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Cell Cycles, Diplokaryosis and the Archezoan Origin of Sex

Archiv für Protistenkunde
Publication Date
DOI: 10.1016/s0003-9365(11)80315-5
  • Meiosis
  • Syngamy
  • Nuclear Fusion
  • Diplokaryosis
  • Archezoa
  • Microsporidia
  • Metamonada
  • Biology


Summary Sex (Le.meiosis, syngamy and nuclear fusion) first evolved in primitively amitochondrial eukaryotes of the kingdom Archezoa.It is argued that meiosis is monophyletic and that it evolved before either cell or nuclear fusion, as a means for ploidy reduction.Meiosis may have begun so as to correct accidental endopolyploidy and been perfected to allow regular asexual ploidy cycles.These could have allowed early archezoa to have the advantages both of large multi genomic phagotrophic cells and of periodic reductions to a haploid stage to facilitate the selective elimination of harmful mutations.I suggest that one-step meioses, if they genuinely exist in protists, are all secondarily derived from conventional two-step meiosis and are not the ancestral condition.The origin of meiosis required changes in the coupling between DNA replication and nuclear division.Consideration of these cell cycle controls suggests that two-step meiosis could have originated by a single mutation that delayed sister-centromere splitting and thereby simultaneously made it possible for meiosis" to occur in the absence of a preceding DNA replication.The proportionality between genome size and meiotic duration can be explained if meiotic chromosome-pairing is mediated primarily by DNA-DNA hybridization: special synaptonemal complex proteins were therefore not necessary for the origin of meiotic pairing. The diplokaryotic state, or diplokaryosis, which is widespread in the archezoan Microsporidia and Metamonada, may have played a key role in the evolution of these two phyla and has significant implications for early evolution of the eukaryotic cell cycle and recombination.Diplo- .karyosis is defined as the coexistence in the same cell of two haploid nuclei physically attached together and which divide equationally so that each daughter cell receives one daughter nucleus from each parent.In principle nuclear fusion could have evolved in a diplokaryotic or in uninucleate archezoan after the origin of meiosis, and before the origin of syngamy as part of an asexual ploidy cycle.Diplokaryosis itself may have directly favoured the origin of nucleocytoplasmic rearrangements associated with encystation.Modification of the centriole/centrosome cycle was important in these and also in the origin of meiosis.If syngamy was the final step in the evolution of sex, not the initial one as commonly assumed, it could have rapidly spread through the population of an asexual archezoan, with a ploidy cycle involving meiosis and nuclear fusion, as the result of the evolution of a gene encoding a membrane-protein that promotes the fusion of the plasma membrane with that of other related cells.Such a fusogenic gene might have spread faster by being closely linked to a highly beneficial novel gene than by virtue of a general effect on recombination, and faster still if it were inserted into a transposon that could spread intragenomically.

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