Genomic structure of the A mating-type locus in a bipolar basidiomycete, Pholiota nameko

Yi, Ruirong; Tachikawa, Takashi; Ishikawa, Mariko; Mukaiyama, Hiroyuki; Bao, Dapeng; Aimi, Tadanori

doi:10.1016/j.mycres.2008.11.002

Cited by 29 publications

(22 citation statements)

References 36 publications

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“…Genes homologous to the MAT-A homeodomain genes were found on scaffold 13, positions 1.071 to 1.074 Mb. The MAT-A locus is comprised of one HD1 gene and one HD2 gene in a divergently transcribed orientation, as has been observed in other agaricomycete MAT-A loci (37,56,84). The MAT-A region of P. chrysosporium displays extensive synteny across Agaricomycetes, a subset of which are shown in Fig.…”

Section: Resultsmentioning

confidence: 61%

“…This strain was excluded from further analyses. Several measures of polymorphism were calculated for the STE3 genes and compared to the EF1␣ locus (a non-mating-type-specific gene on scaffold 11 [ Table 2 (35,84). The black arrows indicate the actual mating-type-specific homeodomain genes of the two classes of DNA binding motifs (HD1 and HD2 [44]).…”

Section: Resultsmentioning

confidence: 99%

“…Much less functional information is available for mating-type loci in bipolar species. For at least two species, it appears that the single mating-type locus in these species encodes only the MAT-A homologues, yet MAT-B homologues are still present in the genome (37,84). Heterologous expression of a pheromone receptor from the bipolar species Coprinellus disseminatus in C. cinerea demonstrated that the protein was still able to function in clamp connection fusion and the completion of the sexual cycle (37).…”

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A Single Mating-Type Locus Composed of Homeodomain Genes Promotes Nuclear Migration and Heterokaryosis in the White-Rot Fungus Phanerochaete chrysosporium

2011

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The white-rot basidiomycete fungus Phanerochaete chrysosporium (Agaricomycetes) is a model species that produces potent wood-degrading enzymes. The mating system of the species has been difficult to characterize due to its cryptic fruiting habit and lack of clamp connections in the heterokaryotic phase. By exploiting the draft genome sequence, we reevaluated the mating system of P. chrysosporium by studying the inheritance and segregation of putative mating-type gene homologues, the homeodomain transcription factor genes (MAT-A) and the pheromone receptors (MAT-B). A pattern of mating incompatibility and fructification consistent with a bipolar system with a single MAT locus was observed, but the rejection response was much weaker than that seen in other agaricomycete species, leading to stable heterokaryons with identical MAT alleles. The homeodomain genes appear to comprise the single MAT locus because they are heterozygous in wild strains and hyperpolymorphic at the DNA sequence level and promote aspects of sexual reproduction, such as nuclear migration, heterokaryon stability, and basidiospore formation. The pheromone receptor loci that might constitute a MAT-B locus, as in many other Agaricomycetes, are not linked to the MAT-A locus and display low levels of polymorphism. This observation is inconsistent with a bipolar mating system that includes pheromones and pheromone receptors as mating-type determinants. The partial uncoupling of nuclear migration and mating incompatibility in this species may be predicted to lead to parasexual recombination and may have contributed to the homothallic behavior observed in previous studies.The mushroom-forming fungi, Agaricomycetes (Basidiomycota), have a mating system in which compatible haploid mycelia (homokaryons) exchange nuclei to form mated mycelia (heterokaryons) that are comprised of cells with two compatible nuclear types (mating types). Once mated, heterokaryons function as genetic diploids, but the two nuclear types divide together in an unfused state until karyogamy occurs in the basidial cells of the fruiting body immediately prior to meiosis and spore formation. In the model mushroom species (e.g., Coprinopsis cinerea and Schizophyllum commune), heterokaryons are termed dikaryons because each cell contains exactly two nuclei, but in a large number of Agaricomycetes species (e.g., 20 to 30% of the nongilled forms [10]), the hyphal cells of heterokaryons are multinucleate. In these fungi (variously termed multinucleate, plurinucleate, or holocenocytic), each cell presumably contains both mating types but a variable number of nuclei per cell, for example, up to 12 nuclei per cell were observed in the termite symbiont Termitomyces (15) and as many as 69 per cell in Wolfiporia extensa (34).In dikaryotic fungi, differentiating homokaryotic from heterokaryotic phases is readily accomplished by observing the characteristic clamp connections or hook cells that function in the maintenance of the binucleate state (43). In contrast, species with multinucleate heterok...

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Section: Resultsmentioning

confidence: 61%

Section: Resultsmentioning

confidence: 99%

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confidence: 99%

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A Single Mating-Type Locus Composed of Homeodomain Genes Promotes Nuclear Migration and Heterokaryosis in the White-Rot Fungus Phanerochaete chrysosporium

2011

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“…The HD1 and HD2 proteins of L. bicolor have the same conserved motifs identified in corresponding proteins of C. cinerea, suggesting functional similarity. Only one pair of homeodomain genes was also detected in the tetrapolar oyster mushroom, Pleurotus djamor (40), and in the A mating type locus of bipolar Pholiota nameko (122). Another bipolar species, Coprinellus disseminatus, contains multiallelic A␣ and A␤ loci, each locus with an HD1 and an HD2 protein-encoding gene (41).…”

Section: Molecular Structure Of a Mating Type Genesmentioning

confidence: 99%

Basidiomycete Mating Type Genes and Pheromone Signaling

2010

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2The genome sequences of the basidiomycete Agaricomycetes species Coprinopsis cinerea, Laccaria bicolor, Schizophyllum commune, Phanerochaete chrysosporium, and Postia placenta, as well as of Cryptococcus neoformans and Ustilago maydis, are now publicly available. Out of these fungi, C. cinerea, S. commune, and U. maydis, together with the budding yeast Saccharomyces cerevisiae, have been investigated for years genetically and molecularly for signaling in sexual reproduction. The comparison of the structure and organization of mating type genes in fungal genomes reveals an amazing conservation of genes regulating the sexual reproduction throughout the fungal kingdom. In agaricomycetes, two mating type loci, A, coding for homeodomain type transcription factors, and B, encoding a pheromone/receptor system, regulate the four typical mating interactions of tetrapolar species. Evidence for both A and B mating type genes can also be identified in basidiomycetes with bipolar systems, where only two mating interactions are seen. In some of these fungi, the B locus has lost its self/nonself discrimination ability and thus its specificity while retaining the other regulatory functions in development. In silico analyses now also permit the identification of putative components of the pheromone-dependent signaling pathways. Induction of these signaling cascades leads to development of dikaryotic mycelia, fruiting body formation, and meiotic spore production. In pheromone-dependent signaling, the role of heterotrimeric G proteins, components of a mitogen-activated protein kinase (MAPK) cascade, and cyclic AMP-dependent pathways can now be defined. Additionally, the pheromone-dependent signaling through monomeric, small GTPases potentially involved in creating the polarized cytoskeleton for reciprocal nuclear exchange and migration during mating is predicted. THE MATING SYSTEMS IN BASIDIOMYCETESThe typical life cycle of the higher basidiomycetes, presently classified as Agaricomycetes (Table 1) (34), consists of haploid, monokaryotic as well as dikaryotic stages, the latter of which prevails in nature. The monokaryotic mycelium contains nuclei of only one genetic type and is thus termed homokaryon. This mycelium, grown from haploid spores, in general contains one nucleus per cell (Fig. 1). The dikaryon is formed when genetically different homokaryons mate. In the saprotrophic agaricomycetes, the mushroom-forming species Schizophyllum commune and Coprinopsis cinerea (Table 1), mating is regulated by a tetrapolar system consisting of two unlinked genetic complexes, named A and B. The term tetrapolar reflects the fact that there are four possible mating interactions scored in matings between haploid strains derived from spores formed on the fruiting bodies of same parent dikaryon: a fully compatible interaction occurs when both A and B between the mates are of different specificities (Fig. 1), an incompatible interaction occurs when allelic specificities are all the same, and two semicompatible interactions occur when either A-o...

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“…However, much of what is known about bipolarity in these species emphasizes that these bipolar states have most likely arisen from a tetrapolar configuration. This can be attained either by (i) loss of function of the P/R locus as an incompatibility factor (as, e.g., in Coprinus disseminatus, Pholiota microspore, and Phanerochaete chrysosporium) (Raper 1966;James et al 2006James et al , 2011Yi et al 2009) or (ii) coalescence of unlinked P/R and HD loci into a contiguous inheritable unit, with both MAT genes remaining functional in mating-type determination. This last scenario was shown to be at the basis of extant bipolar species belonging to two of the three major Basidiomycota lineages, namely Cryptococcus neoformans (subphylum Agaricomycotina) Findley et al 2012) and Ustilago hordei (subphylum Ustilaginomycotina) (Bakkeren et al 2006).…”

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Evolution of Mating Systems in Basidiomycetes and the Genetic Architecture Underlying Mating-Type Determination in the YeastLeucosporidium scottii

et al. 2015

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In most fungi, sexual reproduction is bipolar; that is, two alternate sets of genes at a single mating-type (MAT) locus determine two mating types. However, in the Basidiomycota, a unique (tetrapolar) reproductive system emerged in which sexual identity is governed by two unlinked MAT loci, each of which controls independent mechanisms of self/nonself recognition. Tetrapolar-to-bipolar transitions have occurred on multiple occasions in the Basidiomycota, resulting, for example, from linkage of the two MAT loci into a single inheritable unit. Nevertheless, owing to the scarcity of molecular data regarding tetrapolar systems in the earliest-branching lineage of the Basidiomycota (subphylum Pucciniomycotina), it is presently unclear if the last common ancestor was tetrapolar or bipolar. Here, we address this question, by investigating the mating system of the Pucciniomycotina yeast Leucosporidium scottii. Using whole-genome sequencing and chromoblot analysis, we discovered that sexual reproduction is governed by two physically unlinked gene clusters: a multiallelic homeodomain (HD) locus and a pheromone/receptor (P/R) locus that is biallelic, thereby dismissing the existence of a third P/R allele as proposed earlier. Allele distribution of both MAT genes in natural populations showed that the two loci were in strong linkage disequilibrium, but independent assortment of MAT alleles was observed in the meiotic progeny of a test cross. The sexual cycle produces fertile progeny with similar proportions of the four mating types, but approximately 2/3 of the progeny was found to be nonhaploid. Our study adds to others in reinforcing tetrapolarity as the ancestral state of all basidiomycetes.KEYWORDS sexual reproduction; mating type; mating-type determination; fungi; Basidiomycota S EXUAL reproduction has a pivotal role in the biology of many eukaryotes and is likely a defining evolutionary innovation of this lineage (Dacks and Roger 1999;Goodenough and Heitman 2014). In addition to promoting genetic variation, required for adaptation to fluctuating environments and longterm survival, sexual reproduction in many fungal species, in particular, has a central role in pathogenic development (Bakkeren et al. 2008;Nadal et al. 2008;Heitman 2010;Heitman et al. 2014). It is thus not surprising that recent advances in genome sequencing have revealed that most fungal species have retained the machinery for sexual reproduction and meiosis (Halary et al. 2011;Dyer and O'Gorman 2012;Gioti et al. 2013;Heitman et al. 2014). However, this resilience to keep sexual competence intact comes with an extremely dynamic evolution of sexual behaviors and mating type-determining mechanisms, which may influence important evolutionary and ecological processes, such as adaptation and speciation (Billiard et al. 2011;Heitman et al. 2013;Nieuwenhuis et al. 2013).In the phylum Basidiomycota, sexual reproduction is often dictated by two independent sets of mating-type (MAT)-specific genes that control different stages of the sexual cycle. These...

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Genomic structure of the A mating-type locus in a bipolar basidiomycete, Pholiota nameko

Cited by 29 publications

References 36 publications

A Single Mating-Type Locus Composed of Homeodomain Genes Promotes Nuclear Migration and Heterokaryosis in the White-Rot Fungus Phanerochaete chrysosporium

A Single Mating-Type Locus Composed of Homeodomain Genes Promotes Nuclear Migration and Heterokaryosis in the White-Rot Fungus Phanerochaete chrysosporium

Basidiomycete Mating Type Genes and Pheromone Signaling

Evolution of Mating Systems in Basidiomycetes and the Genetic Architecture Underlying Mating-Type Determination in the YeastLeucosporidium scottii

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