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

de Paula WB, Agip AN, Missirlis F, Ashworth R, Vizcay-Barrena G, Lucas CH, Allen JF - Genome Biol Evol (2013)

Bottom Line: 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.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 germ line may therefore constitute a mechanism for increasing the fidelity of mitochondrial DNA inheritance.

View Article: PubMed Central - PubMed

Affiliation: School of Biological and Chemical Sciences, Queen Mary University of London, London, United Kingdom.

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 germ line may therefore constitute a mechanism for increasing the fidelity of mitochondrial DNA inheritance.

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A model for maintenance of mtDNA by maternal inheritance of template mitochondria transmitted in the cytoplasm. An oocyte (egg cell) contains a nucleus with a haploid chromosome number (n) and a cytoplasm with multiple template mitochondria. A sperm cell, also with a haploid nucleus (n), is motile, and its motility requires ATP from active mitochondria performing oxidative phosphorylation (OXPHOS). Following fertilization, active sperm mitochondria are rapidly degraded, leaving only the maternal, template mitochondria in the cytoplasm of the diploid (2 n) zygote (or fertilized egg). Successive cell divisions in embryogenesis involve mitosis and differentiation—and division—of most template mitochondria into active OXPHOS mitochondria, which eventually dominate and populate not only somatic tissues but also the male germ line in which sperm are generated by meiosis in males for the next generation. However, some cells are sequestered and continue to carry only quiescent, template mitochondria, through meiosis and oogenesis to give the oocytes of females in the next generation. These cells comprise the female germ line. Female germ cells are never supplied with ATP by oxidative phosphorylation in their own mitochondria, but depend for their maintenance, at low metabolic rate, on ATP supplied, directly or indirectly, by neighboring somatic cells (follicle cells or nurse cells) that are specially adapted for this role. This hypothesis, after Allen (1996), predicts that the female germ line forms an indefinitely replicating vehicle for accurate transmission of mtDNA between generations. See also supplementary movie S3, Supplementary Material online.
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evt147-F5: A model for maintenance of mtDNA by maternal inheritance of template mitochondria transmitted in the cytoplasm. An oocyte (egg cell) contains a nucleus with a haploid chromosome number (n) and a cytoplasm with multiple template mitochondria. A sperm cell, also with a haploid nucleus (n), is motile, and its motility requires ATP from active mitochondria performing oxidative phosphorylation (OXPHOS). Following fertilization, active sperm mitochondria are rapidly degraded, leaving only the maternal, template mitochondria in the cytoplasm of the diploid (2 n) zygote (or fertilized egg). Successive cell divisions in embryogenesis involve mitosis and differentiation—and division—of most template mitochondria into active OXPHOS mitochondria, which eventually dominate and populate not only somatic tissues but also the male germ line in which sperm are generated by meiosis in males for the next generation. However, some cells are sequestered and continue to carry only quiescent, template mitochondria, through meiosis and oogenesis to give the oocytes of females in the next generation. These cells comprise the female germ line. Female germ cells are never supplied with ATP by oxidative phosphorylation in their own mitochondria, but depend for their maintenance, at low metabolic rate, on ATP supplied, directly or indirectly, by neighboring somatic cells (follicle cells or nurse cells) that are specially adapted for this role. This hypothesis, after Allen (1996), predicts that the female germ line forms an indefinitely replicating vehicle for accurate transmission of mtDNA between generations. See also supplementary movie S3, Supplementary Material online.

Mentions: The results presented here demonstrate that oocyte mitochondria are in a quiescent state in both a protostome (D. melanogaster) and a deuterostome (D. rerio), representing the two branches of the Bilateria. We interpret this result as a nonpathological condition that secures the faithful maternal transmission of mtDNA, from germ line to germ line, across generations (Allen 1996). Even in exceptional species with doubly uniparental inheritance of mtDNA, only a female germ line gives rise to mitochondria of another female germ line, while the male germ line mitochondria can be inherited from either sex (Zouros et al. 1994; Ghiselli et al. 2013). It should be noted that uniparental inheritance of mitochondria is also the rule in single-celled eukaryotes, protists, with morphologically indistinguishable isogametes (Gyawali and Lin 2011). For multicellular eukaryotes, our conclusion is summarized in figure 5 and supplementary movie S3, Supplementary Material online. This interpretation is consistent with results reported for a cnidarian, the jellyfish A. aurita (de Paula et al. 2013), and might therefore be predicted to apply as a basic pattern of template mitochondrial transmission within the entire animal kingdom.Fig. 5.—


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

de Paula WB, Agip AN, Missirlis F, Ashworth R, Vizcay-Barrena G, Lucas CH, Allen JF - Genome Biol Evol (2013)

A model for maintenance of mtDNA by maternal inheritance of template mitochondria transmitted in the cytoplasm. An oocyte (egg cell) contains a nucleus with a haploid chromosome number (n) and a cytoplasm with multiple template mitochondria. A sperm cell, also with a haploid nucleus (n), is motile, and its motility requires ATP from active mitochondria performing oxidative phosphorylation (OXPHOS). Following fertilization, active sperm mitochondria are rapidly degraded, leaving only the maternal, template mitochondria in the cytoplasm of the diploid (2 n) zygote (or fertilized egg). Successive cell divisions in embryogenesis involve mitosis and differentiation—and division—of most template mitochondria into active OXPHOS mitochondria, which eventually dominate and populate not only somatic tissues but also the male germ line in which sperm are generated by meiosis in males for the next generation. However, some cells are sequestered and continue to carry only quiescent, template mitochondria, through meiosis and oogenesis to give the oocytes of females in the next generation. These cells comprise the female germ line. Female germ cells are never supplied with ATP by oxidative phosphorylation in their own mitochondria, but depend for their maintenance, at low metabolic rate, on ATP supplied, directly or indirectly, by neighboring somatic cells (follicle cells or nurse cells) that are specially adapted for this role. This hypothesis, after Allen (1996), predicts that the female germ line forms an indefinitely replicating vehicle for accurate transmission of mtDNA between generations. See also supplementary movie S3, Supplementary Material online.
© Copyright Policy - creative-commons
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC3814205&req=5

evt147-F5: A model for maintenance of mtDNA by maternal inheritance of template mitochondria transmitted in the cytoplasm. An oocyte (egg cell) contains a nucleus with a haploid chromosome number (n) and a cytoplasm with multiple template mitochondria. A sperm cell, also with a haploid nucleus (n), is motile, and its motility requires ATP from active mitochondria performing oxidative phosphorylation (OXPHOS). Following fertilization, active sperm mitochondria are rapidly degraded, leaving only the maternal, template mitochondria in the cytoplasm of the diploid (2 n) zygote (or fertilized egg). Successive cell divisions in embryogenesis involve mitosis and differentiation—and division—of most template mitochondria into active OXPHOS mitochondria, which eventually dominate and populate not only somatic tissues but also the male germ line in which sperm are generated by meiosis in males for the next generation. However, some cells are sequestered and continue to carry only quiescent, template mitochondria, through meiosis and oogenesis to give the oocytes of females in the next generation. These cells comprise the female germ line. Female germ cells are never supplied with ATP by oxidative phosphorylation in their own mitochondria, but depend for their maintenance, at low metabolic rate, on ATP supplied, directly or indirectly, by neighboring somatic cells (follicle cells or nurse cells) that are specially adapted for this role. This hypothesis, after Allen (1996), predicts that the female germ line forms an indefinitely replicating vehicle for accurate transmission of mtDNA between generations. See also supplementary movie S3, Supplementary Material online.
Mentions: The results presented here demonstrate that oocyte mitochondria are in a quiescent state in both a protostome (D. melanogaster) and a deuterostome (D. rerio), representing the two branches of the Bilateria. We interpret this result as a nonpathological condition that secures the faithful maternal transmission of mtDNA, from germ line to germ line, across generations (Allen 1996). Even in exceptional species with doubly uniparental inheritance of mtDNA, only a female germ line gives rise to mitochondria of another female germ line, while the male germ line mitochondria can be inherited from either sex (Zouros et al. 1994; Ghiselli et al. 2013). It should be noted that uniparental inheritance of mitochondria is also the rule in single-celled eukaryotes, protists, with morphologically indistinguishable isogametes (Gyawali and Lin 2011). For multicellular eukaryotes, our conclusion is summarized in figure 5 and supplementary movie S3, Supplementary Material online. This interpretation is consistent with results reported for a cnidarian, the jellyfish A. aurita (de Paula et al. 2013), and might therefore be predicted to apply as a basic pattern of template mitochondrial transmission within the entire animal kingdom.Fig. 5.—

Bottom Line: 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.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 germ line may therefore constitute a mechanism for increasing the fidelity of mitochondrial DNA inheritance.

View Article: PubMed Central - PubMed

Affiliation: School of Biological and Chemical Sciences, Queen Mary University of London, London, United Kingdom.

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 germ line may therefore constitute a mechanism for increasing the fidelity of mitochondrial DNA inheritance.

Show MeSH
Related in: MedlinePlus