Mating-Type Locus Organization and Mating-Type Chromosome Differentiation in the Bipolar Edible Button Mushroom <i>Agaricus bisporus</i>

In heterothallic basidiomycete fungi, sexual compatibility is restricted by mating types, typically controlled by two loci: <i>PR</i>, encoding pheromone precursors and pheromone receptors, and <i>HD</i>, encoding two types of homeodomain transcription factors. We analysed th...

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Main Authors: Marie Foulongne-Oriol, Ozgur Taskent, Ursula Kües, Anton S. M. Sonnenberg, Arend F. van Peer, Tatiana Giraud
Format: Article
Language:English
Published: MDPI AG 2021-07-01
Series:Genes
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Online Access:https://www.mdpi.com/2073-4425/12/7/1079
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author Marie Foulongne-Oriol
Ozgur Taskent
Ursula Kües
Anton S. M. Sonnenberg
Arend F. van Peer
Tatiana Giraud
author_facet Marie Foulongne-Oriol
Ozgur Taskent
Ursula Kües
Anton S. M. Sonnenberg
Arend F. van Peer
Tatiana Giraud
author_sort Marie Foulongne-Oriol
collection DOAJ
description In heterothallic basidiomycete fungi, sexual compatibility is restricted by mating types, typically controlled by two loci: <i>PR</i>, encoding pheromone precursors and pheromone receptors, and <i>HD</i>, encoding two types of homeodomain transcription factors. We analysed the single mating-type locus of the commercial button mushroom variety, <i>Agaricus bisporus</i> var. <i>bisporus</i>, and of the related variety <i>burnettii</i>. We identified the location of the mating-type locus using genetic map and genome information, corresponding to the <i>HD</i> locus, the <i>PR</i> locus having lost its mating-type role. We found the <i>mip1</i> and <i>β-fg</i> genes flanking the <i>HD</i> genes as in several Agaricomycetes, two copies of the <i>β-fg</i> gene, an additional <i>HD2</i> copy in the reference genome of <i>A. bisporus</i> var. <i>bisporus</i> and an additional <i>HD1</i> copy in the reference genome of <i>A. bisporus</i> var. <i>burnettii.</i> We detected a 140 kb-long inversion between mating types in an <i>A. bisporus</i> var. <i>burnettii</i> heterokaryon, trapping the <i>HD</i> genes, the <i>mip1</i> gene and fragments of additional genes. The two varieties had islands of transposable elements at the mating-type locus, spanning 35 kb in the <i>A. bisporus</i> var. <i>burnettii</i> reference genome. Linkage analyses showed a region with low recombination in the mating-type locus region in the <i>A. bisporus</i> var. <i>burnettii</i> variety. We found high differentiation between <i>β-fg</i> alleles in both varieties, indicating an ancient event of recombination suppression, followed more recently by a suppression of recombination at the <i>mip1</i> gene through the inversion in <i>A. bisporus</i> var. <i>burnettii</i> and a suppression of recombination across whole chromosomes in <i>A. bisporus</i> var. <i>bisporus</i>, constituting stepwise recombination suppression as in many other mating-type chromosomes and sex chromosomes.
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spelling doaj.art-285f2958e6e649498cc10cc9ad19d90f2023-11-22T03:51:17ZengMDPI AGGenes2073-44252021-07-01127107910.3390/genes12071079Mating-Type Locus Organization and Mating-Type Chromosome Differentiation in the Bipolar Edible Button Mushroom <i>Agaricus bisporus</i>Marie Foulongne-Oriol0Ozgur Taskent1Ursula Kües2Anton S. M. Sonnenberg3Arend F. van Peer4Tatiana Giraud5INRAE, MycSA, Mycologie et Sécurité des Aliments, 33882 Villenave d’Ornon, FranceEcologie Systématique Evolution, Bâtiment 360, CNRS, AgroParisTech, Université Paris-Saclay, 91400 Orsay, FranceMolecular Wood Biotechnology and Technical Mycology, Goettingen Center for Molecular Biosciences (GZMB), Büsgen-Institute, University of Goettingen, Büsgenweg 2, 37077 Goettingen, GermanyPlant Breeding, Wageningen University and Research, Droevendaalsesteeg 1, 6708 PB Wageningen, The NetherlandsPlant Breeding, Wageningen University and Research, Droevendaalsesteeg 1, 6708 PB Wageningen, The NetherlandsEcologie Systématique Evolution, Bâtiment 360, CNRS, AgroParisTech, Université Paris-Saclay, 91400 Orsay, FranceIn heterothallic basidiomycete fungi, sexual compatibility is restricted by mating types, typically controlled by two loci: <i>PR</i>, encoding pheromone precursors and pheromone receptors, and <i>HD</i>, encoding two types of homeodomain transcription factors. We analysed the single mating-type locus of the commercial button mushroom variety, <i>Agaricus bisporus</i> var. <i>bisporus</i>, and of the related variety <i>burnettii</i>. We identified the location of the mating-type locus using genetic map and genome information, corresponding to the <i>HD</i> locus, the <i>PR</i> locus having lost its mating-type role. We found the <i>mip1</i> and <i>β-fg</i> genes flanking the <i>HD</i> genes as in several Agaricomycetes, two copies of the <i>β-fg</i> gene, an additional <i>HD2</i> copy in the reference genome of <i>A. bisporus</i> var. <i>bisporus</i> and an additional <i>HD1</i> copy in the reference genome of <i>A. bisporus</i> var. <i>burnettii.</i> We detected a 140 kb-long inversion between mating types in an <i>A. bisporus</i> var. <i>burnettii</i> heterokaryon, trapping the <i>HD</i> genes, the <i>mip1</i> gene and fragments of additional genes. The two varieties had islands of transposable elements at the mating-type locus, spanning 35 kb in the <i>A. bisporus</i> var. <i>burnettii</i> reference genome. Linkage analyses showed a region with low recombination in the mating-type locus region in the <i>A. bisporus</i> var. <i>burnettii</i> variety. We found high differentiation between <i>β-fg</i> alleles in both varieties, indicating an ancient event of recombination suppression, followed more recently by a suppression of recombination at the <i>mip1</i> gene through the inversion in <i>A. bisporus</i> var. <i>burnettii</i> and a suppression of recombination across whole chromosomes in <i>A. bisporus</i> var. <i>bisporus</i>, constituting stepwise recombination suppression as in many other mating-type chromosomes and sex chromosomes.https://www.mdpi.com/2073-4425/12/7/1079mating-type chromosomemating-type genesbipolartetrapolarpseudo-homothallicheterothallic
spellingShingle Marie Foulongne-Oriol
Ozgur Taskent
Ursula Kües
Anton S. M. Sonnenberg
Arend F. van Peer
Tatiana Giraud
Mating-Type Locus Organization and Mating-Type Chromosome Differentiation in the Bipolar Edible Button Mushroom <i>Agaricus bisporus</i>
Genes
mating-type chromosome
mating-type genes
bipolar
tetrapolar
pseudo-homothallic
heterothallic
title Mating-Type Locus Organization and Mating-Type Chromosome Differentiation in the Bipolar Edible Button Mushroom <i>Agaricus bisporus</i>
title_full Mating-Type Locus Organization and Mating-Type Chromosome Differentiation in the Bipolar Edible Button Mushroom <i>Agaricus bisporus</i>
title_fullStr Mating-Type Locus Organization and Mating-Type Chromosome Differentiation in the Bipolar Edible Button Mushroom <i>Agaricus bisporus</i>
title_full_unstemmed Mating-Type Locus Organization and Mating-Type Chromosome Differentiation in the Bipolar Edible Button Mushroom <i>Agaricus bisporus</i>
title_short Mating-Type Locus Organization and Mating-Type Chromosome Differentiation in the Bipolar Edible Button Mushroom <i>Agaricus bisporus</i>
title_sort mating type locus organization and mating type chromosome differentiation in the bipolar edible button mushroom i agaricus bisporus i
topic mating-type chromosome
mating-type genes
bipolar
tetrapolar
pseudo-homothallic
heterothallic
url https://www.mdpi.com/2073-4425/12/7/1079
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