Abstract

Mating-type genes are central to sexual reproduction in ascomycete fungi and result in the establishment of reproductive barriers. Together with hybridization, they both play important roles in the evolution of fungi. Recently, potential hybridization events and MAT genes were separately found in the Elata Clade of Morchella. Herein, we characterized the MAT1–1-1 and MAT1–2-1 genes of twenty-two species in the Esculenta Clade, another main group in the genus Morchella, and proved heterothallism to be the predominant mating strategy among the twenty-two species tested. Ascospores of these species were multi-nuclear and had many mitochondrial nucleoids. The number of ascospore nuclei might be positively related with the species distribution range. Phylogenetic analyses of MAT1–1-1, MAT1–2-1, intergenic spacer (IGS), and partial histone acetyltransferase ELP3 (F1) were performed and compared with the species phylogeny framework derived from the ribosomal internal transcribed spacer region (ITS) and translation elongation factor 1-alpha (EF1-a) to evaluate their species delimitation ability and investigate potential hybridization events. Conflicting topologies among these genes genealogies and the species phylogeny were revealed and hybridization events were detected between several species. Different evolutionary patterns were suggested for MAT genes between the Esculenta and the Elata Clades. Complex evolutionary trajectories of MAT1–1-1, MAT1–2-1, F1 and IGS in the Esculenta Clade were highlighted. These findings contribute to a better understanding of the importance of hybridization and gene transfer in Morchella and especially for the appearance of reproductive modes during its evolutionary process.

Highlights

  • In fungi, sexual reproduction is regulated by genomic regions called mating-type (MAT) loci (Kronstad and Staben 1997; Debuchy et al 2010; Casselton and Feldbrügge 2010), which operate on the establishment of reproductive barriers, determine mating compatibility and result in speciation (Coppin et al 1997; Lee et al 2010; Palumbi 2009; Swanson and Vacquier 2002)

  • Identification of MAT1–1-1 and MAT1–2-1 genes in the genome of yellow morels Through the BLAST analysis of the alpha-box- and HMGcontaining sequences of M. importuna (KY508074 and KY508167) and M. sextelata (KY508145 and KY508228) belonging to the Elata Clade of Morchella, we revealed one MAT1–1-1 and one MAT1–2-1 genes in Morchella sp

  • As the basal taxa of the Esculenta Clade, the length of MAT1–1-1 of M. steppicola was similar to the ones of other species in Esculenta Clade without deletion or insertion; the length of MAT1–2-1 for this species was much longer than the other species since it contained an insertion of fourteen bases

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Summary

Introduction

Sexual reproduction is regulated by genomic regions called mating-type (MAT) loci (Kronstad and Staben 1997; Debuchy et al 2010; Casselton and Feldbrügge 2010), which operate on the establishment of reproductive barriers, determine mating compatibility and result in speciation (Coppin et al 1997; Lee et al 2010; Palumbi 2009; Swanson and Vacquier 2002). The mating-type system is bipolar and has a single MAT locus called MAT1 with two alternate forms as master regulators of sexual reproduction: the MAT1–1-1 and the MAT1–2-1 genes, respectively, encoding for alpha-box and a high mobility group (HMG) domain proteins (Metzenberg and Glass 1990; Debuchy et al 2010). Due to their dissimilar sequences, the two forms of the MAT locus are referred to as idiomorphs instead of alleles (Metzenberg and Glass 1990). Heterothallic fungi are self-sterile, contain only one of the two MAT genes, and need the participation of an opposite mating type partner to reproduce

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