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Female and male gamete mitochondria are distinct and complementary in transcription, structure, and genome function

Female and male gamete mitochondria are distinct and complementary in transcription, structure, and genome function
Female and male gamete mitochondria are distinct and complementary in transcription, structure, and genome function
Respiratory electron transport in mitochondria is coupled to ATP synthesis while generating mutagenic oxygen free radicals. Mitochondrial DNA mutation then accumulates with age, and may set a limit to the lifespan of individual, multicellular organisms. Why is this mutation not inherited? Here we demonstrate that female gametes—oocytes—have unusually small and simple mitochondria that are suppressed for DNA transcription, electron transport, and free radical production. By contrast, male gametes—sperm—and somatic cells of both sexes transcribe mitochondrial genes for respiratory electron carriers and produce oxygen free radicals. This germ-line division between mitochondria of sperm and egg is observed in both the vinegar fruitfly and the zebrafish—species spanning a major evolutionary divide within the animal kingdom. We interpret these findings as an evidence that oocyte mitochondria serve primarily as genetic templates, giving rise, irreversibly and in each new generation, to the familiar energy-transducing mitochondria of somatic cells and male gametes. Suppressed mitochondrial metabolism in the female germline may therefore constitute a mechanism for increasing the fidelity of mitochondrial DNA inheritance.
mitochondrial DNA, maternal inheritance, Drosophila melanogaster, Danio rerio, reactive oxygen species, aging
1759-6653
1969-1977
de Paula, Wilson B.M.
2e943331-0441-4997-8677-f78f193e11a4
Agip, Ahmed-Noor A.
e4783aec-616a-4aad-b55a-5bf49ac62805
Missirlis, Fanis
1a548c69-9d6d-4dbb-9e1d-580936fbf00d
Ashworth, Rachel
23a305c4-a4e4-4b53-a196-cb97508d43d1
Vizcay-Barrena, Gemma
96a02690-2499-4d2f-a6db-79f270fa8f20
Lucas, Cathy H.
521743e3-b250-4c6b-b084-780af697d6bf
Allen, John F
3d462241-5150-4cd4-a460-74d731f322c3
de Paula, Wilson B.M.
2e943331-0441-4997-8677-f78f193e11a4
Agip, Ahmed-Noor A.
e4783aec-616a-4aad-b55a-5bf49ac62805
Missirlis, Fanis
1a548c69-9d6d-4dbb-9e1d-580936fbf00d
Ashworth, Rachel
23a305c4-a4e4-4b53-a196-cb97508d43d1
Vizcay-Barrena, Gemma
96a02690-2499-4d2f-a6db-79f270fa8f20
Lucas, Cathy H.
521743e3-b250-4c6b-b084-780af697d6bf
Allen, John F
3d462241-5150-4cd4-a460-74d731f322c3

de Paula, Wilson B.M., Agip, Ahmed-Noor A., Missirlis, Fanis, Ashworth, Rachel, Vizcay-Barrena, Gemma, Lucas, Cathy H. and Allen, John F (2013) Female and male gamete mitochondria are distinct and complementary in transcription, structure, and genome function. Genome Biology and Evolution, 5 (10), 1969-1977. (doi:10.1093/gbe/evt147).

Record type: Article

Abstract

Respiratory electron transport in mitochondria is coupled to ATP synthesis while generating mutagenic oxygen free radicals. Mitochondrial DNA mutation then accumulates with age, and may set a limit to the lifespan of individual, multicellular organisms. Why is this mutation not inherited? Here we demonstrate that female gametes—oocytes—have unusually small and simple mitochondria that are suppressed for DNA transcription, electron transport, and free radical production. By contrast, male gametes—sperm—and somatic cells of both sexes transcribe mitochondrial genes for respiratory electron carriers and produce oxygen free radicals. This germ-line division between mitochondria of sperm and egg is observed in both the vinegar fruitfly and the zebrafish—species spanning a major evolutionary divide within the animal kingdom. We interpret these findings as an evidence that oocyte mitochondria serve primarily as genetic templates, giving rise, irreversibly and in each new generation, to the familiar energy-transducing mitochondria of somatic cells and male gametes. Suppressed mitochondrial metabolism in the female germline may therefore constitute a mechanism for increasing the fidelity of mitochondrial DNA inheritance.

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de Paula et al 2013 GBE.pdf - Version of Record
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Published date: 2013
Keywords: mitochondrial DNA, maternal inheritance, Drosophila melanogaster, Danio rerio, reactive oxygen species, aging
Organisations: Ocean Biochemistry & Ecosystems

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Local EPrints ID: 360590
URI: http://eprints.soton.ac.uk/id/eprint/360590
ISSN: 1759-6653
PURE UUID: 691435be-855c-417e-92da-5d96f61b645d
ORCID for Cathy H. Lucas: ORCID iD orcid.org/0000-0002-5929-7481

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Date deposited: 16 Dec 2013 10:10
Last modified: 15 Mar 2024 02:47

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Contributors

Author: Wilson B.M. de Paula
Author: Ahmed-Noor A. Agip
Author: Fanis Missirlis
Author: Rachel Ashworth
Author: Gemma Vizcay-Barrena
Author: Cathy H. Lucas ORCID iD
Author: John F Allen

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