Energy, ageing, fidelity and sex: oocyte mitochondrial DNA as a protected genetic template
Energy, ageing, fidelity and sex: oocyte mitochondrial DNA as a protected genetic template
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DOI：
10.1098/rstb.2012.0263
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发表时间：
2013-07-19
影响因子：
6.3
通讯作者：
Allen, John F.
中科院分区：
文献类型：
--
作者：
de Paula, Wilson B. M.;Lucas, Cathy H.;Allen, John F.
氧化磷酸化将ATP合成与呼吸电子传递偶联。在真核生物中，这种偶联发生在携带DNA的线粒体中。呼吸电子传递在分子氧存在下产生自由基，活性氧（ROS），这是致突变的。在动物中，线粒体DNA的突变损伤因此在个体的寿命内累积。受精通常需要一个配子的运动性，而运动性需要ATP。有人提出，氧化磷酸化是不存在的特殊情况下，静止的，模板线粒体，这些仍然隔离在卵母细胞和女性生殖细胞系，卵母细胞线粒体DNA因此受到保护，免受损害，但证据支持这一观点迄今为止一直缺乏。在这里，我们表明，雌性配子的奥雷利亚aurita，普通的水母，不转录线粒体DNA，缺乏电子传递，不产生自由基。相反，雄性配子积极转录线粒体基因的呼吸链成分和产生ROS。电子显微镜显示，精子和卵子之间的这种功能分工伴随着线粒体形态的对比。我们认为，线粒体异配现象的基础上任何动物物种的分裂成两个性别的有性生殖中的互补作用。我们预测，静止的卵母细胞线粒体含有DNA作为一个未表达的模板，避免突变的积累，通过女性生殖系传播。卵母细胞线粒体的活跃后代在每一代的体细胞和雄性配子中进行氧化磷酸化，它们积累的突变不会遗传。我们认为，避免ROS依赖性突变是母系线粒体遗传和女性生殖系发育起源的进化压力。
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.