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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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Relative quantities of mitochondrial mRNA measured for three key protein subunits of the mitochondrial respiratory chain. (a) A schematic representation of the respiratory electron transport chain of the mitochondrial inner membrane. The protein subunits highlighted in blue, green, and yellow represent the products of the mitochondrial genes nad1, cob, and cox1, respectively. Structures are surface models drawn using PyMol (Schrodinger 2010) from Protein Data Bank (PDB) atomic coordinate files with the following accession numbers: respiratory complex I (NADH-ubiquinone oxidoreductase), 3M9S; respiratory complex II (succinate dehydrogenase), 1ZOY; respiratory complex III (the cytochrome b-c1 complex), 1QCR; complex IV (cytochrome c oxidase), 1V54. (b) Respiratory electron transport gene expression profile. Quantities are shown for mitochondrial mRNA expressed in different tissues of male and female individuals of D. melanogaster and D. rerio. The color coding is the same as that used in (a): blue, nad1; green, cob; yellow, coxI. Error bars indicate standard error of the mean (SEM). P ≤ 0.05. See also supplementary tables S1 and S2, Supplementary Material online.
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evt147-F1: Relative quantities of mitochondrial mRNA measured for three key protein subunits of the mitochondrial respiratory chain. (a) A schematic representation of the respiratory electron transport chain of the mitochondrial inner membrane. The protein subunits highlighted in blue, green, and yellow represent the products of the mitochondrial genes nad1, cob, and cox1, respectively. Structures are surface models drawn using PyMol (Schrodinger 2010) from Protein Data Bank (PDB) atomic coordinate files with the following accession numbers: respiratory complex I (NADH-ubiquinone oxidoreductase), 3M9S; respiratory complex II (succinate dehydrogenase), 1ZOY; respiratory complex III (the cytochrome b-c1 complex), 1QCR; complex IV (cytochrome c oxidase), 1V54. (b) Respiratory electron transport gene expression profile. Quantities are shown for mitochondrial mRNA expressed in different tissues of male and female individuals of D. melanogaster and D. rerio. The color coding is the same as that used in (a): blue, nad1; green, cob; yellow, coxI. Error bars indicate standard error of the mean (SEM). P ≤ 0.05. See also supplementary tables S1 and S2, Supplementary Material online.

Mentions: To determine whether oocyte mitochondria are transcriptionally active, we studied the expression of three mitochondrial genes, nad1, cob, and cox1. Each of these genes encodes a protein subunit of the respiratory electron transport chain, as shown schematically in figure 1a. mtDNA transcriptional rate has been correlated with energy output (Virbasius and Scarpulla 1994; Mehrabian et al. 2005). For Drosophila and zebrafish, we find that ovary has the lowest transcriptional rates for these three mitochondrial genes when compared with other somatic tissues and to sperm, as shown in figure 1b. In both species, we find that the quantity of the gene transcripts in ovary is approximately 15-fold lower than in active somatic tissues such as flight muscle in Drosophila and skeletal muscle in zebrafish. The difference between ovary and intestine was 3.2-fold for Drosophila and 5.5-fold for zebrafish (fig. 1b). We also detected normal levels of respiratory electron transport chain gene transcripts in testis, indicating that decreased mitochondrial transcription is specific to female gonads. qRT-PCR primers are as in supplementary table S1, Supplementary Material online, and statistical analysis of data is presented in supplementary table S2, Supplementary Material online.Fig. 1.—


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)

Relative quantities of mitochondrial mRNA measured for three key protein subunits of the mitochondrial respiratory chain. (a) A schematic representation of the respiratory electron transport chain of the mitochondrial inner membrane. The protein subunits highlighted in blue, green, and yellow represent the products of the mitochondrial genes nad1, cob, and cox1, respectively. Structures are surface models drawn using PyMol (Schrodinger 2010) from Protein Data Bank (PDB) atomic coordinate files with the following accession numbers: respiratory complex I (NADH-ubiquinone oxidoreductase), 3M9S; respiratory complex II (succinate dehydrogenase), 1ZOY; respiratory complex III (the cytochrome b-c1 complex), 1QCR; complex IV (cytochrome c oxidase), 1V54. (b) Respiratory electron transport gene expression profile. Quantities are shown for mitochondrial mRNA expressed in different tissues of male and female individuals of D. melanogaster and D. rerio. The color coding is the same as that used in (a): blue, nad1; green, cob; yellow, coxI. Error bars indicate standard error of the mean (SEM). P ≤ 0.05. See also supplementary tables S1 and S2, Supplementary Material online.
© Copyright Policy - creative-commons
Related In: Results  -  Collection

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

evt147-F1: Relative quantities of mitochondrial mRNA measured for three key protein subunits of the mitochondrial respiratory chain. (a) A schematic representation of the respiratory electron transport chain of the mitochondrial inner membrane. The protein subunits highlighted in blue, green, and yellow represent the products of the mitochondrial genes nad1, cob, and cox1, respectively. Structures are surface models drawn using PyMol (Schrodinger 2010) from Protein Data Bank (PDB) atomic coordinate files with the following accession numbers: respiratory complex I (NADH-ubiquinone oxidoreductase), 3M9S; respiratory complex II (succinate dehydrogenase), 1ZOY; respiratory complex III (the cytochrome b-c1 complex), 1QCR; complex IV (cytochrome c oxidase), 1V54. (b) Respiratory electron transport gene expression profile. Quantities are shown for mitochondrial mRNA expressed in different tissues of male and female individuals of D. melanogaster and D. rerio. The color coding is the same as that used in (a): blue, nad1; green, cob; yellow, coxI. Error bars indicate standard error of the mean (SEM). P ≤ 0.05. See also supplementary tables S1 and S2, Supplementary Material online.
Mentions: To determine whether oocyte mitochondria are transcriptionally active, we studied the expression of three mitochondrial genes, nad1, cob, and cox1. Each of these genes encodes a protein subunit of the respiratory electron transport chain, as shown schematically in figure 1a. mtDNA transcriptional rate has been correlated with energy output (Virbasius and Scarpulla 1994; Mehrabian et al. 2005). For Drosophila and zebrafish, we find that ovary has the lowest transcriptional rates for these three mitochondrial genes when compared with other somatic tissues and to sperm, as shown in figure 1b. In both species, we find that the quantity of the gene transcripts in ovary is approximately 15-fold lower than in active somatic tissues such as flight muscle in Drosophila and skeletal muscle in zebrafish. The difference between ovary and intestine was 3.2-fold for Drosophila and 5.5-fold for zebrafish (fig. 1b). We also detected normal levels of respiratory electron transport chain gene transcripts in testis, indicating that decreased mitochondrial transcription is specific to female gonads. qRT-PCR primers are as in supplementary table S1, Supplementary Material online, and statistical analysis of data is presented in supplementary table S2, Supplementary Material online.Fig. 1.—

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