Secondary mutations at the Bβ incompatibility locus of Schizophyllum

Raper, John R.; Raudaskoski, Marjatta

doi:10.1038/hdy.1968.9

Cited by 34 publications

(16 citation statements)

References 13 publications

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“…Such "primary" mutations to self-compatibility of the MAT-B genes have long been known in the model species S. commune and C. cinerea (26,63) and have more recently been shown to be constitutively activating G protein-coupled receptors (58). Of special interest to the present study, many of the secondary mutations that restored self-incompatibility in the primary mutant background created alleles that conferred a unilateral nuclear migration phenotype (66,67), as observed in many of the P. chrysosporium crosses. Control of nuclear migration in bipolar Agaricomycetes.…”

Section: Discussionmentioning

confidence: 90%

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: Discussionmentioning

confidence: 90%

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 formation of pseudoclamps is a phenomenon which has been observed earlier in semicompatible mating interactions (A Bϭ), where nuclei enter the hyphae of the mating partner only at the fusion point. This results in the formation of some pseudoclamps and the death of hyphae in the fusion area (53). In contrast to these bona fide semicompatible mating interactions, the formation of pseudoclamps in mated bar2f and bar2t receptor transformants occurs throughout the colony, with higher occurrence in the latter.…”

Section: Discussionmentioning

confidence: 99%

“…The A loci encode homeodomain transcription factors, while the B loci code for multiallelic pheromone receptors and pheromones (55,63,66). Both the A and B pathways can be activated by the combination of different allelic specificities in at least one sublocus derived from each of the two mates (46,52,53). Thus, for a compatible mating interaction to occur, different A and B mating types (A B ) in the partners are essential.…”

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Transcriptome and Functional Analysis of Mating in the Basidiomycete Schizophyllum commune

et al. 2012

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In this study, we undertook a functional characterization and transcriptome analysis that enabled a comprehensive study of the mating type loci of the mushroom Schizophyllum commune. Induced expression of both the bar2 receptor and the bap2(2) pheromone gene within 6 to 12 h after mates' contact was demonstrated by quantitative real-time PCR. Similar temporal expression patterns were confirmed for the allelic bbr1 receptor and bbp1 pheromone-encoding genes by Northern hybridization. Interestingly, the fusion of clamp connections to the subterminal cell was delayed in mating interactions in which one of the compatible partners expressed the bar2 receptor with a truncated C terminus. This developmental delay allowed the visualization of a green fluorescent protein (Gfp)-labeled truncated receptor at the cell periphery, consistent with a localization in the plasma membrane of unfused pseudoclamps. This finding does not support hypotheses envisioning a receptor localization to the nuclear membrane facilitating recognition between the two different nuclei present in each dikaryotic cell. Rather, Gfp fluorescence observed in such pseudoclamps indicated a role of receptor-pheromone interaction in clamp fusion. Transcriptome changes associated with mating interactions were analyzed in order to identify a role for pheromone-receptor interactions. We detected a total of 89 genes that were transcriptionally regulated in a mating type locus A-dependent manner, employing a cutoff of 5-fold changes in transcript abundance. Upregulation in cell cycle-related genes and downregulation of genes involved in metabolism were seen with this set of experiments. In contrast, mating type locus B-dependent transcriptome changes were observed in 208 genes, with a specific impact on genes related to cell wall and membrane metabolism, stress response, and the redox status of the cell.T he filamentous fungus Schizophyllum commune is a widely distributed mushroom that lives saprophytically and can cause white rot on wood. It has been extensively used to study mating interactions for almost 100 years (47). In addition to studies involving the mushroom Coprinopsis cinerea and the corn smut Ustilago maydis, the mating type genes have been extensively analyzed for this tetrapolar basidiomycete (4, 29). The recent publication of the S. commune genome sequence enables global expression analyses (41). During the life cycle of this fungus, compatible haploid monokaryons can mate to produce a fertile dikaryon with two nuclei per cell, one derived from each mating partner. Under appropriate environmental conditions, the dikaryon is able to form the sexual reproductive fruiting bodies (40). While the fusion of two monokaryotic hyphae (plasmogamy) is independent of mating types, specific steps of sexual development are regulated by the mating type genes encoded in the loci A and B (25, 47). For each of these loci, two linked, multiallelic subloci (termed ␣ and ␤) have been determined by recombination analyses (27,49,51,65). The A loci encode homeodomain ...

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“…The most complex structure so far found is for the B␤2 allele, which codes for one receptor and eight pheromones, with three more pheromones probable from the genomic sequence (22). The B␤2 allele was of special interest due to the numerous primary and secondary mutations that had been induced earlier to show that reversion of tetrapolar to bipolar mating systems is possible and indicating multiple genes responsible for B mating type function (76,81,82). The primary mutations were screened for induction of B-regulated development, thus rendering the mutant functionally bipolar and indicating constitutive signaling without mating (76).…”

Section: Molecular Structure Of B Mating Type Genesmentioning

confidence: 99%

“…The primary mutations were screened for induction of B-regulated development, thus rendering the mutant functionally bipolar and indicating constitutive signaling without mating (76). Secondary mutations were then induced, suppressing the constitutive phenotype and returning phenotypically to a nonconstitutive situation not exactly the same as that of the wild type but associated with loss of some specificity in tetrapolar mating interactions (81,82). It was expected that the primary mutations should be in the receptor gene, rendering it constitutively active or responsive to (some) self-pheromones.…”

Section: Molecular Structure Of B 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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Secondary mutations at the Bβ incompatibility locus of Schizophyllum

Cited by 34 publications

References 13 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

Transcriptome and Functional Analysis of Mating in the Basidiomycete Schizophyllum commune

Basidiomycete Mating Type Genes and Pheromone Signaling

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