Direct repeat-mediated DNA deletion of the mating type MAT1-2 genes results in unidirectional mating type switching in Sclerotinia trifoliorum

Abstract

The necrotrophic fungal pathogen Sclerotinia trifoliorum exhibits ascospore dimorphism and unidirectional mating type switching - self-fertile strains derived from large ascospores produce both self-fertile (large-spores) and self-sterile (small-spores) offsprings in a 4:4 ratio. The present study, comparing DNA sequences at MAT locus of both self-fertile and self-sterile strains, found four mating type genes (MAT1-1-1, MAT1-1-5, MAT1-2-1 and MAT1-2-4) in the self-fertile strain. However, a 2891-bp region including the entire MAT1-2-1 and MAT1-2-4 genes had been completely deleted from the MAT locus in the self-sterile strain. Meanwhile, two copies of a 146-bp direct repeat motif flanking the deleted region were found in the self-fertile strain, but only one copy of this 146-bp motif (a part of the MAT1-1-1 gene) was present in the self-sterile strain. The two direct repeats were believed to be responsible for the deletion through homologous intra-molecular recombination in meiosis. Tetrad analyses showed that all small ascospore-derived strains lacked the missing DNA between the two direct repeats that was found in all large ascospore-derived strains. In addition, heterokaryons at the MAT locus were observed in field isolates as well as in laboratory derived isolates.

Which MAT gene? Pezizomycotina (Ascomycota) mating-type gene nomenclature reconsidered

“…trifoliorum and Ru. sydowiana;Amselem et al, 2011;Van der Nest et al, 2014;Xu et al, 2016). Although the functions of these two genes remain to be investigated, we propose that the name of the gene in the Eurotiomycetes is retained, while the Leotiomycetes gene is renamed MAT1-2-10 (Table 1).…”

“…Similarly, the MAT1 locus of Sc. trifoliorum was partially assembled from genome sequencing, but was completed using conventional sequencing techniques (Xu et al, 2016).…”

Mating System in the Brown Rot Pathogens Monilinia fructicola, M. laxa, and M. fructigena

“…In M. fructicola the second fragment corresponds to the MAT1-1-1 gene extension in the 39 flanking region. Furthermore, the internal dMAT1-1-1 fragments (290 to 299 bp) showed similarity (E-values £ 1e-44) to the direct or inverted repeats (230 to 250 bp) responsible for intramolecular recombination events in homothallic Sclerotinia species (Chitrampalam et al 2013;Xu et al 2016).…”

“…For instance, B. cinerea and B. elliptica display a bipolar heterothallism, S. minor and S. sclerotiorum display homothallism, while Sclerotinia trifoliorum and S. homoeocarpa include either homothallic or heterothallic isolates. In heterothallic species, the MAT1-1 or the MAT1-2 idiomorphs are singly carried by self-sterile individuals, while in homothallic species they are closely linked end-to-end at a single MAT1 locus in self-fertile individuals (Amselem et al 2011;Chitrampalam and Pryor 2015;De Miccolis Angelini et al 2016;Putman et al 2015;Terhem et al 2015;Xu et al 2016). The mating system governing the sexuality in the genus Monilinia was largely unexplored and no information was available for M. laxa and M. fructigena.…”

“…More recently, different hypotheses have been proposed on the possible evolution of homothallic Sclerotinia species from heterothallic ancestors that are consistent with the structure of newly characterized MAT1 loci in Sclerotiniaceae and are more parsimonious involving a lower number of evolutionary changes. According to Xu et al (2016), indeed, a single structural rearrangement, consisting of a simple insertion of the MAT1-2 idiomorph into the MAT1-1 idiomorph at the MAT1 locus in a heterothallic ancestor with a locus like those of B. cinerea, B. elliptica, and Monilinia species, could be the origin of a homothallic locus, like in the Inv+ MAT alleles in S. minor and S. sclerotiorum and in the L allele in S. trifoliorum.…”