Energy, ageing, fidelity and sex: oocyte mitochondrial DNA as a protected genetic template
Energy, ageing, fidelity and sex: oocyte mitochondrial DNA as a protected genetic template
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.
cytoplasmic inheritance, maternal inheritance, Aurelia aurita, mitochondrial genome, oxidative phosphorylation, aging, Weismann barrier
20120263
de Paula, Wilson B.M.
2e943331-0441-4997-8677-f78f193e11a4
Lucas, Cathy H.
521743e3-b250-4c6b-b084-780af697d6bf
Agip, Ahmed-Noor A.
e4783aec-616a-4aad-b55a-5bf49ac62805
Vizcay-Barrena, Gema
22067f58-0d83-4aad-9857-79f5ad2ebab5
Allen, John F.
c2091bd9-b9a5-4af6-8b03-e9784f3a7010
19 July 2013
de Paula, Wilson B.M.
2e943331-0441-4997-8677-f78f193e11a4
Lucas, Cathy H.
521743e3-b250-4c6b-b084-780af697d6bf
Agip, Ahmed-Noor A.
e4783aec-616a-4aad-b55a-5bf49ac62805
Vizcay-Barrena, Gema
22067f58-0d83-4aad-9857-79f5ad2ebab5
Allen, John F.
c2091bd9-b9a5-4af6-8b03-e9784f3a7010
de Paula, Wilson B.M., Lucas, Cathy H., Agip, Ahmed-Noor A., Vizcay-Barrena, Gema and Allen, John F.
(2013)
Energy, ageing, fidelity and sex: oocyte mitochondrial DNA as a protected genetic template.
Philosophical Transactions of The Royal Society B Biological Sciences, 368 (1622), .
(doi:10.1098/rstb.2012.0263).
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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e-pub ahead of print date: 10 June 2013
Published date: 19 July 2013
Keywords:
cytoplasmic inheritance, maternal inheritance, Aurelia aurita, mitochondrial genome, oxidative phosphorylation, aging, Weismann barrier
Organisations:
Ocean Biochemistry & Ecosystems
Identifiers
Local EPrints ID: 353556
URI: http://eprints.soton.ac.uk/id/eprint/353556
ISSN: 0962-8436
PURE UUID: 8d5b6048-8f3e-4796-a59d-1cda0c74199a
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Date deposited: 10 Jun 2013 12:37
Last modified: 15 Mar 2024 02:47
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Author:
Wilson B.M. de Paula
Author:
Ahmed-Noor A. Agip
Author:
Gema Vizcay-Barrena
Author:
John F. Allen
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