A constitutively active G-protein-coupled receptor causes mating self-compatibility in the mushroom Coprinus

Olesnicky, Natalie S.; Brown, Andrew J.; Dowell, Simon J.; Casselton, Lorna A.

doi:10.1093/emboj/18.10.2756

Cited by 106 publications

(102 citation statements)

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“…Only two of the three pheromone genes show a significant match with any published pheromone sequences (supplemental Table 2 at http://www.genetics.org/supplemental/), but all proteins were predicted as probable ORFs or exons using the GeneMark algorithm (Borodovsky and McIninch 1993). Olesnicky et al (1999) suggested that the conserved ER motif located 11 amino acids N-terminal to the modified cysteine of pheromone protein phb2.2 of C. cinereus was likely to have a functional role in peptide processing. All three putative C. disseminatus pheromones display this pair of amino acids in the positions homologous to the ER motif in C. cinereus phb2.2 and other homobasidiomycete pheromones (Fowler et al 2001;Riquelme et al 2005).…”

Section: Resultsmentioning

confidence: 99%

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confidence: 99%

“…The nature of the self-compatible mutant mating types of C. cinerea and S. commune has been investigated by DNA sequencing (Olesnicky et al 1999(Olesnicky et al , 2000Fowler et al 2001). Self-compatible mutants of the B mating type of C. cinerea were created by single amino acid substitutions in the pheromone receptors that caused either illegitimate interactions with homoallelic pheromone or constitutive activation of the B pathway (Olesnicky et al 1999(Olesnicky et al , 2000. For the A mating-type locus of C. cinerea, two primary mutations causing self-compatible phenotypes were investigated and found to be the result of a deletion/recombination event that caused the in-frame fusion of HD1 and HD2 genes from the same A haplotype but from different subloci (Kü es et al 1994;Pardo et al 1996).…”

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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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Section: Resultsmentioning

confidence: 99%

mentioning

confidence: 99%

mentioning

confidence: 99%

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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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“…Galactosidase activity from the FUS1 and RLM1 reporter genes was determined by a previously described in vivo assay by using chlorophenol red galactopyranoside (CPRG) as the substrate (Olesnicky et al, 1999). Briefly, freshly saturated cultures of the different yeast transformants were diluted into fresh YNBD media (OD 600 of 0.02) containing 0.1 M sodium phosphate, pH 7, and 0.1 mg/ml CPRG (Roche Diagnostics, Indianapolis, IN).…”

Section: Measurement Of Lacz Activity In Vivomentioning

confidence: 99%

Oxidative Stress ActivatesFUS1andRLM1Transcription in the YeastSaccharomyces cerevisiaein an Oxidant-dependent Manner

Staleva

Hall

Orlow

2004

MBoC

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Mating in haploid Saccharomyces cerevisiae occurs after activation of the pheromone response pathway. Biochemical components of this pathway are involved in other yeast signal transduction networks. To understand more about the coordination between signaling pathways, we used a "chemical genetic" approach, searching for compounds that would activate the pheromone-responsive gene FUS1 and RLM1, a reporter for the cell integrity pathway. We found that catecholamines (L-3,4-hydroxyphenylalanine [L-dopa], dopamine, adrenaline, and noradrenaline) elevate FUS1 and RLM1 transcription. N-Acetyl-cysteine, a powerful antioxidant in yeast, completely reversed this effect, suggesting that FUS1 and RLM1 activation in response to catecholamines is a result of oxidative stress. The oxidant hydrogen peroxide also was found to activate transcription of an RLM1 reporter. Further genetic analysis combined with immunoblotting revealed that Kss1, one of the mating mitogen-activated protein kinases (MAPKs), and Mpk1, an MAPK of the cell integrity pathway, participated in L-dopa-induced stimulation of FUS1 and RLM1 transcription. We also report that Mpk1 and Hog1, the high osmolarity MAPK, were phosphorylated upon induction by hydrogen peroxide. Together, our results demonstrate that cells respond to oxidative stress via different signal transduction machinery dependent upon the nature of the oxidant. INTRODUCTIONIn the haploid cells of the yeast Saccharomyces cerevisiae, four essential MAPK cascades (Figure 1) respond to different external signals to mediate specific responses. The mating pathway is activated by peptide pheromones and induces cell-cycle arrest and the morphological changes required for mating (Elion, 1998;Gustin et al., 1998). The invasive growth pathway is activated by starvation and induces foraging into the agar substratum. The high osmolarity glycerol (HOG) pathway increases intracellular glycerol levels in response to hypertonic stress, whereas the cell integrity pathway is activated by hypotonic stress, heat shock, or impaired cell wall synthesis. Recently, an additional MAPK cascade has been described: the Kss1 vegetative growth pathway (Lee and Elion, 1999). The Kss1 pathway may be activated by cell wall stress or changes in osmolarity (Cullen et al., 2000).The mating pathway is the most studied cellular response to an external signal. As a relatively simple G protein-coupled cascade, it is a widely used model to study mammalian G protein-coupled receptors. The mating cascade includes pheromone receptors (Ste2 and Ste3), G proteins (Gpa1, Ste4, and Ste18), the p21 activating protein kinase Ste20, a mitogen-activated protein kinase kinase kinase (MAPKKK) Ste11, a mitogen-activated protein kinase kinase (MAPKK) Ste7, a scaffolding protein Ste5 and two MAPKs (Fus3 and Kss1) (Gustin et al., 1998;Madhani and Fink, 1998;Farley et al., 1999). Targets of the terminal MAPK include Ste12, a factor required for transcription of pheromone-responsive genes, and Far1, a bifunctional protein required for polarization and G1...

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“…clamps cells and clamp cell fusion; Kües et al 1992, 1994a,c, Badalyan et al 2004), the A mating type genes were shown to induce hyphal knot and primordia development ) and the B mating type genes to support the A mating type genes in initiation of fruiting body development and to act in fruiting body maturation at the stage of karyogamy (Kües et al 2002b). Therefore not surprisingly, certain mutations in the mating type loci (Kües et al 1994b, Pardo et al 1996, Olesnicky et al 1999, Srivilai et al 2006b) make fruiting body development independent from dikaryon formation (Swamy et al 1984). Basidiospores with such mutations germinate into a self-compatible, fertile mycelium with a dikaryon-like appearance: it has clamp cells at the hyphal septa and often two haploid nuclei in the hyphal cells -since these nuclei are genetic identical, the self-compatible mycelium is called a homokaryon: Also like the dikaryon, under appropriate environmental conditions fruiting bodies develop on the homokaryotic mycelium (Fig.…”

Section: Genetic Access Of Fruiting Body Developmentmentioning

confidence: 99%

Wood production, wood technology, and biotechnological impacts

Kües¹

2007

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A constitutively active G-protein-coupled receptor causes mating self-compatibility in the mushroom Coprinus

Cited by 106 publications

References 55 publications

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

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

Oxidative Stress ActivatesFUS1andRLM1Transcription in the YeastSaccharomyces cerevisiaein an Oxidant-dependent Manner

Wood production, wood technology, and biotechnological impacts

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