Lineage-specific diversity of pheromone response pathway genes is independent of mating strategy in Ceratocystidaceae

Abstract

The pheromone-receptor system plays a crucial role in mate recognition and fertilisation of ascomycete fungi and is strongly regulated by proteins coded for in the mating-type locus. This locus also determines the mating strategy, sexual identity and mate compatibility of fungal species. Genome assemblies are available for many species in the Ceratocystidaceae, a family of fungi with diverse mating strategies. This provided an opportunity to investigate the relationship between sexual strategy and the pheromone-receptor system in these species. The pheromone and pheromone-receptor genes were identified and characterised from the genome sequences of 52 isolates representing 35 species from 14 genera in the Ceratocystidaceae. Additionally, these data were used to elucidate patterns linked to differences between the pheromones and pheromone receptors, and mating strategies. To do this, the target genes were identified using homologous- and syntenic-based approaches. Putative protein sequences and genomic locations were then compared across the entire family, including species of Huntiella that had previously been characterised. With a few exceptions, putatively functional pheromones and receptors were identified in all the Ceratocystidaceae genomes. The results showed no discernible link between the presence, genomic location or structure of these proteins and mating strategy. Interspecific conservation in sequence and genomic locations revealed greater correlation to taxonomic relatedness, although intraspecific variation was also observed. Interestingly, despite reports of sexual reproduction in Ambrosiella species, all genomes of these species lacked the α-pheromone gene and encoded a non-functional α-pheromone receptor. This is the most extensive study of pheromones and their receptors in a Sordariomycetes family and complements efforts aimed at understanding the complex history of sexual reproduction in the Ceratocystidaceae.