scholarly journals The inheritance of viable mitochondria

Author(s):  
Liliana Milani ◽  
Fabrizio Ghiselli

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.

2017 ◽  
Author(s):  
Liliana Milani ◽  
Fabrizio Ghiselli

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.


2017 ◽  
Author(s):  
Fabrizio Ghiselli ◽  
Aleksey Komissarov ◽  
Liliana Milani ◽  
Joseph P Dunham ◽  
Sophie Breton ◽  
...  

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.


Author(s):  
Fabrizio Ghiselli ◽  
Aleksey Komissarov ◽  
Liliana Milani ◽  
Joseph P Dunham ◽  
Sophie Breton ◽  
...  

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.


2018 ◽  
Author(s):  
Sébastien Renaut ◽  
Davide Guerra ◽  
Walter R. Hoeh ◽  
Donald T. Stewart ◽  
Arthur E. Bogan ◽  
...  

AbstractFreshwater mussels (Bivalvia: Unionida) serve an important role as aquatic ecosystem engineers but are one of the most critically imperilled groups of animals. Here, we used a combination of sequencing strategies to assemble and annotate a draft genome of Venustaconcha ellipsiformis, which will serve as a valuable genomic resource given the ecological value and unique “doubly uniparental inheritance” mode of mitochondrial DNA transmission of freshwater mussels. The genome described here was obtained by combining high coverage short reads (65X genome coverage of Illumina paired-end and 11X genome coverage of mate-pairs sequences) with low coverage Pacific Biosciences long reads (0.3X genome coverage). Briefly, the final scaffold assembly accounted for a total size of 1.54Gb (366,926 scaffolds, N50 = 6.5Kb, with 2.3% of “N” nucleotides), representing 86% of the predicted genome size of 1.80Gb, while over one third of the genome (37.5%) consisted of repeated elements and more than 85% of the core eukaryotic genes were recovered. Given the repeated genetic bottlenecks of V. ellipsiformis populations as a result of glaciations events, heterozygosity was also found to be remarkably low (0.6%), in contrast to most other sequenced bivalve species. Finally, we reassembled the full mitochondrial genome and found six polymorphic sites with respect to the previously published reference. This resource opens the way to comparative genomics studies to identify genes related to the unique adaptations of freshwater mussels and their distinctive mitochondrial inheritance mechanism.


Genetics ◽  
2003 ◽  
Vol 164 (2) ◽  
pp. 603-611 ◽  
Author(s):  
Marco Passamonti ◽  
Jeffrey L Boore ◽  
Valerio Scali

Abstract Doubly uniparental inheritance (DUI) provides an intriguing system for addressing aspects of molecular evolution and intermolecular recombination of mitochondrial DNA. For this reason, a large sequence analysis has been performed on Tapes philippinarum (Bivalvia, Veneridae), which has mitochondrial DNA heteroplasmy that is consistent with a DUI. The sequences of a 9.2-kb region (containing 29 genes) from 9 individuals and the sequences of a single gene from another 44 individuals are analyzed. Comparisons suggest that the two sex-related mitochondrial genomes do not experience a neutral pattern of divergence and that selection may act with varying strength on different genes. This pattern of evolution may be related to the long, separate history of M and F genomes within their tissue-specific “arenas.” Moreover, our data suggest that recombinants, although occurring in soma, may seldom be transmitted to progeny in T. philippinarum.


PLoS ONE ◽  
2011 ◽  
Vol 6 (11) ◽  
pp. e28194 ◽  
Author(s):  
Liliana Milani ◽  
Fabrizio Ghiselli ◽  
Maria Gabriella Maurizii ◽  
Marco Passamonti

PeerJ ◽  
2018 ◽  
Vol 6 ◽  
pp. e5593 ◽  
Author(s):  
Beata Śmietanka ◽  
Marek Lubośny ◽  
Aleksandra Przyłucka ◽  
Karin Gérard ◽  
Artur Burzyński

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.


Genome ◽  
2006 ◽  
Vol 49 (7) ◽  
pp. 799-807 ◽  
Author(s):  
Andrew T Cogswell ◽  
Ellen L.R Kenchington ◽  
Eleftherios Zouros

Species of the family Mytilidae have 2 mitochondrial genomes, one that is transmitted through the egg and one that is transmitted through the sperm. In the Mytilus edulis species complex (M. edulis, M. galloprovincialis, and M. trossulus) there is also a strong mother-dependent sex-ratio bias in favor of one or the other sex among progeny from pair matings. In a previous study, we have shown that sperm mitochondria enter the egg and that their behavior during cell division is different depending on whether the egg originated from a female- or male-biased mother. Specifically, in eggs from females that produce mostly or exclusively daughters, sperm mitochondria disperse randomly among cells after egg division. In eggs from females that produce predominantly sons, sperm mitochondria tend to stay together in the same cell. Here, we extend these observations and show that in 2- and 4-cell embryos from male-biased mothers most sperm mitochondria are located near or at the cleavage furrow of the major cell, in contrast to embryos from female-biased mothers where there is no preferential association of sperm mitochondria with the cleavage furrow. This observation provides evidence for an early developmental mechanism through which sperm mitochondria are preferentially channeled into the primordial cells of male embryos, thus making the paternal mitochondrial genome the dominant mtDNA component of the male germ line.Key words: mussels, doubly uniparental inheritance of mtDNA, sperm mitochondria.


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