Abstract
Oxidative phosphorylation couples ATP synthesis to respiratory electron transport. In eukaryotes, this coupling occurs in mitochondria, which carry DNA. Respiratory electron transport in the presence of molecular oxygen generates free radicals, reactive oxygen species (ROS), which are mutagenic. In animals, mutational damage to mitochondrial DNA therefore accumulates within the lifespan of the individual. Fertilization generally requires motility of one gamete, and motility requires ATP. It has been proposed that oxidative phosphorylation is nevertheless absent in the special case of quiescent, template mitochondria, that these remain sequestered in oocytes and female germ lines and that oocyte mitochondrial DNA is thus protected from damage, but evidence to support that view has hitherto been lacking. Here we show that female gametes of Aurelia aurita, the common jellyfish, do not transcribe mitochondrial DNA, lack electron transport, and produce no free radicals. In contrast, male gametes actively transcribe mitochondrial genes for respiratory chain components and produce ROS. Electron microscopy shows that this functional division of labour between sperm and egg is accompanied by contrasting mitochondrial morphology. We suggest that mitochondrial anisogamy underlies division of any animal species into two sexes with complementary roles in sexual reproduction. We predict that quiescent oocyte mitochondria contain DNA as an unexpressed template that avoids mutational accumulation by being transmitted through the female germ line. The active descendants of oocyte mitochondria perform oxidative phosphorylation in somatic cells and in male gametes of each new generation, and the mutations that they accumulated are not inherited. We propose that the avoidance of ROS-dependent mutation is the evolutionary pressure underlying maternal mitochondrial inheritance and the developmental origin of the female germ line.
Highlights
Oxidative phosphorylation couples ATP synthesis to respiratory electron transport
It has been proposed that oxidative phosphorylation is absent in the special case of quiescent, template mitochondria, that these remain sequestered in oocytes and female germ lines and that oocyte mitochondrial DNA is protected from damage, but evidence to support that view has hitherto been lacking
It posits that the retention of a given gene within a bioenergetic organelle is the result of natural selection, whereby the corresponding selective advantage for the individual organelle is the ability of the organelle to sense and respond to changes in the redox state of its bioenergetic membrane by being able to regulate the synthesis of proteins in the electron transport chain by means of gene expression
Summary
Mitochondria are the double-membrane-bounded bioenergetic organelles found in the cytoplasm of most eukaryotic cells. Among the many proposals that have been put forward to account for the retention of genomes and genetic systems in mitochondria and chloroplasts [12,24 –29], one hypothesis applies to mitochondria and chloroplasts [19] It posits that the retention of a given gene within a bioenergetic organelle is the result of natural selection, whereby the corresponding selective advantage for the individual organelle is the ability of the organelle to sense and respond to changes in the redox state of its bioenergetic membrane by being able to regulate the synthesis of proteins in the electron transport chain by means of gene expression. CoRR predicts that a mitochondrial redox sensor kinase plays a corresponding role in redox control of respiratory electron transport through effects on mitochondrial gene expression
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