The Sclerotinia sclerotiorum Mating Type Locus (MAT) Contains a 3.6-kb Region That Is Inverted in Every Meiotic Generation

Abstract

Sclerotinia sclerotiorum is a fungal plant pathogen and the causal agent of lettuce drop, an economically important disease of California lettuce. The structure of the S. sclerotiorum mating type locus MAT has previously been reported and consists of two idiomorphs that are fused end-to-end as in other homothallics. We investigated the diversity of S. sclerotiorum MAT using a total of 283 isolates from multiple hosts and locations, and identified a novel MAT allele that differed by a 3.6-kb inversion and was designated Inv+, as opposed to the previously known S. sclerotiorum MAT that lacked the inversion and was Inv-. The inversion affected three of the four MAT genes: MAT1-2-1 and MAT1-2-4 were inverted and MAT1-1-1 was truncated at the 3’-end. Expression of MAT genes differed between Inv+ and Inv- isolates. In Inv+ isolates, only one of the three MAT1-2-1 transcript variants of Inv- isolates was detected, and the alpha1 domain of Inv+ MAT1-1-1 transcripts was truncated. Both Inv- and Inv+ isolates were self-fertile, and the inversion segregated in a 1∶1 ratio regardless of whether the parent was Inv- or Inv+. This suggested the involvement of a highly regulated process in maintaining equal proportions of Inv- and Inv+, likely associated with the sexual state. The MAT inversion region, defined as the 3.6-kb MAT inversion in Inv+ isolates and the homologous region of Inv- isolates, was flanked by a 250-bp inverted repeat on either side. The 250-bp inverted repeat was a partial MAT1-1-1 that through mediation of loop formation and crossing over, may be involved in the inversion process. Inv+ isolates were widespread, and in California and Nebraska constituted half of the isolates examined. We speculate that a similar inversion region may be involved in mating type switching in the filamentous ascomycetes Chromocrea spinulosa, Sclerotinia trifoliorum and in certain Ceratocystis species.

Characterization and distribution of mating-type genes of the turfgrass pathogen Sclerotinia homoeocarpa on a global scale

“…The evolution of homothallism from an ancestral heterothallic state has been hypothesized in many Ascomycota, including recently for S. sclerotiorum (Chitrampalam et al, 2013). Data from our study is not in conflict with this suggestion, and could provide a more parsimonious explanation for the transition between homothallism and heterothallism compared to the homothallism origin models discussed above.…”

“…To follow the naming conventions proposed by Turgeon and Yoder (2000), the putative gene adjacent to MAT1-1-1 in the Sclerotiniaceae and Rutstroemiaceae, currently also designated as MAT1-1-5, would need to be designated as MAT1-1-8. However, while the MAT1-1-5 and MAT1-2-4 designations were used in the literature first by (Mandel et al, 2007), the first GenBank accessions containing these designations are for S. homoeocarpa (Liberti et al, 2012) and S. sclerotiorum (Chitrampalam et al, 2013), respectively, and it is unclear which has priority (see Supplementary Material for additional discussion on nomenclature).…”

MAT gene idiomorphs suggest a heterothallic sexual cycle in a predominantly asexual and important pine pathogen

“…The novel ORF found alongside the MAT1-2-1 gene in the MAT1-2 idiomorph was designated as the MAT1-2-5 gene being the fifth such gene described associated with the MAT1-2 idiomorph. The function of these additional MAT genes in the MAT idiomorphs, which has also been observed in other fungal species (Kanamori et al, 2007;Martin et al, 2011;Chitrampalam et al, 2013), remain unknown.…”

Mating-type switching by chromosomal inversion in methylotrophic yeasts suggests an origin for the three-locusSaccharomyces cerevisiaesystem

“…Such a system can be formed spontaneously by DNA introgression between the MAT idiomorphs in a heterothallic fungus (SI Appendix, Fig. S7), as appears to have occurred very recently in Sclerotinia sclerotiorum (Pezizomycotina), which inverts part of its MAT locus in every meiotic generation (57). Further evidence for a two-locus ancestor comes from computer simulations (Fig.…”