Limits...
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.

Show MeSH

Related in: MedlinePlus

Mitochondrial ultrastructure in somatic cells and in male and female gametes. Transmission electron micrographs of D. melanogaster (a) flight muscle, (b) sperm, and (c) oocyte; and D. rerio (e) cardiac muscle, (f) sperm, and (g) oocyte. Letter (m) indicates mitochondria, (n) a haploid nucleus, and (f) a flagellum. Oocyte mitochondria are seen as simpler structures, ranging from 200 to 500 nm, lacking cristae development and matrix electron density (c and g). Muscle (a and e) and sperm (b and f) mitochondria were used as a somatic and male gametic tissue control samples for normal development, respectively. Images were taken using 9,300× magnification. The scale bar corresponds to 500 nm. Stereological analysis of the morphological variations among the three samples: (d) Drosophila; (h) Danio. V(c,m) is the ratio of crista volume to mitochondrion volume. Error bars are SEM, P ≤ 0.01.
© Copyright Policy - creative-commons
Related In: Results  -  Collection

License
getmorefigures.php?uid=PMC3814205&req=5

evt147-F4: Mitochondrial ultrastructure in somatic cells and in male and female gametes. Transmission electron micrographs of D. melanogaster (a) flight muscle, (b) sperm, and (c) oocyte; and D. rerio (e) cardiac muscle, (f) sperm, and (g) oocyte. Letter (m) indicates mitochondria, (n) a haploid nucleus, and (f) a flagellum. Oocyte mitochondria are seen as simpler structures, ranging from 200 to 500 nm, lacking cristae development and matrix electron density (c and g). Muscle (a and e) and sperm (b and f) mitochondria were used as a somatic and male gametic tissue control samples for normal development, respectively. Images were taken using 9,300× magnification. The scale bar corresponds to 500 nm. Stereological analysis of the morphological variations among the three samples: (d) Drosophila; (h) Danio. V(c,m) is the ratio of crista volume to mitochondrion volume. Error bars are SEM, P ≤ 0.01.

Mentions: We examined the ultrastructural morphology of mitochondria in Drosophila flight muscle (fig. 4a) and zebrafish cardiac muscle (fig. 4e), in sperm (Drosophila,fig. 4b; zebrafish, fig. 4f), and in ovary (Drosophila,fig. 4c; zebrafish, fig. 4g). In fruitfly and zebrafish muscle (fig. 4a and e), the single mitochondrion in the field of view is large and has numerous cristae. It is also seen for both species that the mitochondrial matrix presents a relatively high density of the osmium stain. Drosophila sperm mitochondria (fig. 4b) are morphologically specialized, containing a paracrystalline lattice (Perotti 1973), and are therefore more difficult to compare. However, zebrafish sperm mitochondria (fig. 4f) show typical mitochondrial inner-membrane invagination and matrix density characteristic of metabolically active mitochondria. By contrast, Drosophila and zebrafish ovaries (fig. 4c and g, respectively), on the same scale, contain small (<0.5 µm) mitochondria of much simpler morphology, present in a cytoplasm rich in ribosomes and distinct from the nucleus from which it is separated by the characteristic nuclear double membrane (fig. 4c). In both species, stereological analysis confirms that oocyte mitochondrial cristae account for a much lower proportion of total mitochondrial volume than in other tissues (fig. 4d and h for Drosophila and zebrafish, respectively).Fig. 4.—


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 ultrastructure in somatic cells and in male and female gametes. Transmission electron micrographs of D. melanogaster (a) flight muscle, (b) sperm, and (c) oocyte; and D. rerio (e) cardiac muscle, (f) sperm, and (g) oocyte. Letter (m) indicates mitochondria, (n) a haploid nucleus, and (f) a flagellum. Oocyte mitochondria are seen as simpler structures, ranging from 200 to 500 nm, lacking cristae development and matrix electron density (c and g). Muscle (a and e) and sperm (b and f) mitochondria were used as a somatic and male gametic tissue control samples for normal development, respectively. Images were taken using 9,300× magnification. The scale bar corresponds to 500 nm. Stereological analysis of the morphological variations among the three samples: (d) Drosophila; (h) Danio. V(c,m) is the ratio of crista volume to mitochondrion volume. Error bars are SEM, P ≤ 0.01.
© Copyright Policy - creative-commons
Related In: Results  -  Collection

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

evt147-F4: Mitochondrial ultrastructure in somatic cells and in male and female gametes. Transmission electron micrographs of D. melanogaster (a) flight muscle, (b) sperm, and (c) oocyte; and D. rerio (e) cardiac muscle, (f) sperm, and (g) oocyte. Letter (m) indicates mitochondria, (n) a haploid nucleus, and (f) a flagellum. Oocyte mitochondria are seen as simpler structures, ranging from 200 to 500 nm, lacking cristae development and matrix electron density (c and g). Muscle (a and e) and sperm (b and f) mitochondria were used as a somatic and male gametic tissue control samples for normal development, respectively. Images were taken using 9,300× magnification. The scale bar corresponds to 500 nm. Stereological analysis of the morphological variations among the three samples: (d) Drosophila; (h) Danio. V(c,m) is the ratio of crista volume to mitochondrion volume. Error bars are SEM, P ≤ 0.01.
Mentions: We examined the ultrastructural morphology of mitochondria in Drosophila flight muscle (fig. 4a) and zebrafish cardiac muscle (fig. 4e), in sperm (Drosophila,fig. 4b; zebrafish, fig. 4f), and in ovary (Drosophila,fig. 4c; zebrafish, fig. 4g). In fruitfly and zebrafish muscle (fig. 4a and e), the single mitochondrion in the field of view is large and has numerous cristae. It is also seen for both species that the mitochondrial matrix presents a relatively high density of the osmium stain. Drosophila sperm mitochondria (fig. 4b) are morphologically specialized, containing a paracrystalline lattice (Perotti 1973), and are therefore more difficult to compare. However, zebrafish sperm mitochondria (fig. 4f) show typical mitochondrial inner-membrane invagination and matrix density characteristic of metabolically active mitochondria. By contrast, Drosophila and zebrafish ovaries (fig. 4c and g, respectively), on the same scale, contain small (<0.5 µm) mitochondria of much simpler morphology, present in a cytoplasm rich in ribosomes and distinct from the nucleus from which it is separated by the characteristic nuclear double membrane (fig. 4c). In both species, stereological analysis confirms that oocyte mitochondrial cristae account for a much lower proportion of total mitochondrial volume than in other tissues (fig. 4d and h for Drosophila and zebrafish, respectively).Fig. 4.—

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