Positioning of Nuclei in the Secondary Mycelium ofSchizophyllum communein Relation to Differential Gene Expression

Schuurs, Theo A.; Dalstra, H.J.P.; Scheer, José M. J.; Wessels, J. G. H.

doi:10.1006/fgbi.1997.1028

Cited by 59 publications

(49 citation statements)

References 37 publications

(35 reference statements)

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“…In this study, the pheromone receptor was visualized at the cell periphery, consistent with a localization in the plasma membrane. No evidence of nuclear membrane localization, as has been proposed in some previous hypotheses, was found (5,60). Another prediction of these models was that pheromone receptors would be expected to be localized in the plasma membrane close to the encoding nucleus by virtue of localized expression and incorporation.…”

Section: Discussionmentioning

confidence: 87%

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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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Section: Discussionmentioning

confidence: 87%

“…Under this model, productive interaction between non-self-pheromones and their cognate receptor occurs only when the nuclei are in close proximity to each other (60). Another hypothesis (5) proposed that receptor localization to the nuclear envelope was necessary for detection of intracellular pheromone(s).…”

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confidence: 99%

Transcriptome and Functional Analysis of Mating in the Basidiomycete Schizophyllum commune

et al. 2012

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“…These MAT-B processes, as understood from the model mushroom species, appear to involve nuclear migration and clamp cell fusion (11), as well as nuclear positioning and heterokaryon stability (73). Expression of the nonmating-type-specific MAT-B homologues of the bipolar mushroom C. disseminatus in a heterologous species showed that these pheromone receptors were still able to drive clamp cell fusion and to complete the sexual cycle (37).…”

Section: Discussionmentioning

confidence: 99%

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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“…The homobasidiomycete pheromone/receptor systems are also possibly unique because these proteins have not been detected extracellularly (Brown and Casselton 2001). It has been suggested that the pheromone/receptor system of mushroom fungi functions in the recognition between the two compatible nuclei of the dikaryotic cell (Schuurs et al 1998;Debuchy 1999). This function may be indispensable and an intact pheromone/receptor system might be required for proper dikaryon maintenance in all species, bipolar or tetrapolar.…”

Section: Discussionmentioning

confidence: 99%

Evolution of the Bipolar Mating System of the Mushroom Coprinellus disseminatus From Its Tetrapolar Ancestors Involves Loss of Mating-Type-Specific Pheromone Receptor Function

et al. 2006

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Mating incompatibility in mushroom fungi is controlled by the mating-type loci. In tetrapolar species, two unlinked mating-type loci exist (A and B), whereas in bipolar species there is only one locus. The A and B mating-type loci encode homeodomain transcription factors and pheromones and pheromone receptors, respectively. Most mushroom species have a tetrapolar mating system, but numerous transitions to bipolar mating systems have occurred. Here we determined the genes controlling mating type in the bipolar mushroom Coprinellus disseminatus. Through positional cloning and degenerate PCR, we sequenced both the transcription factor and pheromone receptor mating-type gene homologs from C. disseminatus. Only the transcription factor genes segregate with mating type, discounting the hypothesis of genetic linkage between the A and B mating-type loci as the causal origin of bipolar mating behavior. The mating-type locus of C. disseminatus is similar to the A mating-type locus of the model species Coprinopsis cinerea and encodes two tightly linked pairs of homeodomain transcription factor genes. When transformed into C. cinerea, the C. disseminatus A and B homologs elicited sexual reactions like native matingtype genes. Although mating type in C. disseminatus is controlled by only the transcription factor genes, cellular functions appear to be conserved for both groups of genes. M ATING in fungi is controlled by the loci that determine the mating type of an individual, and only individuals with differing mating types can mate. Basidiomycete fungi have evolved a unique mating system, termed tetrapolar or bifactorial incompatibility, in which mating type is determined by two unlinked loci; compatibility at both loci is required for mating to occur. The origin of the tetrapolar mating system in the basidiomycetes is likely to be ancient since it is observed in at least two of the three major lineages, the Ustilaginomycetes, or smut fungi, and the Hymenomycetes, primarily the mushroom fungi (Burnett 1975). Also unique to the basidiomycetes is the presence of multiple alleles at the mating-type loci that allows most individuals within a population to be mating compatible with one another. Only the mushroom-forming homobasidiomycetes possess large allelic series at both loci, typically termed the A and B mating-type loci (Whitehouse 1949;Raper 1966).The multiallelic tetrapolar mating system is considered to be a novel innovation that could have only evolved once (Raper 1966;Raper and Flexer 1971). For this reason, the ancestor of the homobasidiomycetes is accepted as having a tetrapolar mating system. Although most (65%) of the homobasidiomycetes possess a tetrapolar mating system, many species (25%) instead have a bipolar system controlled by a single locus with multiple alleles (Raper 1966). The distribution of bipolar species is scattered throughout the homobasidiomycete phylogeny, and bipolar species appear to have multiple independent origins from tetrapolar mating systems (Hibbett and Donoghue 2001). The popul...

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Positioning of Nuclei in the Secondary Mycelium ofSchizophyllum communein Relation to Differential Gene Expression

Cited by 59 publications

References 37 publications

Transcriptome and Functional Analysis of Mating in the Basidiomycete Schizophyllum commune

Transcriptome and Functional Analysis of Mating in the Basidiomycete Schizophyllum commune

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

Evolution of the Bipolar Mating System of the Mushroom Coprinellus disseminatus From Its Tetrapolar Ancestors Involves Loss of Mating-Type-Specific Pheromone Receptor Function

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