Abstract
BackgroundThe retention of a genome in mitochondria (mtDNA) has several consequences, among which the problem of ensuring a faithful transmission of its genetic information through generations despite the accumulation of oxidative damage by reactive oxygen species (ROS) predicted by the free radical theory of ageing. A division of labour between male and female germ line mitochondria was proposed: since mtDNA is maternally inherited, female gametes would prevent damages by repressing oxidative phosphorylation, thus being quiescent genetic templates. We assessed mitochondrial activity in gametes of an unusual biological system (doubly uniparental inheritance of mitochondria, DUI), in which also sperm mtDNA is transmitted to the progeny, thus having to overcome the problem of maintaining genetic information viability while producing ATP for swimming.ResultsUltrastructural analysis shows no difference in the conformation of mitochondrial cristae in male and female mature gametes, while mitochondria in immature oocytes exhibit a simpler internal structure. Our data on transcriptional activity in germ line mitochondria show variability between sexes and different developmental stages, but we do not find evidence for transcriptional quiescence of mitochondria. Our observations on mitochondrial membrane potential are consistent with mitochondria being active in both male and female gametes.ConclusionsOur findings and the literature we discussed may be consistent with the hypothesis that template mitochondria are not functionally silenced, on the contrary their activity might be fundamental for the inheritance mechanism. We think that during gametogenesis, fertilization and embryo development, mitochondria undergo selection for different traits (e.g. replication, membrane potential), increasing the probability of the transmission of functional organelles. In these phases of life cycle, the great reduction in mtDNA copy number per organelle/cell and the stochastic segregation of mtDNA variants would greatly improve the efficiency of selection. When a higher mtDNA copy number per organelle/cell is present, selection on mtDNA deleterious mutants is less effective, due to the buffering effect of wild-type variants. In our opinion, 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 a mitochondrial activity would be necessary for the selective process.ReviewersThis article was reviewed by Nick Lane, Fedor S Severin and Fyodor Kondrashov.
Highlights
The retention of a genome in mitochondria has several consequences, among which the problem of ensuring a faithful transmission of its genetic information through generations despite the accumulation of oxidative damage by reactive oxygen species (ROS) predicted by the free radical theory of ageing
Metazoan mitochondrial DNA is very compact and typically consists of 13 genes encoding proteins involved in oxidative phosphorylation (OXPHOS), 24 genes involved in mtDNA translation (2 rRNAs and 22 tRNAs), and a control region for mtDNA replication and transcription, so, mitochondria are involved in multiple cellular processes, the information stored in their genome is limited, and concerns only OXPHOS activity
The retention of a genome in the mitochondrion entails three major issues: 1) mitochondrial and nuclear products interact to carry out their function, so the two genomes need to coevolve despite their markedly different evolutionary dynamics; 2) the potential evolution of selfish mitochondrial variants leading to genomic conflicts [10]; 3) OXPHOS is accompanied by the generation of mutagenic reactive oxygen species (ROS), so mtDNA is located in a potentially hostile environment, which can compromise the integrity of the genetic information [11]
Summary
The retention of a genome in mitochondria (mtDNA) has several consequences, among which the problem of ensuring a faithful transmission of its genetic information through generations despite the accumulation of oxidative damage by reactive oxygen species (ROS) predicted by the free radical theory of ageing. The retention of a genome in the mitochondrion entails three major issues: 1) mitochondrial and nuclear products (proteins and RNAs) interact to carry out their function, so the two genomes need to coevolve despite their markedly different evolutionary dynamics (i.e. substitution rate, recombination and population size; see [7-9] for review); 2) the potential evolution of selfish mitochondrial variants leading to genomic conflicts [10]; 3) OXPHOS is accompanied by the generation of mutagenic reactive oxygen species (ROS), so mtDNA is located in a potentially hostile environment, which can compromise the integrity of the genetic information [11]. It was observed that the physiological level of ROS in normally functioning mitochondria is negligible thanks to defense systems that regulate ROS generation and removal (see [14], for a review)
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