Evolutionary Plasticity of Mating-Type Determination Mechanisms inParamecium aureliaSibling Species

Abstract

The Paramecium aurelia complex, a group of morphologically similar but sexually incompatible sibling species, is a unique example of the evolutionary plasticity of mating-type systems. Each species has two mating types, O (Odd) and E (Even). Although O and E types are homologous in all species, three different modes of determination and inheritance have been described: genetic determination by Mendelian alleles, stochastic developmental determination, and maternally inherited developmental determination. Previous work in three species of the latter kind have revealed the key roles of the E-specific transmembrane protein mtA and its highly specific transcription factor mtB: type O clones are produced by maternally inherited genome rearrangements that inactivate either mtA or mtB during development. Here we show, through transcriptome analyses in 5 additional species representing the three determination systems, that mtA expression specifies type E in all cases. We further show that the Mendelian system depends on functional and non-functional mtA alleles, and identify novel developmental rearrangements in mtA and mtB which now explain all cases of maternally inherited mating-type determination. Epistasis between these genes likely evolved from less specific interactions between paralogs in the P. aurelia common ancestor, after a whole-genome duplication, but the mtB gene was subsequently lost in three P. aurelia species which appear to have returned to an ancestral regulation mechanism. These results suggest a model accounting for evolutionary transitions between determination systems, and highlight the diversity of molecular solutions explored among sibling species to maintain an essential mating-type polymorphism in cell populations.

Massive colonization of protein-coding exons by selfish genetic elements in Paramecium germline genomes

“…Mutations in MAC-destined regions can generate sequence motifs that are recognized by the IES excision machinery and thereby create new IESs. There is indeed evidence that cryptic IES signals occasionally trigger the excision of MAC-destined sequences [ 4 , 29 ] and that some IESs originated from MAC-destined sequences [ 12 , 13 ]. However, our results suggest that the vast majority of IESs correspond to unrecognizable fossils of mobile elements—as initially proposed by Klobutcher and Herrick [ 10 , 11 ].…”

“…Such mutations are expected to be generally deleterious and hence to be counterselected. But occasionally, they might have been positively selected in some genes because they provide a mean to modulate their expression during MAC development or to generate phenotypic diversity among clones, as previously observed for IESs overlapping mating-type genes in many species [ 12 , 13 ]. This scenario would notably explain the presence of conserved IESs overlapping with cellular genes (e.g., Fig 5B ).…”

“…tetraurelia lineage [ 4 ]. There is also evidence that some IESs originated from MAC sequences, as described, for example, for the IESs involved in mating type determination in several species [ 12 , 13 ]. The extent to which the 45,000 IESs detected in P .…”

“…P . tetraurelia belongs to the Paramecium aurelia group of species that comprises a score of morphologically similar yet genetically isolated species [ 14 – 17 ] (see [ 13 ] for a detailed description of the species). Here, we sequenced the germline MIC genomes of 8 P .…”

Massive colonization of protein-coding exons by selfish genetic elements inParameciumgermline genomes

“…However, the rather small number of mobile IESs detected (23 copies out of 45,000 IESs) suggested a limited activity of transposable IESs in the recent evolutionary history of the P. tetraurelia lineage [4]. There is also evidence that some IESs originated from MAC sequences, as described for instance for the IESs involved in mating type determination in several species [12,13]. The extent to which the 45,000 IESs detected in P. tetraurelia derive from TEs or from MAC sequences therefore remained unclear.…”