Ancient Trans-specific Polymorphism at Pheromone Receptor Genes in Basidiomycetes

Abstract

In the majority of sexual organisms, reproduction occurs almost exclusively through the combination of distinct and alternate forms, called sexes or mating types. In some fungi, there can be dozens to hundreds of alternate alleles that determine compatible mating types. Such extensive polymorphism is expected to be maintained by balancing selection, and in extreme cases may give rise to trans-specific polymorphism. Here, we analyzed sequences of two pheromone receptors in the Microbotryum fungal species complex (Basidiomycota), which has only two alternate mating types. Several lines of evidence strongly suggest that the pheromone receptors are two allelic sequences acting to determine the alternate A1 and A2 mating types required for mating in Microbotryum. Phylogenetic trees of pheromone receptors in the Microbotryum species complex indicated a trans-specific polymorphism: the Microbotryum sequences from a given mating type were all more similar to the pheromone receptors of distantly related classes of fungi than to the alternate pheromone receptor in the Microbotryum species. A phylogenetic tree built using other known pheromone receptors from basidiomycetes showed that trans-specific polymorphism is widespread. The pheromone receptor alleles from Microbotryum appeared as the oldest, being at least 370 million years old. This represents the oldest known trans-specific polymorphism known in any organism so far, which may be due to the existence of sex chromosomes, obligate sexuality, mitochondrial inheritance linked to the mating type, and a highly selfing mating system in Microbotryum.

Evolution of Mating Systems in Basidiomycetes and the Genetic Architecture Underlying Mating-Type Determination in the YeastLeucosporidium scottii

“…A1 and STE3.A2), and the presence of each allele is always correlated with the mating behavior (Devier et al 2009;Coelho et al 2011). The same holds true for the L. scottii species complex (de Garcia et al 2015) ( Figure 3A), thus showing that pheromone receptor genes are useful markers of mating-type identity across a broad range of Pucciniomycotina species.…”

“…A complete synteny recovery can be observed outside the left and right boundaries of the P/R locus defined by the genes encoding the PP1/PP2Ac and Prefoldin 3 proteins, respectively (Figure 1). It is currently recognized that pheromone receptor alleles in both Microbotryales and Sporidiobolales have been anciently recruited to the P/R locus and maintained across speciation by balancing selection (Devier et al 2009;Coelho et al 2010). Recent phylogenetic analysis of L. scottii P/R alleles revealed that the same holds true: the STE3.A1 allele sequences were all more similar to the same allele specificity from the distantly related red yeast species than to the alternate conspecific allele (STE3.A2) (de Garcia et al 2015).…”

Recent and Massive Expansion of the Mating-Type-Specific Region in the Smut Fungus Microbotryum

“…There is little doubt that the divergence between the A2 and A1 pheromone receptor alleles is ancient (Devier et al 2009). The sequences of these homologs are excessively challenging to align, so recombination between the two mating types in this region must have stopped a very long time ago, perhaps as long as 4 3 10 8 years ago (Devier et al 2009).…”

“…The sequences of these homologs are excessively challenging to align, so recombination between the two mating types in this region must have stopped a very long time ago, perhaps as long as 4 3 10 8 years ago (Devier et al 2009). If we define "strata" as SR regions with different times since cessation of homologous meiotic recombination, following Lahn and Page (1999), the 4.5-kb region adjacent to the pheromone receptor ( Figure 2A) exhibiting poor alignment with the opposite mating type can be regarded as a remnant of an ancient stratum, similar to the Y chromosome region carrying the mammalian sex-determining SRY locus.…”

“…If we define "strata" as SR regions with different times since cessation of homologous meiotic recombination, following Lahn and Page (1999), the 4.5-kb region adjacent to the pheromone receptor ( Figure 2A) exhibiting poor alignment with the opposite mating type can be regarded as a remnant of an ancient stratum, similar to the Y chromosome region carrying the mammalian sex-determining SRY locus. A1-A2 DNA sequence divergence in this region cannot be calculated due to inability to align the sequences from the two mating types, and divergence at the protein level in the pheromone receptor locus is very high (A1-A2 protein identity = 28.4%; Devier et al 2009). Suppression of recombination in this ancient stratum around the pheromone receptor is necessary to prevent recombination between the pheromone and pheromone receptor genes to ensure recognition of the opposite mating type (Kahman and Schirawski 2007;Bakkeren et al 2008).…”