Mating-Type Locus Organization and Mating-Type Chromosome Differentiation in the Bipolar Edible Button Mushroom Agaricus bisporus.

Marie Foulongne-Oriol,Arend F Van Peer,Tatiana Giraud,Ursula Kües,Ozgur Taskent,Anton S M Sonnenberg

doi:10.3390/genes12071079

Abstract

In heterothallic basidiomycete fungi, sexual compatibility is restricted by mating types, typically controlled by two loci: PR, encoding pheromone precursors and pheromone receptors, and HD, encoding two types of homeodomain transcription factors. We analysed the single mating-type locus of the commercial button mushroom variety, Agaricus bisporus var. bisporus, and of the related variety burnettii. We identified the location of the mating-type locus using genetic map and genome information, corresponding to the HD locus, the PR locus having lost its mating-type role. We found the mip1 and β-fg genes flanking the HD genes as in several Agaricomycetes, two copies of the β-fg gene, an additional HD2 copy in the reference genome of A. bisporus var. bisporus and an additional HD1 copy in the reference genome of A. bisporus var. burnettii. We detected a 140 kb-long inversion between mating types in an A. bisporus var. burnettii heterokaryon, trapping the HD genes, the mip1 gene and fragments of additional genes. The two varieties had islands of transposable elements at the mating-type locus, spanning 35 kb in the A. bisporus var. burnettii reference genome. Linkage analyses showed a region with low recombination in the mating-type locus region in the A. bisporus var. burnettii variety. We found high differentiation between β-fg alleles in both varieties, indicating an ancient event of recombination suppression, followed more recently by a suppression of recombination at the mip1 gene through the inversion in A. bisporus var. burnettii and a suppression of recombination across whole chromosomes in A. bisporus var. bisporus, constituting stepwise recombination suppression as in many other mating-type chromosomes and sex chromosomes.

Highlights

We found a long stretch of extra DNA (35 kb estimated in length) in the MAT locus of the A. bisporus var. burnettii strain JB137-S8 between the mip1 footprint and the b gene pair
In the reference genomes of the two A. bisporus varieties, we found the genes orthologous to the PR mating-type locus scattered across the genome and lacking a mating-type role
1 of A. bisporus and report the structure of the HD genes and their organization at the mating-type locus for the reference strains of the two varieties bisporus and burnettii

Summary

Introduction

Mating systems are responsible for the degree of selfing/outcrossing in natural populations and impact gene flow, the accumulation of deleterious alleles, and adaptability [1,2,3,4,5,6]. Mating systems can be controlled by, and reciprocally influence, genetic systems governing mating compatibility, such as self-incompatibility systems in plants [7]. Sexual compatibility is governed by a mating-type system, which is most often controlled by two loci segregating independently in basidiomycetes (e.g., rusts, smuts and mushrooms) [8]. To mate and produce offspring successfully, two haploid cells must carry different alleles at both loci. Four different mating types are produced following meiosis in the heterothallic fungi with two mating-type loci, and they are called tetrapolar

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