Unequal Recombination and Evolution of the Mating-Type (MAT) Loci in the Pathogenic FungusGrosmannia clavigeraand Relatives

Abstract

Sexual reproduction in fungi is regulated by the mating-type (MAT) locus where recombination is suppressed. We investigated the evolution of MAT loci in eight fungal species belonging to Grosmannia and Ophiostoma (Sordariomycetes, Ascomycota) that include conifer pathogens and beetle symbionts. The MAT1-2 idiomorph/allele was identified from the assembled and annotated Grosmannia clavigera genome, and the MAT locus is flanked by genes coding for cytoskeleton protein (SLA) and DNA lyase. The synteny of these genes is conserved and consistent with other members in Ascomycota. Using sequences from SLA and flanking regions, we characterized the MAT1-1 idiomorph from other isolates of G. clavigera and performed dotplot analysis between the two idiomorphs. Unexpectedly, the MAT1-2 idiomorph contains a truncated MAT1-1-1 gene upstream of the MAT1-2-1 gene that bears the high-mobility-group domain. The nucleotide and amino acid sequence of the truncated MAT1-1-1 gene is similar to its homologous copy in the MAT1-1 idiomorph in the opposite mating-type isolate, except that positive selection is acting on the truncated gene and the alpha(α)-box that encodes the transcription factor has been deleted. The MAT idiomorphs sharing identical gene organization were present in seven additional species in the Ophiostomatales, suggesting that the presence of truncated MAT1-1-1 gene is a general pattern in this order. We propose that an ancient unequal recombination event resulted in the ancestral MAT1-1-1 gene integrated into the MAT1-2 idiomorph and surviving as the truncated MAT1-1-1 genes. The α-box domain of MAT1-1-1 gene, located at the same MAT locus adjacent to the MAT1-2-1 gene, could have been removed by deletion after recombination due to mating signal interference. Our data confirmed a 1:1 MAT/sex ratio in two pathogen populations, and showed that all members of the Ophiostomatales studied here including those that were previously deemed asexual have the potential to reproduce sexually. This ability can potentially increase genetic variability and can enhance fitness in new, ecological niches.

Asexual Propagation of a Virulent Clone Complex in a Human and Feline Outbreak of Sporotrichosis

“…The presumed heterothallism in these species is also confirmed by the amplification of a single mating type in all 196 isolates tested. The general SLA-MAT-APN pattern, as well as the synteny and orientation of the MAT1-1-1, MAT1-1-2, and MAT1-1-3 genes on the MAT1-1 idiomorph, is consistent with other representatives of Grosmannia and Ophiostoma in the Ophiostomatales (39,58). This pattern suggests a shared common heterothallic ancestor among members of the Ophiostomatales.…”

“…The boundaries of both MAT1-1 and MAT1-2 loci within a 20-kb scaffold fragment containing both mating types were determined by reciprocal alignment using ClustalW (41) implemented in the BioEdit software (42). We also characterized the MAT1-2 idiomorph of S. globosa, another human pathogen, using longrange PCR amplification with a primer-walking sequencing approach (39).…”

“…2). The deduced amino acid sequences of SLA2 and APN2 shared, respectively, 89% and 62% identity with those of Grosmannia clavigera, a tree pathogen in the Ophiostomatales (39). Three open reading frames (ORFs) were predicted in the MAT1-1 idiomorph of the S. schenckii genome: MAT1-1-1, MAT1-1-2, and MAT1-1-3, encoding proteins of 893, 362, and 191 amino acids (aa), respectively (Fig.…”

“…However, little is known at the molecular level of the sexual cycle of Ophiostomatales; MAT loci and flanking genes have been identified only in Ophiostoma ulmi, O. novo-ulmi, Ophiostoma himal-ulmi, and O. quercus (27,(36)(37)(38). Recently the MAT genes have been characterized in six Grosmannia species, as well as in Ophiostoma montium, and unequal recombination has been suggested to account for the presence of a truncated MAT1-1-1 in isolates of the opposite mating type (39). Although sexual reproduction has never been observed, the sexual state of Sporothrix species is predicted to be Ophiostoma-like based on the observation that Sporothrix is phylogenetically nested within Ophiostoma (21,22).…”

Fungal Frequency and Mite Load Trends Interact with a Declining Mountain Pine Beetle Population

“…Sexual spores benefit fungi by increasing the genetic diversity and foster further sexual reproduction by increasing the distinct mating types to occur in the new host. It is probable that mite dissemination of the O. montium sexual spores may contribute to the greater genetic recombination found in that species [21,74].…”