Mitochondrial activity in gametes and transmission of viable mtDNA

Oxidative phosphorylation makes mitochondria a potentially detrimental environment for DNA because of the possible mutagenic effect of Reactive Oxygen Species (ROS) that can affect the transmission of a correct genetic information through generations. How can a faithful transmission be achieved? Since the mtDNA is commonly maternally inherited, it was proposed that female gametes would prevent damages by repressing oxidative phosphorylation and being quiescent genetic templates. We show evidence from several species that are consistent with mitochondria being active in both gamete types, not only in species with strictly maternal inheritance (SMI), but also in species that naturally transmit mitochondria also through males (doubly uniparental inheritance of mitochondria, DUI). Consistently with these observations, we support the alternative hypothesis that the activity of template mitochondria is fundamental for the inheritance mechanism. During gametogenesis, fertilization, and embryo development, the great reduction in mtDNA copy number per organelle/cell and the stochastic segregation of mtDNA variants would greatly improve the efficiency of selection: a combination of drift and selection on germ line mtDNA population might be responsible for the maintenance of viable mitochondrial genetic information through generations, and the mitochondrial activity would be the phenotype under selection. In this case, efficient mechanisms of mitochondrial genome preservation and/or ROS scavenging, or alternative pathways of ATP production, would act to favour an accurate transmission of the genetic information, albeit coupled with a full mitochondrial activity. Thanks to its unusual features, DUI emerges as an excellent model system to study these problematics.