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, 3 (8), e2879

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

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

Shehre-Banoo Malik et al. PLoS One.

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.

Conflict of interest statement

Competing Interests: The authors have declared that no competing interests exist.

Figures

Figure 1
Figure 1. The double-strand break repair model of meiotic recombination, depicting interactions among proteins included in this study.
The names of meiosis-specific proteins are highlighted in green. Exact stoichiometry is not implied. In meiosis I, cohesins bind to sister chromatids (A), after which double-strand DNA breaks are made by Spo11 (accessory proteins not shown) and the axial elements (Hop1) of the synaptonemal complex are formed (B). Double strand break repair is initiated (coupled with (B) in S. cerevisiae) and Hop1 forms lateral elements of the synaptonemal complex (C). Strand exchange proteins are attracted to the double-strand break (accessory proteins not shown) (D). The resulting heteroduplex (E) may be resolved by crossovers, which utilize meiosis-specific proteins (F), or by gene conversion, which does not (G, proteins not shown). This model is based primarily upon details from S. cerevisiae, but includes details from mammals for Msh4 and Msh5, and speculates on the role of Drosophila Mei-9 (Rad1) in (F) as reviewed by , –. Table 1 gives additional details and references.
Figure 2
Figure 2. Phylogenetic trees for meiosis-specific proteins Hop2, Mnd1, Spo11 and Mer3.
All trees shown are the consensus tree topologies determined from ≥700 best trees (i.e. those with the highest posterior probabilities) inferred by Bayesian analysis using alignments of inferred proteins. Animals are indicated in red text, fungi brown, ‘Amoebozoa’ teal, ‘Archaeplastida’ in green, Alveolates plum, ‘Chromista’ purple, ‘Excavata’ blue and prokaryotes shown in black. Branches with the best support – i.e., those with 0.95 to 1.00 Bayesian posterior probabilities – have thicker lines. Numbers at the nodes indicate Bayesian posterior probability followed by percent bootstrap support from 100 replicates of PROML. An asterisk (*) denotes topological constraints placed upon the nodes uniting Fungi and Opisthokonts for Bayesian analysis. Scale bars represent 0.1 amino acid substitutions per site. Details for each tree and the accession numbers for all sequences are provided in Figures S1.1–S1.4 in Supporting Information File S1. (A) Hop2 homologs, unrooted. 167 aligned amino acid sites were analyzed, this consensus topology derived from 900 trees, α = 3.86 (2.71<α<5.37), pI = 0.014 (0.0004<pI<0.051) and lnL = −8363.01. (B) Mnd1 homologs, unrooted. 202 aligned amino acid sites were analyzed, this consensus topology derived from 850 trees, α = 2.80 (2.18<α<3.52), pI = 0.01 (0.0005<pI<0.043) and lnL = −11589.94. (C) Spo11 homologs, rooted with the eukaryotic Top6A paralog outgroup. 148 aligned amino acid sites were analyzed, this consensus topology derived from 700 trees, α = 1.76 (1.34<α<2.23), pI = 0.10 (0.03<pI<0.17) and lnL = −10624.08. (D) Mer3 homologs unrooted. 610 aligned amino acid sites were analyzed, this consensus topology derived from 950 trees, α = 1.60 (1.39<α<1.83), pI = 0.04 (0.02<pI<0.06) and lnL = −27086.67.

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