Botrytis cinerea virulence is drastically reduced after disruption of chitin synthase class III gene (Bcchs3a)

Soulié, Marie-Christine; Perino, C.; Piffeteau, Annie; Choquer, Mathias; Malfatti, Pierrette; Cimerman, Agnes; Kunz, Caroline; Boccara, Martine; Vidal-Cros, Anne

doi:10.1111/j.1462-5822.2006.00711.x

Cited by 74 publications

(57 citation statements)

References 50 publications

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“…1B to F, arrowheads). These extracellular structures were similar to those observed in the class III chitin synthase mutant of Botrytis cinerea (40). Vesicles with electron dense contents were frequently seen in ⌬B-18 (Fig.…”

Section: Resultssupporting

confidence: 60%

“…Class III chitin synthases have been reported to be involved in the virulence of some pathogens. Deletion of Bcchs3a in the phytopathogenic fungus Botrytis cinerea and double deletion of WdCHS3 and class I chitin synthase WdCHS2 in the human pathogen Wangiella dermatitidis both caused a reduction of virulence (40,48). On the other hand, the deletion mutant of a class III chitin synthase-encoding gene, CgChsIII, of the maize pathogen Colletotrichum graminicola did not exhibit the significant phenotypic difference from the wild-type strain (50).…”

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confidence: 99%

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Class III Chitin Synthase ChsB of Aspergillus nidulans Localizes at the Sites of Polarized Cell Wall Synthesis and Is Required for Conidial Development

Fukuda¹,

Yamada²,

Deoka³

et al. 2009

Eukaryot Cell

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Class III chitin synthases play important roles in tip growth and conidiation in many filamentous fungi. However, little is known about their functions in those processes. To address these issues, we characterized the deletion mutant of a class III chitin synthase-encoding gene of Aspergillus nidulans, chsB, and investigated ChsB localization in the hyphae and conidiophores. Multilayered cell walls and intrahyphal hyphae were observed in the hyphae of the chsB deletion mutant, and wavy septa were also occasionally observed. ChsB tagged with FLAG or enhanced green fluorescent protein (EGFP) localized mainly at the tips of germ tubes, hyphal tips, and forming septa during hyphal growth. EGFP-ChsB predominantly localized at polarized growth sites and between vesicles and metulae, between metulae and phialides, and between phalides and conidia in asexual development. These results strongly suggest that ChsB functions in the formation of normal cell walls of hyphae, as well as in conidiophore and conidia development in A. nidulans.Chitin, a polymer of ␤-1,4-linked N-acetylglucosmine, is one of the major structural components of the fungal cell wall. Its metabolism, including synthesis, degradation, assembly, and cross-linking to other cell wall components, is thought to be very important for many fungi (5,22,24,36,45). Fungal chitin synthases have been classified into seven groups, classes I to VII, depending on the structures of their conserved regions (6). The genes encoding the synthases belonging to classes III, V, VI, and VII are only found in fungi with high chitin contents in their cell walls. We have identified six chitin synthase genes from Aspergillus nidulans and designated them chsA, chsB, chsC, chsD, csmA, and csmB; these gene products belong to classes II, III, I, IV, V, and VI, respectively (9,13,30,31,44,52). The chsB deletion mutant grew very slowly and formed small colonies with highly branched hyphae, suggesting its important role in hyphal tip growth (3, 52). Repression of chsB expression in the deletion mutant of chsA, chsC, or chsD exaggerated the defects in the formation of aerial hyphae, the production of cell mass, or the growth under high-osmolarity conditions, respectively, compared to each single mutant. These results indicate that chsB functions at various stages of development (15, 16).The deletion of class III chitin synthase-encoding genes leads to severe defects in most of the filamentous fungi thus far investigated. However, their detailed functions are currently unknown. In Neurospora crassa, inactivation of the gene encoding Chs-1, a class III chitin synthase with 63% identity to A. nidulans ChsB, leads to slow growth, aberrant hyphal morphology, and a decrease in chitin synthase activity. The mutant of chs-1 became sensitive to Nikkomycin Z, a chitin synthase inhibitor (53). In Aspergillus fumigatus, two genes encoding class III chitin synthases, chsC and chsG, have been identified. Their gene products showed 66 and 89% identity, respectively, to A. nidulans ChsB. The chsG deletio...

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Section: Resultssupporting

confidence: 60%

mentioning

confidence: 99%

Class III Chitin Synthase ChsB of Aspergillus nidulans Localizes at the Sites of Polarized Cell Wall Synthesis and Is Required for Conidial Development

Fukuda¹,

Yamada²,

Deoka³

et al. 2009

Eukaryot Cell

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“…We cannot exclude the possibility that this effect is due to the impaired cell wall integrity of Bccrz1 mutants, since bmp3 mutants (loss of cell wall integrity MAP kinase) were also defective in mycelium-derived infection (data not shown), while spores were still able to infect the plant (54). Moreover, B. cinerea chitin synthase (Bcchs1 or Bcchs3a) mutants exhibiting reduced chitin contents in their cell walls were also shown to be affected in virulence (66,67). The fact that Mg 2ϩ supplementation improved the cell wall stability and penetration rates of Bccrz1 mutants indicates the importance of intact cell walls for normal infection efficiencies.…”

Section: Bccrz1 Acts As a Downstream Target Of (Yeast) Calcineurinmentioning

confidence: 97%

Calcineurin-Responsive Zinc Finger Transcription Factor CRZ1 of Botrytis cinerea Is Required for Growth, Development, and Full Virulence on Bean Plants

2008

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Recently, we showed that the ␣ subunit BCG1 of a heterotrimeric G protein is an upstream activator of the Ca 2؉ /calmodulin-dependent phosphatase calcineurin in the gray mold fungus Botrytis cinerea. To identify the transcription factor acting downstream of BCG1 and calcineurin, we cloned the gene encoding the B. cinerea homologue of CRZ1 ("CRaZy," calcineurin-responsive zinc finger transcription factor), the mediator of calcineurin function in yeast. BcCRZ1 is able to partially complement the corresponding Saccharomyces cerevisiae mutant, and the subcellular localization of the green fluorescent protein-BcCRZ1 fusion product in yeast cells depends on the calcium level and calcineurin activity. Bccrz1 deletion mutants are not able to grow on minimal media and grow slowly on media containing plant extracts. Hyphal morphology, conidiation, and sclerotium formation are impaired. The cell wall and membrane integrity, stress response (extreme pH, H 2 O 2 , Ca 2؉ , Li ؉ ), and ability of the hyphae to penetrate the intact plant surface are affected in the mutants. However, BcCRZ1 is almost dispensable for the conidium-derived infection of bean plants. The addition of Mg 2؉ restores the growth rate, conidiation, and penetration and improves the cell wall integrity but has no impact on sclerotium formation or hypersensitivity to Ca 2؉ and H 2 O 2 . The expression of a set of recently identified BCG1-and calcineurin-dependent genes is also affected in ⌬Bccrz1 mutants, confirming that this transcription factor acts downstream of calcineurin in B. cinerea. Since the Bccrz1 mutants still respond to calcineurin inhibitors, we conclude that BcCRZ1 is not the only target of calcineurin.

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“…On the other hand, it was shown that disruption of only one CHS gene could lead to a drastic reduction in the pathogenicity of plant parasites (53,74,86,88), suggesting that targeting only one enzyme might be sufficient. Apparently, there are fewer CHS genes in oomycetes than in fungi.…”

Section: Vol 7 2008 Aphanomyces Euteiches Cell Wall Chitosaccharidementioning

confidence: 99%

Cell Wall Chitosaccharides Are Essential Components and Exposed Patterns of the Phytopathogenic OomyceteAphanomyces euteiches

et al. 2008

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Chitin is an essential component of fungal cell walls, where it forms a crystalline scaffold, and chitooligosaccharides derived from it are signaling molecules recognized by the hosts of pathogenic fungi. Oomycetes are cellulosic fungus-like microorganisms which most often lack chitin in their cell walls. Here we present the first study of the cell wall of the oomycete Aphanomyces euteiches, a major parasite of legume plants. Biochemical analyses demonstrated the presence of ca. 10% N-acetyl-D-glucosamine (GlcNAc) in the cell wall. Further characterization of the GlcNAc-containing material revealed that it corresponds to noncrystalline chitosaccharides associated with glucans, rather than to chitin per se. Two putative chitin synthase (CHS) genes were identified by data mining of an A. euteiches expressed sequence tag collection and Southern blot analysis, and full-length cDNA sequences of both genes were obtained. Phylogeny analysis indicated that oomycete CHS diversification occurred before the divergence of the major oomycete lineages. Remarkably, lectin labeling showed that the Aphanomyces euteiches chitosaccharides are exposed at the cell wall surface, and study of the effect of the CHS inhibitor nikkomycin Z demonstrated that they are involved in cell wall function. These data open new perspectives for the development of antioomycete drugs and further studies of the molecular mechanisms involved in the recognition of pathogenic oomycetes by the host plants.

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Botrytis cinerea virulence is drastically reduced after disruption of chitin synthase class III gene (Bcchs3a)

Cited by 74 publications

References 50 publications

Class III Chitin Synthase ChsB of Aspergillus nidulans Localizes at the Sites of Polarized Cell Wall Synthesis and Is Required for Conidial Development

Class III Chitin Synthase ChsB of Aspergillus nidulans Localizes at the Sites of Polarized Cell Wall Synthesis and Is Required for Conidial Development

Calcineurin-Responsive Zinc Finger Transcription Factor CRZ1 of Botrytis cinerea Is Required for Growth, Development, and Full Virulence on Bean Plants

Cell Wall Chitosaccharides Are Essential Components and Exposed Patterns of the Phytopathogenic OomyceteAphanomyces euteiches

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