Evolutionary dynamics of cytoplasmic segregation and fusion: Mitochondrial mixing facilitated the evolution of sex at the origin of eukaryotes

Sexual reproduction is a trait shared by all complex life, but the complete account of its origin is missing. Virtually all theoretical work on the evolution of sex has been centered around the benefits of reciprocal recombination among nuclear genes, paying little attention to the evolutionary dynamics of multi-copy mitochondrial genomes. Here I develop a mathematical model to study the evolution of nuclear alleles inducing cell fusion in an ancestral population of clonal proto-eukaryotes. Segregational drift maintains high mitochondrial variance between clonally reproducing hosts, but the effect of segregation is opposed by cytoplasmic mixing which tends to reduce variation between cells in favor of higher heterogeneity within the cell. Despite the reduced long-term population fitness, alleles responsible for sexual cell fusion can spread to fixation. The evolution of sex requires negative epistatic interactions between mitochondrial mutations under strong purifying selection, low mutation load and weak mitochondrial-nuclear associations. I argue that similar conditions could have been maintained during the late stages of eukaryogenesis, facilitating the evolution of sexual cell fusion and meiotic recombination without compromising the stability of the emerging complex cell

Conflict and cooperation in eukaryogenesis: implications for the timing of endosymbiosis and the evolution of sex

Roughly 1.5-2.0 Gya, the eukaryotic cell evolved from an endosymbiosis of an archaeal host and proteobacterial symbionts. The timing of this endosymbiosis relative to the evolution of eukaryotic features remains subject to considerable debate, yet the evolutionary process itself constrains the timing of these events. Endosymbiosis entailed levels-of-selection conflicts, and mechanisms of conflict mediation had to evolve for eukaryogenesis to proceed. The initial mechanisms of conflict mediation (e.g. signalling with calcium and soluble adenylyl cyclase, substrate carriers, adenine nucleotide translocase, uncouplers) led to metabolic homeostasis in the eukaryotic cell. Later mechanisms (e.g. mitochondrial gene loss) contributed to the chimeric eukaryotic genome. These integral features of eukaryotes were derived because of, and therefore subsequent to, endosymbiosis. Perhaps the greatest opportunity for conflict arose with the emergence of eukaryotic sex, involving whole-cell fusion. A simple model demonstrates that competition on the lower level severely hinders the evolution of sex. Cytoplasmic mixing, however, is beneficial for non-cooperative endosymbionts, which could have used their aerobic metabolism to manipulate the life history of the host. While early evolution of sex may have facilitated symbiont acquisition, sex would have also destabilized the subsequent endosymbiosis. More plausibly, the evolution of sex and the true nucleus concluded the transition

Réparation de l'ADN et mutagenèse dans les mitochondries des vertébrés : preuve de l'asymétrie de l'héritage des brins d'ADN

International audienceA variety of endogenous and exogenous factors induce chemical and structural alterations in cellular DNA in addition to the errors occurring throughout DNA synthesis. These types of DNA damage are cytotoxic, miscoding or both and are believed to be at the origin of cancer and other age-related diseases. A human cell, aside from nuclear DNA, contains thousands of copies of mitochondrial DNA (mtDNA), a double-stranded, circular molecule of 16,569 bp. It has been proposed that mtDNA is a critical target of reactive oxygen species: by-products of oxidative phosphorylation that are generated in the organelle during aerobic respiration. Indeed, oxidative damage to mtDNA is more extensive and persistent as compared to that to nuclear DNA. Although transversions are the hallmark of mutations induced by reactive oxygen species, paradoxically, the majority of mtDNA mutations that occur during ageing and cancer are transitions. Furthermore, these mutations show a striking strand orientation bias: T→C/G→A transitions preferentially occur on the light strand, whereas C→T/A→G on the heavy strand of mtDNA. Here, we propose that the majority of mtDNA progenies, created after multiple rounds of DNA replication, are derived from the heavy strand only, owing to asymmetric replication of the DNA strand anchored to the inner membrane via the D-loop structure.Divers facteurs endogènes et exogènes induisent des altérations chimiques et structurelles dans l'ADN cellulaire, en plus des erreurs qui se produisent tout au long de la synthèse de l'ADN. Ces types de dommages à l'ADN sont cytotoxiques, dus à un mauvais codage ou aux deux, et on pense qu'ils sont à l'origine du cancer et d'autres maladies liées à l'âge. Une cellule humaine, outre l'ADN nucléaire, contient des milliers de copies de l'ADN mitochondrial (ADNmt), une molécule circulaire double brin de 16 569 pb. Il a été proposé que l'ADNmt soit une cible critique des espèces réactives de l'oxygène : des sous-produits de la phosphorylation oxydative qui sont générés dans l'organelle pendant la respiration aérobie. En effet, les dommages oxydatifs de l'ADNmt sont plus étendus et plus persistants que ceux de l'ADN nucléaire. Bien que les transversions soient la marque des mutations induites par les espèces réactives de l'oxygène, paradoxalement, la majorité des mutations de l'ADNmt qui se produisent au cours du vieillissement et du cancer sont des transitions. De plus, ces mutations présentent un biais d'orientation des brins frappant : A→G/G→A transitions se produisent de préférence sur le brin léger, tandis que T→C/A→G sur le brin lourd de l'ADNmt. Ici, nous proposons que la majorité des descendants de l'ADNmt, créés après plusieurs cycles de réplication de l'ADN, soient dérivés du brin lourd uniquement, en raison de la réplication asymétrique du brin d'ADN ancré à la membrane interne via la structure en boucle D.Traduit avec www.DeepL.com/Translator (version gratuite