ArticlePhilosophical transactions of the Royal Society of London. Series B, Biological sciences2013
Energy, ageing, fidelity and sex: oocyte mitochondrial DNA as a protected genetic template.
Article in Philosophical transactions of the Royal Society of London. Series B, Biological sciences, 2013. The graph could read no effect estimate from its abstract, so it casts no vote on the map. Cited by 25 papers.
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Who cites it
25 citing papers in PubMed, 58 citations in OpenAlex.
- Mitochondrial DNA Damage and Its Repair Mechanisms in Aging Oocytes.International journal of molecular sciences · 2024Review
- The role of mitochondria in sex- and age-specific gene expression in a species without sex chromosomes.Proceedings of the National Academy of Sciences of the United States of America · 2024Article
- Sperm-Induced CaCells · 2023Review
- The role of mitochondria in sex- and age-specific gene expression in a species without sex chromosomes.bioRxiv : the preprint server for biology · 2023Article
- An Interplay between Epigenetics and Translation in Oocyte Maturation and Embryo Development: Assisted Reproduction Perspective.Biomedicines · 2022Review
- Article
- Bioenergetic consequences of sex-specific mitochondrial DNA evolution.Proceedings. Biological sciences · 2021Article
- The need for high-quality oocyte mitochondria at extreme ploidy dictates mammalian germline development.eLife · 2021Article
- The most abundant maternal lncRNA Sirena1 acts post-transcriptionally and impacts mitochondrial distribution.Nucleic acids research · 2020Article
- Reversible Thiol Oxidation Inhibits the Mitochondrial ATP Synthase inAntioxidants (Basel, Switzerland) · 2020Article
- The deteriorating soma and the indispensable germline: gamete senescence and offspring fitness.Proceedings. Biological sciences · 2019Article
- Mitochondrial Dysfunction in Primary Ovarian Insufficiency.Endocrinology · 2019Review
- Iron Sulfur and Molybdenum Cofactor Enzymes Regulate theFrontiers in physiology · 2018Article
- Our (Mother's) Mitochondria and Our Mind.Perspectives on psychological science : a journal of the Association for Psychological Science · 2018Review
- Darwinism for the Genomic Age: Connecting Mutation to Diversification.Frontiers in genetics · 2017Article
- Selection for Mitochondrial Quality Drives Evolution of the Germline.PLoS biology · 2016Article
- Mitochondria, the Cell Cycle, and the Origin of Sex via a Syncytial Eukaryote Common Ancestor.Genome biology and evolution · 2016Article
- Restoration of normal embryogenesis by mitochondrial supplementation in pig oocytes exhibiting mitochondrial DNA deficiency.Scientific reports · 2016Article
- The evolution of sex: A new hypothesis based on mitochondrial mutational erosion: Mitochondrial mutational erosion in ancestral eukaryotes would favor the evolution of sex, harnessing nuclear recombination to optimize compensatory nuclear coadaptation.BioEssays : news and reviews in molecular, cellular and developmental biology · 2015Article
- Mitochondrial maintenance failure in aging and role of sexual dimorphism.Archives of biochemistry and biophysics · 2015Review
Corrections and comments
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Authors and funding
5 authors at 3 institutions in 1 country.
Funding
No grant is acknowledged in the PubMed record.
Abstract
Oxidative phosphorylation couples ATP synthesis to respiratory electron transport. In eukaryotes, this coupling occurs in mitochondria, which carry DNA. Respiratory electron transport in the presence of molecular oxygen generates free radicals, reactive oxygen species (ROS), which are mutagenic. In animals, mutational damage to mitochondrial DNA therefore accumulates within the lifespan of the individual. Fertilization generally requires motility of one gamete, and motility requires ATP. It has been proposed that oxidative phosphorylation is nevertheless absent in the special case of quiescent, template mitochondria, that these remain sequestered in oocytes and female germ lines and that oocyte mitochondrial DNA is thus protected from damage, but evidence to support that view has hitherto been lacking. Here we show that female gametes of Aurelia aurita, the common jellyfish, do not transcribe mitochondrial DNA, lack electron transport, and produce no free radicals. In contrast, male gametes actively transcribe mitochondrial genes for respiratory chain components and produce ROS. Electron microscopy shows that this functional division of labour between sperm and egg is accompanied by contrasting mitochondrial morphology. We suggest that mitochondrial anisogamy underlies division of any animal species into two sexes with complementary roles in sexual reproduction. We predict that quiescent oocyte mitochondria contain DNA as an unexpressed template that avoids mutational accumulation by being transmitted through the female germ line. The active descendants of oocyte mitochondria perform oxidative phosphorylation in somatic cells and in male gametes of each new generation, and the mutations that they accumulated are not inherited. We propose that the avoidance of ROS-dependent mutation is the evolutionary pressure underlying maternal mitochondrial inheritance and the developmental origin of the female germ line.
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