species.
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Mitochondrial activity in gametes and Uniparental Inheritance: a comment on ‘What can we infer about the origin of sex in early eukaryotes?’
Philosophical Transactions of the Royal Society B: Biological Sciences, 2018Co-Authors: Fabrizio Ghiselli, Sophie Breton, Liliana MilaniAbstract:In his insightful article, Speijer [1] discussed the origin of sex under multiple points of view, providing a comprehensive and balanced overview of different theories and hypotheses. However, we think that the section ‘Higher mutational loads in one gamete type and retention of Uniparental mitochondrial Inheritance’ (§9) needs some clarification. Speijer [1] elaborates on the correlation between gamete metabolic and physiological differences and their organellar contribution across generations. Specifically, he quotes the ‘division of labour’ hypothesis, which postulates that male gametes maximize energy production for motility by sacrificing mitochondrial DNA (mtDNA) to oxidative phosphorylation (OXPHOS) and its mutagenic by-products, while non-motile female gametes repress OXPHOS, thus being somewhat inactive [2]. Basically, we clarify two discussion points: (i) the exceptions to the strictly maternal Inheritance (SMI) of mitochondria and (ii) the claim that mtDNA is highly mutated in sperm and the supposed causal relationship between such damage and OXPHOS. Exceptions to SMI by which bioenergetically active mitochondria are stably inherited through generations might represent a challenge for the division of labour hypothesis. Doubly Uniparental Inheritance (DUI) is the only known evolutionarily stable exception to the SMI typical of Metazoa. In DUI animals (approx. 100 species of gonochoric bivalve molluscs identified so far [3]), two mitochondrial lineages are inherited, one through eggs (F-type) and the other through sperm (M-type). Eggs are homoplasmic for the F-type, while spermatozoa are homoplasmic for the M-type. These ‘mother-to-daughter’ and ‘father-to-son’ mitochondrial lineages have evolved independently for millions of years (e.g. more than 200 Myr in unionids), accumulating up to 40% of DNA sequence divergence. Since eggs do not transmit the M-type, germ line mitochondria of DUI males are apportioned from the four/five mitochondria of the fertilizing spermatozoon, which carry mtDNA that must be functional and successfully inherited [ …
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A comparative analysis of mitochondrial ORFans: new clues on their origin and role in species with doubly Uniparental Inheritance of mitochondria.
Genome Biology and Evolution, 2013Co-Authors: Liliana Milani, Fabrizio Ghiselli, Sophie Breton, Davide Guerra, Marco PassamontiAbstract:Despite numerous comparative mitochondrial genomics studies revealing that animal mitochondrial genomes are highly conserved in terms of gene content, supplementary genes are sometimes found, often arising from gene duplication. Mitochondrial ORFans (ORFs having no detectable homology and unknown function) were found in bivalve molluscs with Doubly Uniparental Inheritance (DUI) of mitochondria. In DUI animals, two mitochondrial lineages are present: one transmitted through females (F-type) and the other through males (M-type), each showing a specific and conserved ORF. The analysis of 34 mitochondrial major Unassigned Regions of Musculista senhousia F- and M-mtDNA allowed us to verify the presence of novel mitochondrial ORFs in this species and to compare them with ORFs from other species with ascertained DUI, with other bivalves and with animals showing new mitochondrial elements. Overall, 17 ORFans from nine species were analyzed for structure and function. Many clues suggest that the analyzed ORFans arose from endogenization of viral genes. The co-option of such novel genes by viral hosts may have determined some evolutionary aspects of host life cycle, possibly involving mitochondria. The structure similarity of DUI ORFans within evolutionary lineages may also indicate that they originated from independent events. If these novel ORFs are in some way linked to DUI establishment, a multiple origin of DUI has to be considered. These putative proteins may have a role in the maintenance of sperm mitochondria during embryo development, possibly masking them from the degradation processes that normally affect sperm mitochondria in species with strictly maternal Inheritance.
