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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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Mitochondrial production of ROS visualized in ovary and in sperm cells. ROS accumulation in Drosophila ovary (a), zebrafish ovary (b), Drosophila sperm (c), and zebrafish sperm (d). The bright field micrograph shows the corresponding scale bars. DAPI indicates nuclear DNA in the blue channel. Oxidized H2DCF-DA is seen in the green channel and reports the relative amount of ROS in different tissues. Merged overlay of both channels highlights the abundance of ROS in diploid follicle cells compared with the female germ line cells in images (a) and (b), suggesting a reduced rate of electron transfer to oxygen in this cell type. Yellow arrows point to sperm mitochondria, which accumulate ROS as shown in images (c) and (d). See also supplementary figure S2 and movie S2, Supplementary Material online.
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evt147-F3: Mitochondrial production of ROS visualized in ovary and in sperm cells. ROS accumulation in Drosophila ovary (a), zebrafish ovary (b), Drosophila sperm (c), and zebrafish sperm (d). The bright field micrograph shows the corresponding scale bars. DAPI indicates nuclear DNA in the blue channel. Oxidized H2DCF-DA is seen in the green channel and reports the relative amount of ROS in different tissues. Merged overlay of both channels highlights the abundance of ROS in diploid follicle cells compared with the female germ line cells in images (a) and (b), suggesting a reduced rate of electron transfer to oxygen in this cell type. Yellow arrows point to sperm mitochondria, which accumulate ROS as shown in images (c) and (d). See also supplementary figure S2 and movie S2, Supplementary Material online.

Mentions: To estimate the production of ROS by female germ cells, Drosophila ovary at stages 3, 5, and 7 (fig. 3a), and zebrafish egg cell types I and II (fig. 3b) were stained with DAPI, visualizing DNA as blue, and with the ROS indicator H2DCF-DA, which fluoresces green when oxidized. This fluorophore is used to estimate ROS production in situ (Owusu-Ansah et al. 2008). Within ovaries of Drosophila (fig. 3a) and zebrafish (fig. 3b), diploid follicle cells show, respectively, 50-fold and 100-fold higher H2DCF-DA fluorescence intensity than the female germ cells that they surround (supplementary fig. S2, Supplementary Material online). We further certified that the differences in the fluorescence intensity found in those two cells types were not due to discrepancies in the number of mitochondria per cell and per area analyzed (supplementary fig. S1, Supplementary Material online) but rather due to differences in mitochondrial activity. By contrast, sperm cells show H2DCF-DA fluorescence in their mitochondria as seen in figure 3c for Drosophila and figure 3d for zebrafish. The results in figure 3 suggest that ROS production, like mtDNA transcription (fig. 1b), is repressed specifically in oocyte mitochondria. See also supplementary figure S2 and movie S2, Supplementary Material online.Fig. 3.—


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)

Mitochondrial production of ROS visualized in ovary and in sperm cells. ROS accumulation in Drosophila ovary (a), zebrafish ovary (b), Drosophila sperm (c), and zebrafish sperm (d). The bright field micrograph shows the corresponding scale bars. DAPI indicates nuclear DNA in the blue channel. Oxidized H2DCF-DA is seen in the green channel and reports the relative amount of ROS in different tissues. Merged overlay of both channels highlights the abundance of ROS in diploid follicle cells compared with the female germ line cells in images (a) and (b), suggesting a reduced rate of electron transfer to oxygen in this cell type. Yellow arrows point to sperm mitochondria, which accumulate ROS as shown in images (c) and (d). See also supplementary figure S2 and movie S2, Supplementary Material online.
© Copyright Policy - creative-commons
Related In: Results  -  Collection

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

evt147-F3: Mitochondrial production of ROS visualized in ovary and in sperm cells. ROS accumulation in Drosophila ovary (a), zebrafish ovary (b), Drosophila sperm (c), and zebrafish sperm (d). The bright field micrograph shows the corresponding scale bars. DAPI indicates nuclear DNA in the blue channel. Oxidized H2DCF-DA is seen in the green channel and reports the relative amount of ROS in different tissues. Merged overlay of both channels highlights the abundance of ROS in diploid follicle cells compared with the female germ line cells in images (a) and (b), suggesting a reduced rate of electron transfer to oxygen in this cell type. Yellow arrows point to sperm mitochondria, which accumulate ROS as shown in images (c) and (d). See also supplementary figure S2 and movie S2, Supplementary Material online.
Mentions: To estimate the production of ROS by female germ cells, Drosophila ovary at stages 3, 5, and 7 (fig. 3a), and zebrafish egg cell types I and II (fig. 3b) were stained with DAPI, visualizing DNA as blue, and with the ROS indicator H2DCF-DA, which fluoresces green when oxidized. This fluorophore is used to estimate ROS production in situ (Owusu-Ansah et al. 2008). Within ovaries of Drosophila (fig. 3a) and zebrafish (fig. 3b), diploid follicle cells show, respectively, 50-fold and 100-fold higher H2DCF-DA fluorescence intensity than the female germ cells that they surround (supplementary fig. S2, Supplementary Material online). We further certified that the differences in the fluorescence intensity found in those two cells types were not due to discrepancies in the number of mitochondria per cell and per area analyzed (supplementary fig. S1, Supplementary Material online) but rather due to differences in mitochondrial activity. By contrast, sperm cells show H2DCF-DA fluorescence in their mitochondria as seen in figure 3c for Drosophila and figure 3d for zebrafish. The results in figure 3 suggest that ROS production, like mtDNA transcription (fig. 1b), is repressed specifically in oocyte mitochondria. See also supplementary figure S2 and movie S2, Supplementary Material online.Fig. 3.—

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