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 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.

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.

scholarly journals Pursuing the quest for better understanding the taxonomic distribution of the system of doubly uniparental inheritance of mtDNA

PeerJ ◽  
2016 ◽  
Vol 4 ◽  
pp. e2760 ◽  
Author(s):  
Arthur Gusman ◽  
Sophia Lecomte ◽  
Donald T. Stewart ◽  
Marco Passamonti ◽  
Sophie Breton
Keyword(s):  
Maternal Inheritance ◽  
Uniparental Inheritance ◽  
Bivalve Species ◽  
Animal Kingdom ◽  
Doubly Uniparental Inheritance ◽  
Taxonomic Distribution ◽  
Scrobicularia Plana ◽  
Mitochondrial Transmission ◽  
And Function ◽  
Yoldia Hyperborea

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 nuculanoidYoldia hyperborea(Gould, 1841)and the veneroidScrobicularia 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.

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 Atypical mitochondrial inheritance patterns in eukaryotes

Genome ◽  
2015 ◽  
Vol 58 (10) ◽  
pp. 423-431 ◽  
Author(s):  
Sophie Breton ◽  
Donald T. Stewart
Keyword(s):  
Sex Determination ◽  
Molecular Mechanisms ◽  
Maternal Inheritance ◽  
Uniparental Inheritance ◽  
Mitochondrial Inheritance ◽  
Doubly Uniparental Inheritance ◽  
Inheritance Patterns ◽  
Sexual Systems ◽  
Evolutionary Forces ◽  
Mtdna Inheritance

Mitochondrial DNA (mtDNA) is predominantly maternally inherited in eukaryotes. Diverse molecular mechanisms underlying the phenomenon of strict maternal inheritance (SMI) of mtDNA have been described, but the evolutionary forces responsible for its predominance in eukaryotes remain to be elucidated. Exceptions to SMI have been reported in diverse eukaryotic taxa, leading to the prediction that several distinct molecular mechanisms controlling mtDNA transmission are present among the eukaryotes. We propose that these mechanisms will be better understood by studying the deviations from the predominating pattern of SMI. This minireview summarizes studies on eukaryote species with unusual or rare mitochondrial inheritance patterns, i.e., other than the predominant SMI pattern, such as maternal inheritance of stable heteroplasmy, paternal leakage of mtDNA, biparental and strictly paternal inheritance, and doubly uniparental inheritance of mtDNA. The potential genes and mechanisms involved in controlling mitochondrial inheritance in these organisms are discussed. The linkage between mitochondrial inheritance and sex determination is also discussed, given that the atypical systems of mtDNA inheritance examined in this minireview are frequently found in organisms with uncommon sexual systems such as gynodioecy, monoecy, or andromonoecy. The potential of deviations from SMI for facilitating a better understanding of a number of fundamental questions in biology, such as the evolution of mtDNA inheritance, the coevolution of nuclear and mitochondrial genomes, and, perhaps, the role of mitochondria in sex determination, is considerable.

scholarly journals The draft genome of Ruditapes philippinarum (the Manila clam), a promising model system for mitochondrial biology

2017 ◽  
Author(s):  
Fabrizio Ghiselli ◽  
Aleksey Komissarov ◽  
Liliana Milani ◽  
Joseph P Dunham ◽  
Sophie Breton ◽  
...  
Keyword(s):  
De Novo ◽  
Germ Line ◽  
Draft Genome ◽  
Ruditapes Philippinarum ◽  
Manila Clam ◽  
Uniparental Inheritance ◽  
Mitochondrial Inheritance ◽  
Doubly Uniparental Inheritance ◽  
Illumina Hiseq ◽  
Inheritance System

The Class Bivalvia is a highly successful and ancient group including 20,000+ known species. They represent a good model for studying adaptation (anoxia/hypoxia, salinity, temperature, ...), and they are useful bioindicators for monitoring the concentration of pollutants in the water. They also make up an important source of food all over the world, with a production corresponding to ~20% of the global aquaculture yield. A striking feature of bivalves is the presence of an unusual mitochondrial inheritance system: the Doubly Uniparental Inheritance (DUI), so far detected in ~100 bivalve species. In DUI species, two mitochondrial genomes (mtDNAs) are present: one is transmitted through eggs (F-type), the other through sperm (M-type); the amino acid p-distance between conspecific M and F genomes ranges from 10% to over 50%. DUI provides a unique point of view for studying mitochondrial biology. In DUI systems: i) males are naturally heteroplasmic, with very divergent mtDNAs; ii) it is possible to study mitochondrial inheritance and bottleneck by following germ line mitochondria during development; iii) mitochondria are under selection for male functions. Here we present the draft genome of the DUI species Ruditapes philippinarum (the Manila clam). DNA from a male individual was sequenced with 40x Illumina HiSeq and 30x PacBio RSII. The best de novo assembly was obtained with Canu assembler, with contig N50=76kb (86% complete, 5% fragmented, and 9% missing metazoan orthologs according to BUSCO). Here we report the results of the first analyses and the technical challenges we faced, especially with the de novo assembly.

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