Diverse members of the Xylariales lack canonical mating-type regions

Abstract

A survey of genomes reported here for 10 isolates of Monosporascus species and an additional 25 genomes from other members of the Xylariales (representing 15 genera) available in public databases indicated that genes typically associated with MAT1-1 (mat A) or MAT1-2 (mat a) mating types are absent or have diverged greatly relative to counterparts in other Pezizomycotina. This was particularly surprising for isolates known to be homothallic, given that homothallic members of the Pezizomycotina typically possess a MAT1-1-1 (mat A-1) gene and one or both of two other closely-linked mating-type genes, MAT1-1-2 (mat A-2) and MAT1-1-3 (mat A-3), in addition to MAT1-2-1 (mat a-1). We failed to detect candidate genes for either MAT1-1-1 or MAT1-1-2 in any member of the Xylariales. Genes related to MAT1-2-1 and MAT1-1-3 are present in the genomes examined, but most appear to be orthologs of MATA_HMG (high-mobility group) genes with non-mating-type functions rather than orthologs of mating-type genes. Several MATA_HMG genes were found in genome positions that suggest they are derived from mating-type genes, but these genes are highly divergent relative to known MAT1-2-1 and MAT1-1-3 genes. The genomes examined represent substantial diversity within the order and include M. cannonballus, M. ibericus, Xylaria hypoxylon, X. striata, Daldinia eschscholzii, Eutypa lata, Rosellinia necatrix, Microdochium bolleyi and several others. We employed a number of avenues to search for homologs, including multiple BLAST approaches and examination of annotated genes adjacent to genes known to flank mating regions in other members of the Ascomycota. The results suggest that the mating regions have been lost from, or altered dramatically in, the Xylariales genomes examined and that mating and sexual development in these fungi are controlled differently than has been reported for members of the Pezizomycotina studied to date.

Keywords: Genomics; Mating type; Microdochium; Monosporascus; Xylaria; Xylariales.

Fig. 1.

Comparison of sla2/apn2 gene regions from three Xylariales genomes with the mating- type regions from Neurospora crassa. Homologs of sla2 and apn2 are commonly found flanking mating-type genes in other Ascomycota and gene orientations are highly conserved (discussed in text). Note that the orientations of sla2, apn2 and MATA_HMG genes in Microdochium bolleyi J235TASD1 are consistent with the orientations of sla2, apn2 and MATA_HMG mating-type genes (mat a-1 and mat A-3) in N. crassa. On the other hand, the orientation of the MATA_HMG gene in two strains of Monosporascus sp., MG133 and MG162, is reversed relative to homologs in M. bolleyi and N. crassa; and the order of the three genes is different in Xylaria hypoxylon OSC100004. The arrangement of these genes in other members of the Xylariales varies substantially. In contrast with the results shown here, in most cases MATA_HMG genes in members of the Xylariales were not observed to be linked with sla2 and apn2 homologs (Supplemental Table S2). Accession numbers for N. crassa mating-type proteins and gene regions are given in Table 2. Accession numbers for the Xylariales genomes are given in Table 1, and specific gene locations and protein IDs are presented in Supplemental Table S2.