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Light controls growth and development via a conserved pathway in the fungal kingdom.

Idnurm A, Heitman J - PLoS Biol. (2005)

Bottom Line: One UV-sensitive mutant that filaments equally well in the light and the dark was identified and found to have an insertion in the BWC2 gene, whose product is structurally similar to N. crassa WC-2.Deletion of BWC1 or BWC2 reduces the virulence of C. neoformans in a murine model of infection; the Bwc1-Bwc2 system thus represents a novel protein complex that influences both development and virulence in a pathogenic fungus.These results demonstrate that a role for blue/UV light in controlling development is an ancient process that predates the divergence of the fungi into the ascomycete and basidiomycete phyla.

View Article: PubMed Central - PubMed

Affiliation: Department of Molecular Genetics and Microbiology, Howard Hughes Medical Institute, Duke University Medical Center, Durham, North Carolina, USA.

ABSTRACT
Light inhibits mating and haploid fruiting of the human fungal pathogen Cryptococcus neoformans, but the mechanisms involved were unknown. Two genes controlling light responses were discovered through candidate gene and insertional mutagenesis approaches. Deletion of candidate genes encoding a predicted opsin or phytochrome had no effect on mating, while strains mutated in the white collar 1 homolog gene BWC1 mated equally well in the light or the dark. The predicted Bwc1 protein shares identity with Neurospora crassa WC-1, but lacks the zinc finger DNA binding domain. BWC1 regulates cell fusion and repression of hyphal development after fusion in response to blue light. In addition, bwc1 mutant strains are hypersensitive to ultraviolet light. To identify other components required for responses to light, a novel self-fertile haploid strain was created and subjected to Agrobacterium-mediated insertional mutagenesis. One UV-sensitive mutant that filaments equally well in the light and the dark was identified and found to have an insertion in the BWC2 gene, whose product is structurally similar to N. crassa WC-2. The C. neoformans Bwc1 and Bwc2 proteins interact in the yeast two-hybrid assay. Deletion of BWC1 or BWC2 reduces the virulence of C. neoformans in a murine model of infection; the Bwc1-Bwc2 system thus represents a novel protein complex that influences both development and virulence in a pathogenic fungus. These results demonstrate that a role for blue/UV light in controlling development is an ancient process that predates the divergence of the fungi into the ascomycete and basidiomycete phyla.

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Ascomycete White Collar 1 Homologs Contain a Zinc Finger Domain; The Basidiomycete Homologs Do NotComparison of the structure of the predicted WC-1 proteins from the ascomycetes N. crassa (Nc), Aspergillus nidulans (An), Magnaporthe grisea (Mg), Fusarium graminarium (Fg), and Tubor borchii (Tb), and the basidiomycetes C. neoformans (Cn), Coprinus cinereus (Cc), Ustilago maydis (Um), and Phanerochaete chrysosporium (Pc). Other domains are PAS (PER, ARNT, SIM) and NLS (nuclear localization signal), and the specialized PAS domain that interacts with the chromophore FAD is marked. Sequences are from GenBank (Nc, X94300; An, AF515628; Tb, AJ575416), the Broad Institute (Mg, Cn, Fg, Cc, Um), or the Department of Energy (Pc).
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pbio-0030095-g004: Ascomycete White Collar 1 Homologs Contain a Zinc Finger Domain; The Basidiomycete Homologs Do NotComparison of the structure of the predicted WC-1 proteins from the ascomycetes N. crassa (Nc), Aspergillus nidulans (An), Magnaporthe grisea (Mg), Fusarium graminarium (Fg), and Tubor borchii (Tb), and the basidiomycetes C. neoformans (Cn), Coprinus cinereus (Cc), Ustilago maydis (Um), and Phanerochaete chrysosporium (Pc). Other domains are PAS (PER, ARNT, SIM) and NLS (nuclear localization signal), and the specialized PAS domain that interacts with the chromophore FAD is marked. Sequences are from GenBank (Nc, X94300; An, AF515628; Tb, AJ575416), the Broad Institute (Mg, Cn, Fg, Cc, Um), or the Department of Energy (Pc).

Mentions: In contrast to the N. crassa WC-1 protein, the predicted C. neoformans Bwc1 protein has no zinc finger DNA binding domain or any other known DNA binding motif. Matches to wc-1 were obtained from other fungi and the predicted proteins examined for these domains (Figure 4). The proteins share a similar structure with regard to the PAS domains, and all of the ascomycete wc-1 genes examined contained a zinc finger DNA binding domain, whereas none of the basidiomycete wc-1 homologs encode products with this domain. This suggests that the structural differences between the homologs are conserved in each phylum and are not unique to C. neoformans.


Light controls growth and development via a conserved pathway in the fungal kingdom.

Idnurm A, Heitman J - PLoS Biol. (2005)

Ascomycete White Collar 1 Homologs Contain a Zinc Finger Domain; The Basidiomycete Homologs Do NotComparison of the structure of the predicted WC-1 proteins from the ascomycetes N. crassa (Nc), Aspergillus nidulans (An), Magnaporthe grisea (Mg), Fusarium graminarium (Fg), and Tubor borchii (Tb), and the basidiomycetes C. neoformans (Cn), Coprinus cinereus (Cc), Ustilago maydis (Um), and Phanerochaete chrysosporium (Pc). Other domains are PAS (PER, ARNT, SIM) and NLS (nuclear localization signal), and the specialized PAS domain that interacts with the chromophore FAD is marked. Sequences are from GenBank (Nc, X94300; An, AF515628; Tb, AJ575416), the Broad Institute (Mg, Cn, Fg, Cc, Um), or the Department of Energy (Pc).
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC1064852&req=5

pbio-0030095-g004: Ascomycete White Collar 1 Homologs Contain a Zinc Finger Domain; The Basidiomycete Homologs Do NotComparison of the structure of the predicted WC-1 proteins from the ascomycetes N. crassa (Nc), Aspergillus nidulans (An), Magnaporthe grisea (Mg), Fusarium graminarium (Fg), and Tubor borchii (Tb), and the basidiomycetes C. neoformans (Cn), Coprinus cinereus (Cc), Ustilago maydis (Um), and Phanerochaete chrysosporium (Pc). Other domains are PAS (PER, ARNT, SIM) and NLS (nuclear localization signal), and the specialized PAS domain that interacts with the chromophore FAD is marked. Sequences are from GenBank (Nc, X94300; An, AF515628; Tb, AJ575416), the Broad Institute (Mg, Cn, Fg, Cc, Um), or the Department of Energy (Pc).
Mentions: In contrast to the N. crassa WC-1 protein, the predicted C. neoformans Bwc1 protein has no zinc finger DNA binding domain or any other known DNA binding motif. Matches to wc-1 were obtained from other fungi and the predicted proteins examined for these domains (Figure 4). The proteins share a similar structure with regard to the PAS domains, and all of the ascomycete wc-1 genes examined contained a zinc finger DNA binding domain, whereas none of the basidiomycete wc-1 homologs encode products with this domain. This suggests that the structural differences between the homologs are conserved in each phylum and are not unique to C. neoformans.

Bottom Line: One UV-sensitive mutant that filaments equally well in the light and the dark was identified and found to have an insertion in the BWC2 gene, whose product is structurally similar to N. crassa WC-2.Deletion of BWC1 or BWC2 reduces the virulence of C. neoformans in a murine model of infection; the Bwc1-Bwc2 system thus represents a novel protein complex that influences both development and virulence in a pathogenic fungus.These results demonstrate that a role for blue/UV light in controlling development is an ancient process that predates the divergence of the fungi into the ascomycete and basidiomycete phyla.

View Article: PubMed Central - PubMed

Affiliation: Department of Molecular Genetics and Microbiology, Howard Hughes Medical Institute, Duke University Medical Center, Durham, North Carolina, USA.

ABSTRACT
Light inhibits mating and haploid fruiting of the human fungal pathogen Cryptococcus neoformans, but the mechanisms involved were unknown. Two genes controlling light responses were discovered through candidate gene and insertional mutagenesis approaches. Deletion of candidate genes encoding a predicted opsin or phytochrome had no effect on mating, while strains mutated in the white collar 1 homolog gene BWC1 mated equally well in the light or the dark. The predicted Bwc1 protein shares identity with Neurospora crassa WC-1, but lacks the zinc finger DNA binding domain. BWC1 regulates cell fusion and repression of hyphal development after fusion in response to blue light. In addition, bwc1 mutant strains are hypersensitive to ultraviolet light. To identify other components required for responses to light, a novel self-fertile haploid strain was created and subjected to Agrobacterium-mediated insertional mutagenesis. One UV-sensitive mutant that filaments equally well in the light and the dark was identified and found to have an insertion in the BWC2 gene, whose product is structurally similar to N. crassa WC-2. The C. neoformans Bwc1 and Bwc2 proteins interact in the yeast two-hybrid assay. Deletion of BWC1 or BWC2 reduces the virulence of C. neoformans in a murine model of infection; the Bwc1-Bwc2 system thus represents a novel protein complex that influences both development and virulence in a pathogenic fungus. These results demonstrate that a role for blue/UV light in controlling development is an ancient process that predates the divergence of the fungi into the ascomycete and basidiomycete phyla.

Show MeSH
Related in: MedlinePlus