Doubly Uniparental Inheritance of Mitochondria As a Model System for Studying Germ Line Formation

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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The inheritance of viable mitochondria

10.7287/peerj.preprints.3122 ◽

2017 ◽

Author(s):

Liliana Milani ◽

Fabrizio Ghiselli

Keyword(s):

Genetic Information ◽

Mitochondrial Membrane ◽

De Novo ◽

Germ Line ◽

Mitochondrial Genomes ◽

Uniparental Inheritance ◽

Oxygen Species ◽

Deleterious Mutations ◽

Mtdna Mutation ◽

Doubly Uniparental Inheritance

Mitochondria cannot be produced de novo by the cell, but are inherited across generations. Their peculiar genetics (multiple genomes per cell, no meiosis, replication independent from cell cycle, high mutation rate) and the possible exposition to Reactive Oxygen Species (ROS) are predicted to produce a fast accumulation of deleterious mutations, a phenomenon known as Müller’s ratchet. Nonetheless, mitochondrial genomes persist accurately over million years. How is a viable mitochondrial genetic information preserved? To answer this question we review the following relevant topics: 1) the sources of mtDNA mutation (replication and ROS); 2) the origin of mitochondrial membrane potential; 3) the activity of germ line mitochondria; 4) the mitochondrial bottleneck; 5) mtDNA drift and selection. Finally we discuss such topics in the light of an unusual biological system (Doubly Uniparental Inheritance of mitochondria, DUI), in which also sperm mtDNA is regularly transmitted to the progeny.

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The inheritance of viable mitochondria

10.7287/peerj.preprints.3122v1 ◽

2017 ◽

Author(s):

Liliana Milani ◽

Fabrizio Ghiselli

Keyword(s):

Genetic Information ◽

Mitochondrial Membrane ◽

De Novo ◽

Germ Line ◽

Mitochondrial Genomes ◽

Uniparental Inheritance ◽

Oxygen Species ◽

Deleterious Mutations ◽

Mtdna Mutation ◽

Doubly Uniparental Inheritance

Mitochondria cannot be produced de novo by the cell, but are inherited across generations. Their peculiar genetics (multiple genomes per cell, no meiosis, replication independent from cell cycle, high mutation rate) and the possible exposition to Reactive Oxygen Species (ROS) are predicted to produce a fast accumulation of deleterious mutations, a phenomenon known as Müller’s ratchet. Nonetheless, mitochondrial genomes persist accurately over million years. How is a viable mitochondrial genetic information preserved? To answer this question we review the following relevant topics: 1) the sources of mtDNA mutation (replication and ROS); 2) the origin of mitochondrial membrane potential; 3) the activity of germ line mitochondria; 4) the mitochondrial bottleneck; 5) mtDNA drift and selection. Finally we discuss such topics in the light of an unusual biological system (Doubly Uniparental Inheritance of mitochondria, DUI), in which also sperm mtDNA is regularly transmitted to the progeny.

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

10.7287/peerj.preprints.3096v1 ◽

2017 ◽

Cited By ~ 1

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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Male-Dependent Doubly Uniparental Inheritance of Mitochondrial DNA and Female-Dependent Sex-Ratio in the Mussel Mytilus galloprovincialis

Genetics ◽

10.1093/genetics/145.4.1073 ◽

1997 ◽

Vol 145 (4) ◽

pp. 1073-1082 ◽

Cited By ~ 9

Author(s):

Carlos Saavedra ◽

María-Isabel Reyero ◽

Eleftherios Zouros

Keyword(s):

Mitochondrial Dna ◽

Sex Ratio ◽

Mytilus Galloprovincialis ◽

Germ Line ◽

Female Parent ◽

Female Gonad ◽

Uniparental Inheritance ◽

Male Gonad ◽

Doubly Uniparental Inheritance ◽

Male Progeny

We have investigated sex ratio and mitochondrial DNA inheritance in pair-matings involving five female and five male individuals of the Mediterranean mussel Mytilus galloprovincialis. The percentage of male progeny varied widely among families and was found to be a characteristic of the female parent and independent of the male to which it was mated. Thus sex-ratio in Mytilus appears to be independent of the nuclear genotype of the sperm. With a few exceptions, doubly uniparental inheritance (DUI) of mtDNA was observed in all families fathered by four of the five males: female and male progeny contained the mother's mtDNA (the F genome), but males contained also the father's paternal mtDNA (the M genome). Two hermaphrodite individuals found among the progeny of these crosses contained the F mitochondrial genome in the female gonad and both the F and M genomes in the male gonad. All four families fathered by the fifth male showed the standard maternal inheritance (SMI) of animal mtDNA: both female and male progeny contained only the maternal mtDNA. These observations illustrate the intimate linkage between sex and mtDNA inheritance in species with DUI and suggest different major roles for each gender. We propose a model according to which development of a male gonad requires the presence in the early germ cells of an agent associated with sperm-derived mitochondria, these mitochondria are endowed with a paternally encoded replicative advantage through which they overcome their original minority in the fertilized egg and this advantage (and, therefore, the chance of an early entrance into the germ line) is countered by a maternally encoded egg factor.

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Differential Segregation Patterns of Sperm Mitochondria in Embryos of the Blue Mussel (Mytilus edulis)

Genetics ◽

10.1093/genetics/166.2.883 ◽

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.

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

Canadian Journal of Zoology ◽

10.1139/cjz-2020-0166 ◽

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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