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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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bwc1 Mutants Are Hypersensitive to UV LightTen-fold serial dilutions of log-phase yeast cells of bwc1 mutant or wild type (WT) were plated in duplicate on YPD medium, and one plate was UV irradiated (~48 mJ/cm2). Reintroduction of a wild-type copy of the BWC1 gene into the bwc1 + BWC1 mutant strain restores UV sensitivity to the wild-type level.
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pbio-0030095-g003: bwc1 Mutants Are Hypersensitive to UV LightTen-fold serial dilutions of log-phase yeast cells of bwc1 mutant or wild type (WT) were plated in duplicate on YPD medium, and one plate was UV irradiated (~48 mJ/cm2). Reintroduction of a wild-type copy of the BWC1 gene into the bwc1 + BWC1 mutant strain restores UV sensitivity to the wild-type level.

Mentions: To search further for a function of OPS1, PHY1, and BWC1, growth of the single- and multiple-mutant strains was examined under a variety of in vitro conditions. The mutations had no effect on previously identified attributes required for virulence in mammalian hosts, such as the production of the pigment melanin or the polysaccharide capsule, or growth at 37 °C (unpublished data). The ops1 and phy1 mutant strains were as sensitive to UV light as wild type, but the bwc1 mutants were markedly hypersensitive to UV light (Figure 3). Reintroduction of a wild-type copy of the BWC1 gene into the bwc1 mutant strain restored a wild-type level of sensitivity to UV light. Based on studies in other organisms, one target gene could be that encoding photolyase. However, there is no evidence for a photolyase in C. neoformans, based on the lack of photoreactivation and the absence of a homolog in genome databases (unpublished data). We conclude that Bwc1 functions in response to blue light to inhibit mating, and to UV light to regulate resistance to UV irradiation.


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

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

bwc1 Mutants Are Hypersensitive to UV LightTen-fold serial dilutions of log-phase yeast cells of bwc1 mutant or wild type (WT) were plated in duplicate on YPD medium, and one plate was UV irradiated (~48 mJ/cm2). Reintroduction of a wild-type copy of the BWC1 gene into the bwc1 + BWC1 mutant strain restores UV sensitivity to the wild-type level.
© Copyright Policy
Related In: Results  -  Collection

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

pbio-0030095-g003: bwc1 Mutants Are Hypersensitive to UV LightTen-fold serial dilutions of log-phase yeast cells of bwc1 mutant or wild type (WT) were plated in duplicate on YPD medium, and one plate was UV irradiated (~48 mJ/cm2). Reintroduction of a wild-type copy of the BWC1 gene into the bwc1 + BWC1 mutant strain restores UV sensitivity to the wild-type level.
Mentions: To search further for a function of OPS1, PHY1, and BWC1, growth of the single- and multiple-mutant strains was examined under a variety of in vitro conditions. The mutations had no effect on previously identified attributes required for virulence in mammalian hosts, such as the production of the pigment melanin or the polysaccharide capsule, or growth at 37 °C (unpublished data). The ops1 and phy1 mutant strains were as sensitive to UV light as wild type, but the bwc1 mutants were markedly hypersensitive to UV light (Figure 3). Reintroduction of a wild-type copy of the BWC1 gene into the bwc1 mutant strain restored a wild-type level of sensitivity to UV light. Based on studies in other organisms, one target gene could be that encoding photolyase. However, there is no evidence for a photolyase in C. neoformans, based on the lack of photoreactivation and the absence of a homolog in genome databases (unpublished data). We conclude that Bwc1 functions in response to blue light to inhibit mating, and to UV light to regulate resistance to UV irradiation.

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