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.

Molecular and Genetic Evidence for a Tetrapolar Mating System in the Basidiomycetous Yeast Kwoniella mangrovensis and Two Novel Sibling Species

“…A somewhat parallel situation was observed in the distantly related red yeasts of the Sporidiobolales (class Microbotryomycetes, subphylum Pucciniomycotina) for which genomic regions around the P/R locus exhibited extensive rearrangements between complementary mating types of each species, while synteny was well conserved across species when the homologous regions of the same mating type were compared (41). A similar conclusion was reached by Kellner et al (6) when comparing the triallelic P/R loci of different smut species in the Ustilaginomycetes. These findings suggest that the MAT gene structure of each allele of the P/R loci in different species was fixed long before speciation occurred.…”

“…In the bipolar species, there are normally only two possible versions for the content of the single MAT locus, and hence only two mating types exist. Recent studies have suggested that the basidiomycete bipolar mating systems are evolutionarily derived from tetrapolar ancestral states (4)(5)(6).…”

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

“…Second, within the same strain, pheromone precursor genes code for identical peptides, suggesting the presence of only one MAT specificity per strain. This organization contrasts, for example, with the triallelic P/R locus of several smut species in the Ustilaginales, in which two different MAT-specific pheromones are encoded at each P/R allele (Schirawski et al 2005;Kellner et al 2011). It also differs from other model species in the subphylum Agaricomycotina, such as Schizophyllum commune and C. cinerea, in that these species have evolved an enormous repertoire of pheromone/receptor alleles likely arising by duplication of an archetypal P/R locus, followed by rounds of recombination and diversification between alleles (Riquelme et al 2005).…”

Two new records of smut fungi for Panama and new combinations into the genus Tolyposporium

“…& Begerow AJ236155 (Piepenbring et al, 1999), Tolyposporium isolepidis EU246949 (Vánky & Lutz, 2008), Tolyposporium junci AF009876 (Begerow et al, 1997), Tolyposporium neillii EU246952 (Vánky & Lutz, 2008), Tolyposporium piluliforme AF009871 (as Heterotolyposporium piluliforme, Begerow et al, 1997), Ustanciosporium gigantosporum (Liro) M. Piepenbr. JN367325 (Kellner et al, 2011), Ustanciosporium standleyanum (Zundel) M. Piepenbr. JN367326 (Kellner et al, 2011), Ustilago affinis Ellis & Everh.…”

“…JN367325 (Kellner et al, 2011), Ustanciosporium standleyanum (Zundel) M. Piepenbr. JN367326 (Kellner et al, 2011), Ustilago affinis Ellis & Everh. AF133581 (Begerow et al, 2000), Ustilago echinata J. Schröt.…”