Mating Type Loci of Sporisorium reilianum : Novel Pattern with Three a and Multiple b Specificities

Abstract

Sporisorium reilianum and Ustilago maydis are two closely related smut fungi, which both infect maize but differ fundamentally in their mode of plant invasion and site of symptom development. As a prelude to studying the molecular basis of these differences, we have characterized the mating type loci of S. reilianum. S. reilianum has two unlinked mating type loci, a and b. Genes in both loci and adjacent regions show a high degree of synteny to the corresponding genes of U. maydis. The b locus occurs in at least five alleles and encodes two subunits of a heterodimeric homeodomain transcription factor, while the a locus encodes a pheromone/ receptor system. However, in contrast to that of U. maydis, the a locus of S. reilianum exists in three alleles containing two active pheromone genes each. The alleles of the a locus appear to have arisen through recent recombination events within the locus itself. This has created a situation where each pheromone is specific for recognition by only one mating partner.Sporisorium reilianum causes head smut in maize and sorghum (41,42). This soilborne pathogen infects the host plant at the seedling stage (25), supposedly through the roots (37). The infection is systemic, and disease symptoms become apparent only after the onset of flower development when the fungal sori replace male or female inflorescences. In its mode of colonizing the host, S. reilianum is fundamentally different from the well-studied close relative Ustilago maydis, which can infect maize plants via the leaves, stems, or flowers and rapidly causes the formation of prominent tumor-like structures on all green parts of the plant (18). For U. maydis the route of infection has been studied in detail. When haploid, yeast-like sporidia of different mating types recognize each other, they form conjugation hyphae that grow towards each other and fuse at their tips. The resulting dikaryon is filamentous and shows tip growth, leaving empty sections devoid of cytoplasm behind. On the plant surface the dikaryon differentiates into infection structures, so-called appressoria, which are characteristic swellings of the hyphal tips at the site of entry (9, 55). For S. reilianum a detailed molecular investigation of the infection process is lacking. However, it was demonstrated that haploid sporidia as well as germinated teliospores grow filamentously in the vicinity of the root (39). In an in vitro root infection system using germinated teliospores (37), roots were shown to be invaded by hyphae without the apparent formation of appressoria (37).In U. maydis the initial stages of the infection process are regulated by two unlinked mating type loci (23). The a locus exists in two alleles and encodes a pheromone/receptor system responsible for recognition of haploid sporidia. The lipopeptide pheromones Mfa1 and Mfa2 are secreted by sporidia of the opposite a mating type and are reciprocally detected through specific seven-transmembrane pheromone receptors (Pra2 and Pra1). After detection of the pheromone signal, the cells resp...

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).…”

Regulation of haplid phenotypes in Ustilago maydis by ammonium transporters and components of the b mating locus.

“…The genetic material within and around these loci shows a high degree of synteny with U. maydis (Schirawski, Heinze, Wagenknecht, & Kahmann, 2005). The b locus exists in at least five different alleles and encodes two subunits of a heterodimeric homeodomain transcription factor (Schirawski et al, 2005). In contrast to U. maydis which has only two alleles, the a locus of S.…”

“…Like some other closely related smuts, the mating type locus is composed of two unlinked genomic regions, a and b, which code for a pheromone and pheromone receptor and homeodomain proteins, respectively. The genetic material within and around these loci shows a high degree of synteny with U. maydis (Schirawski, Heinze, Wagenknecht, & Kahmann, 2005). The b locus exists in at least five different alleles and encodes two subunits of a heterodimeric homeodomain transcription factor (Schirawski et al, 2005).…”

“…reilianum can be one of three alleles all containing two pheromone precursors (Schirawski et al, 2005). These different versions, designated a1, a2, and a3…”

Examination of the relevance of PI3K and PTEN pathway in Ustilago maydis.

“…The a-locus has two idomorphs, a1 and a2, that both contain genes encoding a secreted mating pheromone a (mfa1/2) and a G protein-coupled pheromone receptor (pra1/2) used in self, non-self recognition. The a1 locus also encodes Right Border a protein 1 (Rba1) which is thought to target to mitochondrial membrane and the a2 locus encodes two mitochondrial proteins Lga2 and Rga2, as well as a pseudogene rba2 (Schirawski et al, 2005). Studies focusing on the lga2 and rga2 genes from the a locus have demonstrated their involvement in determining mitochondrial inheritance in daughter cells (Brefort et al, 2009).…”