Interspecific Sex in Grass Smuts and the Genetic Diversity of Their Pheromone-Receptor System

Abstract

The grass smuts comprise a speciose group of biotrophic plant parasites, so-called Ustilaginaceae, which are specifically adapted to hosts of sweet grasses, the Poaceae family. Mating takes a central role in their life cycle, as it initiates parasitism by a morphological and physiological transition from saprobic yeast cells to pathogenic filaments. As in other fungi, sexual identity is determined by specific genomic regions encoding allelic variants of a pheromone-receptor (PR) system and heterodimerising transcription factors. Both operate in a biphasic mating process that starts with PR–triggered recognition, directed growth of conjugation hyphae, and plasmogamy of compatible mating partners. So far, studies on the PR system of grass smuts revealed diverse interspecific compatibility and mating type determination. However, many questions concerning the specificity and evolutionary origin of the PR system remain unanswered. Combining comparative genetics and biological approaches, we report on the specificity of the PR system and its genetic diversity in 10 species spanning about 100 million years of mating type evolution. We show that three highly syntenic PR alleles are prevalent among members of the Ustilaginaceae, favouring a triallelic determination as the plesiomorphic characteristic of this group. Furthermore, the analysis of PR loci revealed increased genetic diversity of single PR locus genes compared to genes of flanking regions. Performing interspecies sex tests, we detected a high potential for hybridisation that is directly linked to pheromone signalling as known from intraspecies sex. Although the PR system seems to be optimised for intraspecific compatibility, the observed functional plasticity of the PR system increases the potential for interspecific sex, which might allow the hybrid-based genesis of newly combined host specificities.

Author Summary

Sexual reproduction is prevalent among eukaryotes and involves the maintenance of different sexes within reproducing populations. Due to similarities to higher eukaryotes like animals and plants, fungi serve as adequate model systems to study sex determination, mate recognition, and mating type evolution. In fungi, sexual identity is determined by a few genes that reside at specific genomic regions. Those so-called mating type loci encode a pheromone-receptor system and heterodimerising transcription factors. Intensive studies of various model organisms uncovered important aspects of sex in fungi. However, comparative surveys that cover distinct phylogenetic groups within the fungal kingdom are still rare, leaving many questions unanswered about the diversity, specificity, and evolutionary transitions of fungal mating types. Here, we report on mating genetics and the specificity of mate recognition in the plant biotrophic basidiomycete family Ustilaginaceae. In our Ustilaginaceae-wide study, we unravel a conserved triallelic pheromone-receptor system that preserved interspecific sexual compatibility for more than 100 million years and most likely gave rise to the convergent evolution of biallelic mating type determinations. Moreover, our results demonstrate that grass smuts represent a valuable model group to study the hybrid-based genesis of novel genotypes and their evolutionary impact on speciation.