Meiosis gene inventory of four ciliates reveals the prevalence of a synaptonemal complex-independent crossover pathway

Mol Biol Evol. 2014 Mar;31(3):660-72. doi: 10.1093/molbev/mst258. Epub 2013 Dec 13.

Abstract

To establish which meiosis genes are present in ciliates, and to look for clues as to which recombination pathways may be treaded by them, four genomes were inventoried for 11 meiosis-specific and 40 meiosis-related genes. We found that the set of meiosis genes shared by Tetrahymena thermophila, Paramecium tetraurelia, Ichthyophthirius multifiliis, and Oxytricha trifallax is consistent with the prevalence of a Mus81-dependent class II crossover pathway that is considered secondary in most model eukaryotes. There is little evidence for a canonical class I crossover pathway that requires the formation of a synaptonemal complex (SC). This gene inventory suggests that meiotic processes in ciliates largely depend on mitotic repair proteins for executing meiotic recombination. We propose that class I crossovers and SCs were reduced sometime during the evolution of ciliates. Consistent with this reduction, we provide microscopic evidence for the presence only of degenerate SCs in Stylonychia mytilus. In addition, lower nonsynonymous to synonymous mutation rates of some of the meiosis genes suggest that, in contrast to most other nuclear genes analyzed so far, meiosis genes in ciliates are largely evolving at a slower rate than those genes in fungi and animals.

Keywords: Ciliophora; Ichthyophthirius; Oxytricha; Paramecium; Tetrahymena; crossover pathway; genome architecture; meiosis; phylogeny.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Cell Nucleus / genetics
  • Cell Nucleus / ultrastructure
  • Ciliophora / genetics*
  • Ciliophora / ultrastructure
  • Crossing Over, Genetic*
  • Genes, Protozoan / genetics*
  • Likelihood Functions
  • Meiosis / genetics*
  • Phylogeny
  • Synaptonemal Complex* / genetics
  • Synaptonemal Complex* / ultrastructure