Deciphering the relationship between mating system and the molecular evolution of the pheromone and receptor genes in...

Here, we present a study of the molecular evolution of the pheromone receptor genes (pre-1 and pre-2) in Neurospora taxa with different mating systems. We focus on comparisons between heterothallic and homothallic taxa, reproducing sexually by outcrossing and by intrahaploid selfing, respectively. Our general aim was to use a phylogenetic framework to investigate whether the evolutionary trajectory of the pheromone and receptor genes in Neurospora differs between heterothallic and homothallic taxa, and among the homothallic lineages/clades previously indicated to represent independent switches from heterothallism to homothallism in the evolutionary history of the genus. We complemented molecular evolution analyses with an expression study of the pre genes and their upstream regulators, the mating-type (mat) genes, in homothallic taxa. Our analyses suggest that the pheromone receptor gene pre-1 is functionally conserved in both heterothallic and homothallic taxa. Moreover, we found evidence of positive selection for a small fraction of codons in the cytoplasmic signal-transducing C-terminal region of the protein PRE-1. Distribution of positively selected codons differs between heterothallic and homothallic groups, suggesting functional divergence associated with mating system. The gene pre-2 was shown to evolve under high selective constraints, with no strong evidence for positive selection. Although our data suggest that both pre-1 and pre-2 are overall functional in homothallic taxa, individual taxa display frame-shift mutations causing premature stop codons, which might indicate loss of function. Transcriptional patterns of pre and mat genes in six homothallic taxa, selected to represent six different switches from heterothallism to homothallism, do not support a universal pattern of regulation of these genes during reproductive tissue development. Taken together, our analyses suggest that the pheromone receptor genes pre-1 and pre-2 are in general functional in homothallic Neurospora taxa, in contrast with the situation for the mat genes that are generally degenerate in these taxa.