The early evolution of meiotic genes

Meiosis is a hallmark of eukaryotes. However, to demonstrate that homologous sexual processes are pan-eukaryotic, it is necessary to compare the molecular machinery of meiotic recombination across diverse eukaryotic groups, especially protists. The homologs of 34 meiotic genes encoding components of the meiotic recombination machinery, sister chromatid cohesion and synaptonemal complexes were identified in the genomes of diverse eukaryotes and verified by phylogenetic analyses. Twelve of these genes function only in meiosis in model organisms (Spo11-1, Spo11-2, Hop1, Hop2, Mnd1, Dmc1, Msh4, Msh5, Mer3, Zip1, Zip4 and Rec8). Homologs of meiosis-specific genes were identified in several organisms previously considered to be asexual, indicating that they are derived from sexual lineages, and may have as-yet-unobserved meiosis. The putatively early-diverged protists Trichomonas and Giardia have orthologs of eight and six of the meiosis-specific genes, respectively. Using degenerate PCR, additional meiosis-specific genes were identified in Naegleria, Acanthamoeba, Amphidinium and other protists. All of the meiotic genes are conserved in animals, fungi and plants; most of the meiotic genes (including the meiosis-specific genes) are also broadly conserved among protist lineages. These data indicate that the molecular machinery for meiotic recombination evolved once, early during eukaryotic evolution, prior to the divergence of major eukaryotic lineages. Thus, the eukaryotic cenancestor likely had each component of this “meiosis detection toolkit”. Many of the 34 meiotic genes – including ten meiosis-specific genes – evolved by gene duplications early during eukaryotic evolution, revealing that gene duplication has been a pervasive evolutionary force in the evolution of the meiotic machinery.