An Expanded Inventory of Conserved Meiotic Genes Provides Evidence for Sex in Trichomonas vaginalis

Abstract

Meiosis is a defining feature of eukaryotes but its phylogenetic distribution has not been broadly determined, especially among eukaryotic microorganisms (i.e. protists)—which represent the majority of eukaryotic ‘supergroups’. We surveyed genomes of animals, fungi, plants and protists for meiotic genes, focusing on the evolutionarily divergent parasitic protist Trichomonas vaginalis. We identified homologs of 29 components of the meiotic recombination machinery, as well as the synaptonemal and meiotic sister chromatid cohesion complexes. T. vaginalis has orthologs of 27 of 29 meiotic genes, including eight of nine genes that encode meiosis-specific proteins in model organisms. Although meiosis has not been observed in T. vaginalis, our findings suggest it is either currently sexual or a recent asexual, consistent with observed, albeit unusual, sexual cycles in their distant parabasalid relatives, the hypermastigotes. T. vaginalis may use meiotic gene homologs to mediate homologous recombination and genetic exchange. Overall, this expanded inventory of meiotic genes forms a useful “meiosis detection toolkit”. Our analyses indicate that these meiotic genes arose, or were already present, early in eukaryotic evolution; thus, the eukaryotic cenancestor contained most or all components of this set and was likely capable of performing meiotic recombination using near-universal meiotic machinery.

Investigating Host Induced Meiosis in a Fungal Plant Pathogen

“…G. zeae, M. grisea, S. reilianum, and U. maydis lack clear orthologs to DMC1, MND1, and HOP2 (Table 1). Loss of DMC1, MND1, and HOP2 is not unique to the fungal plant pathogens as it has been reported in Drosophila melanogaster, Caenorhabditis elegans, and N. crassa (Malik et al, 2007). Recently in a comparison of eight Candida genomes, these genes were absent in C. guilliermondii and C. lusitaniae (Butler et al, 2009).…”

“…While analyzing the Giardia lamblia genome, Ramesh et al (2005) augmented the list of core meiotic proteins identified by Villeneuve and Hillers (2001) to include HOP1, HOP2, MND1, RAD52, MSH2, MSH6, MLH2, MLH3, and PMS1. While identifying meiotic homologs in Trichomonas vaginalis, Malik et al (2007) added RAD1, MER3, SMC1-5, RAD18, RAD21, REC8, PDS5, and SCC3 to the list of core meiotic proteins conserved across a wide range of plants, animals and fungi. Of the 29 proteins conserved across eukaryotes, only SPO11, HOP1, HOP2, MND1, DMC1, MSH4, MSH5, MER3, and REC8 are reported to be functional solely during meiosis (Malik et al, 2007).…”

“…While identifying meiotic homologs in Trichomonas vaginalis, Malik et al (2007) added RAD1, MER3, SMC1-5, RAD18, RAD21, REC8, PDS5, and SCC3 to the list of core meiotic proteins conserved across a wide range of plants, animals and fungi. Of the 29 proteins conserved across eukaryotes, only SPO11, HOP1, HOP2, MND1, DMC1, MSH4, MSH5, MER3, and REC8 are reported to be functional solely during meiosis (Malik et al, 2007). Interestingly, when looking at the phylogenetic distribution of the 29 core meiotic proteins across the fungi studied by Malik et al (2007), one can observe that the loss of key meiosis proteins is restricted to the 9 proteins only functional during meiosis (with the exception of MLH2 and MLH3 in some fungi).…”

“…Of the 29 proteins conserved across eukaryotes, only SPO11, HOP1, HOP2, MND1, DMC1, MSH4, MSH5, MER3, and REC8 are reported to be functional solely during meiosis (Malik et al, 2007). Interestingly, when looking at the phylogenetic distribution of the 29 core meiotic proteins across the fungi studied by Malik et al (2007), one can observe that the loss of key meiosis proteins is restricted to the 9 proteins only functional during meiosis (with the exception of MLH2 and MLH3 in some fungi). Table 1 shows the presence and absence of these 9 proteins across the model yeasts S. cerevisiae and S. pombe, the model basidiomycete mushroom, C. cinereus, and fungal plant pathogens, including: Gibberella zeae (wheat head blight fungus), Magnaporthe grisea (rice blast fungus), Sporisorium reilianum (maize head smut), and U. maydis (common smut of corn).…”

“…This loss is not unique to the fungal plant pathogens, as D. melanogaster, N. crassa, C. guilliermondii and C. lusitaniae lack clear HOP1 orthologs (Butler et al, 2009;Malik et al, 2007). HOP1 is a structural component of the synaptonemal complex (SC), a tripartite structure which holds homologous chromosomes together during meiosis (reviewed in Loidl, 2006).…”