Organization and Evolutionary Trajectory of the Mating Type (MAT) Locus in Dermatophyte and Dimorphic Fungal Pathogens

Abstract

Sexual reproduction in fungi is governed by a specialized genomic region, the mating type (MAT) locus, whose gene identity, organization, and complexity are diverse. We identified the MAT locus of five dermatophyte fungal pathogens (Microsporum gypseum, Microsporum canis, Trichophyton equinum, Trichophyton rubrum, and Trichophyton tonsurans) and a dimorphic fungus, Paracoccidioides brasiliensis, and performed phylogenetic analyses. The identified MAT locus idiomorphs of M. gypseum control cell type identity in mating assays, and recombinant progeny were produced. Virulence tests in Galleria mellonella larvae suggest the two mating types of M. gypseum may have equivalent virulence. Synteny analysis revealed common features of the MAT locus shared among these five dermatophytes: namely, a small size (ϳ3 kb) and a novel gene arrangement. The SLA2, COX13, and APN2 genes, which flank the MAT locus in other Ascomycota are instead linked on one side of the dermatophyte MAT locus. In addition, the transcriptional orientations of the APN2 and COX13 genes are reversed compared to the dimorphic fungi Histoplasma capsulatum, Coccidioides immitis, and Coccidioides posadasii. A putative transposable element, pogo, was found to have inserted in the MAT1-2 idiomorph of one P. brasiliensis strain but not others. In conclusion, the evolution of the MAT locus of the dermatophytes and dimorphic fungi from the last common ancestor has been punctuated by both gene acquisition and expansion, and asymmetric gene loss. These studies further support a foundation to develop molecular and genetic tools for dermatophyte and dimorphic human fungal pathogens.

Both mating types in the heterothallic fungus Ophiostoma quercus contain MAT1-1 and MAT1-2 genes

“…Of these, the α-box protein encoding gene, MAT1-1-1 (Coppin et al 1997;Debuchy and Turgeon 2006), was first identified in Saccharomyces cerevisiae (Astell et al 1981) and has subsequently been identified in all fungal MAT1-1 idiomorphs ; Kanematsu et al 2007;Li et al 2010). The MAT1-1-2 gene encodes an amphipathic α-helix protein with a conserved Histidine, Proline, Glycine (HPG) domain (Debuchy and Turgeon 2006), while the MAT1-1-3 gene encodes a protein with a High Mobility Group (HMG) domain (Coppin et al 1997;Debuchy and Turgeon 2006).…”

“…For example, comparisons of MAT DNA sequences in different fungi have improved our understanding of the evolution of homothallic and heterothallic mating strategies (Arie et al 1997;Bennett et al 2003;Conde-Ferráez et al 2007;Fraser and Heitman 2004;Li et al 2010;Martin et al 2011;Steenkamp et al 2000;Turgeon 1998). Also, the availability of information on the mating idiomorphs allowed for the assessment of the presence of MAT genes in the genome of apparently asexual species (Foster and Fitt 2003;Mandel et al 2007;Turgeon 1998).…”

The Evolution of Sex: a Perspective from the Fungal Kingdom

“…Since the MAT locus genes are intact and major meiotic genes are conserved in the completed genomic sequences from four different H. capsulatum isolates, this loss of mating ability could involve epigenetic factors. In Microsporum gypseum, cleistothecium formation and the production of asci and ascospores were observed by mating assays (160,302). By scanning electron microscopy, the cleistothecium was found to be enveloped by coiled and spiral hyphae.…”

Unisexual Reproduction Reverses Muller’s Ratchet

“…Our study indicates that transitions to unisexual reproduction from bisexual reproduction may not inevitably lead to Muller's ratchet and an evolutionary dead end, as previously hypothesized (Bell 1982;Charlesworth et al 1993;Lynch et al 1995;Paland and Lynch 2006;Gioti et al 2013). In addition, many pathogenic eukaryotes are thought to have clonal population structures, but recent work has uncovered evidence of cryptic sexual or unisexual cycles (Gräser et al 1996;Peever et al 1999;Berbee et al 2003;Heitman 2006;Morgan et al 2007;Heitman 2010;Li et al 2010;Farrer et al 2011;Stewart et al 2013;Roach et al 2014). Human pathogens of significant public health concern, such as those from the Leishmania, Trypanosoma, and Toxoplasma genera, show signatures of recombination and unisexual cycles (Jenni et al 1986;Gaunt et al 2003;Akopyants et al 2009;Wendte et al 2010;Minot et al 2012).…”