Skip to main content
SpringerLink
Log in

Botrytis cinerea chitin synthase BcChsVI is required for normal growth and pathogenicity

  • Research Article
  • Published:
Current Genetics Aims and scope Submit manuscript

Abstract

Fungal chitin synthase of classes V and VI (or VII), which contain an additional N-terminal myosin motor domain, have been shown to play important roles in pathogenesis. To study the function of BcChsVI in Botrytis cinerea, BcChs6 gene was disrupted through Agrobacterium tumefaciens-mediated transformation. The Bcchs6 disruption mutant exhibited a 45.5 % increasing in its chitin content when compared with wild strain. The qRT-PCR analysis revealed that in Bcchs6 mutant the expression of BcChs6 was significantly decreased, while the expression of BcChs2 and BcChs3a was increased when compared with wild type. It is probable that the disruption of this gene provoked a compensatory mechanism regulating the cellular response to cell wall damage. Interestingly, the radial growth of Bcchs6 mutant was drastically reduced when 50 % solute was removed from the regular PDA medium, and they were more sensitive to Calcofluor white and other cell wall disturbing chemicals. Pathogenicity assays on tomato leaves indicated that they were significantly reduced in their ability to cause disease. Our results demonstrated that BcChs6 is necessary for proper hyphal growth and pathogenicity of B. cinerea on tomato leaves.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Aguayo C, Riquelme J, Valenzuela PDT, Hahn M, Moreno ES (2011) Bchex virulence gene of Botrytis cinerea: characterization and functional analysis. J Gen Plant Pathol 77:230–238

    Article  Google Scholar 

  • Amnuaykanjanasin A, Epstein L (2003) A class V chitin synthase gene, chsA is essential for conidial and hyphal wall strength in the fungus Colletotrichum graminicola (Glomerella graminicola). Fungal Genet Biol 38:272–285

    Article  PubMed  CAS  Google Scholar 

  • Arbelet D, Malfatti P, Simond-Côte E, Fontaine T, Desquilbet L, Expert D, Kunz C, Soulié MC (2010) Disruption of the Bcchs3a chitin synthase gene in Botrytis cinerea is responsible for altered adhesion and overstimulation of host plant immunity. Mol Plant Microbe Interact 23(10):1324–1334

    Article  PubMed  CAS  Google Scholar 

  • Chigira Y, Abe K, Gomi K, Nakajima T (2002) chsZ, a gene for a novel class of chitin synthase from Aspergillus oryzae. Curr Genet 41:261–267

    Article  PubMed  CAS  Google Scholar 

  • Choquer M, Boccara M, Goncalves IR, Soulie′ MC, Vidal-Cros A (2004) Survey of the Botrytis cinerea chitin synthase multigenic family through the analysis of six euascomycetes genomes. Eur J Biochem 271:2153–2164

    Article  PubMed  CAS  Google Scholar 

  • Choquer M, Fournier E, Kunz C, Levis C, Pradier JM, Simon A, Viaud M (2007) Botrytis cinerea virulence factors: new insights into a necrotrophic and polyphageous pathogen. FEMS Microbiol Lett 277(1):1–10

    Article  PubMed  CAS  Google Scholar 

  • Cui Z, Ding Z, Yang X, Wang K, Zhu T (2009) Gene disruption and characterization of a class V chitin synthase in Botrytis cinerea. Can J Microbiol 55(11):1267–1274

    Article  PubMed  CAS  Google Scholar 

  • Garcera-Teruel A, Xoconostle-Cazares B, Rosas-Quijano R, Ortiz L, Leon-Ramirez C, Specht CA, Sentandreu R, Ruiz-Herrera J (2004) Loss of virulence in Ustilago maydis by Umchs6 gene disruption. Res Microbiol 155:87–97

    Article  PubMed  CAS  Google Scholar 

  • Jarvis WR (1980) Taxonomy and epidemiology. In: Coley-Smith JR, Verhoeff K, Jarvis WR (eds) The biology of botrytis. Academic Press, London, pp 219–250

    Google Scholar 

  • Jiang JH, Ding LS, Michailides TJ, Li H, Ma Z (2009) Molecular characterization of field azoxystrobin-resistant isolates of Botrytis cinerea. Pestic Biochem Phys 93:72–76

    Article  CAS  Google Scholar 

  • Kim JE, Lee HJ, Lee J, Kim KW, Yun SH, Shim WB, Lee YW (2009) Gibberella zeae chitin synthase genes, GzCHS5 and GzCHS7, are required for hyphal growth, perithecia formation, and pathogenicity. Curr Genet 55:449–459

    Article  PubMed  CAS  Google Scholar 

  • Kong LA, Yang J, Li GT, Qi LL, Zhang YJ, Wang CF, Zhao WS, Xu JR, Peng YL (2012) Different chitin synthase genes are required for various developmental and plant infection processes in the rice blast fungus Magnaporthe oryzae. PLoS Pathog 8(2):e1002526

    Article  PubMed  CAS  Google Scholar 

  • Kretschmer M, Leroch M, Mosbach A, Walker AS, Fillinger S, Mernke D, Schoonbeek HJ, Pradier JM, Leroux P, De Waard MA, Hahn M (2009) Fungicide-driven evolution and molecular basis of multidrug resistance in field populations of the grey mould fungus Botrytis cinerea. PLoS Pathog 5(12):e1000696

    Article  PubMed  Google Scholar 

  • Larson TM, Kendra DF, Busman M, Brown DW (2011) Fusarium verticillioides chitin synthases CHS5 and CHS7 are required for normal growth and pathogenicity. Curr Genet 57:177–189

    Article  PubMed  CAS  Google Scholar 

  • Latge JP (2007) The cell wall: a carbohydrate armour for the fungal cell. Mol Microbiol 66(2):279–290

    Article  PubMed  CAS  Google Scholar 

  • Leroch M, Kretschmer M, Hahn M (2011) Fungicide resistance phenotypes of Botrytis cinerea isolates from commercial vineyards in south west Germany. J Phytopathol 159:63–65

    Article  CAS  Google Scholar 

  • Leroux P, Fritz R, Debieu D, Albertini C, Lanen C, Bach J, Gredt M, Chapeland F (2002) Mechanisms of resistance to fungicides in field strains of Botrytis cinerea. Pest Manag Sci 58(9):876–888

    Article  PubMed  CAS  Google Scholar 

  • Liu W, Leroux P, Fillinger S (2008) The HOG1-like MAP kinase Sak1 of Botrytis cinerea is negatively regulated by the upstream histidine kinase Bos1 and is not involved in dicarboximide and phenylpyrrole resistance. Fungal Genet Biol 45(7):1062–1074

    Article  PubMed  CAS  Google Scholar 

  • Madrid MP, Di Pietro A, Roncero MI (2003) Class V chitin synthase determines pathogenesis in the vascular wilt fungus Fusarium oxysporum and mediates resistance to plant defence compounds. Mol Microbiol 47(1):257–266

    Article  PubMed  CAS  Google Scholar 

  • Martin-Urdiroz M, Roncero MI, Gonza′lez-Reyes JA, Ruiz-Rolda′n C (2008) ChsVb, a class VII chitin synthase involved in septation, is critical for pathogenicity in Fusarium oxysporum. Eukaryot Cell 7(1):112–121

    Article  PubMed  CAS  Google Scholar 

  • Merzendorfer H (2011) The cellular basis of chitin synthesis in fungi and insects: common principles and differences. Eur J Cell Biol 90:759–769

    Article  PubMed  CAS  Google Scholar 

  • Müller C, Hjort CM, Hansen K, Nielsen J (2002) Altering the expression of two chitin synthase genes differentially affects the growth and morphology of Aspergillus oryzae. Microbiology 148:4025–4033

    PubMed  Google Scholar 

  • Nino-Vega GA, Carrero L, San-Blas G (2004) Isolation of the CHS4 gene of Paracoccidioides brasiliensis and its accommodation in a new class of chitin synthases. Med Mycol 42:51–57

    Article  PubMed  CAS  Google Scholar 

  • Roncero C (2002) The genetic complexity of chitin synthesis in fungi. Curr Genet 41:367–378

    Article  PubMed  CAS  Google Scholar 

  • Soulie′ MC, Piffeteau A, Choquer M, Boccara M, Vidal-Cros A (2003) Disruption of Botrytis cinerea class I chitin synthase gene Bcchs1 results in cell wall weakening and reduced virulence. Fungal Genet Biol 40(1):38–46

    Article  Google Scholar 

  • Soulie′ MC, Perino C, Piffeteau A, Choquer M, Malfatti P, Cimerman A, Kunz C, Boccara M, Vidal-Cros A (2006) Botrytis cinerea virulence is drastically reduced after disruption of chitin synthase class III gene (Bcchs3a). Cell Microbiol 8(8):1310–1321

    Article  Google Scholar 

  • Takeshita N, Ohta A, Horiuchi H (2005) CsmA, a class V chitin synthase with a myosin motor-like domain, is localized through direct interaction with the actin cytoskeleton in Aspergillus nidulans. Mol Biol Cell 16:1961–1970

    Article  PubMed  CAS  Google Scholar 

  • Takeshita N, Yamashita S, Ohta A, Horiuchi H (2006) Aspergillus nidulans class V and VI chitin synthases CsmA and CsmB, each with a myosin motor-like domain, perform compensatory functions that are essential for hyphal tip growth. Mol Microbiol 59(5):1380–1394

    Article  PubMed  CAS  Google Scholar 

  • Treitschke S, Doehlemann G, Schuster M, Steinberg G (2010) The myosin motor domain of fungal chitin synthase V is dispensable for vesicle motility but required for virulence of the Maize pathogen Ustilago maydis. Plant Cell 22:2476–2494

    Article  PubMed  CAS  Google Scholar 

  • Tsuizaki M, Takeshita N, Ohta A, Horiuchi H (2009) Myosin motor-like domain of the class VI chitin synthase CsmB is essential to its functions in Aspergillus nidulans. Biosci Biotechnol Biochem 73(5):1163–1167

    Article  PubMed  CAS  Google Scholar 

  • Weber I, Gruber C, Steinberg G (2003) A class-V myosin required for mating, hyphal growth, and pathogenicity in the dimorphic plant pathogen Ustilago maydis. Plant Cell 15:2826–2842

    Article  PubMed  CAS  Google Scholar 

  • Weber I, Assmann D, Thines E, Steinberg G (2006) Polar localizing class V myosin chitin synthases are essential during early plant infection in the plant pathogenic fungus Ustilago maydis. Plant Cell 18:225–242

    Article  PubMed  CAS  Google Scholar 

  • Werner S, Sugui JA, Gero Steinberg G, Deising HB (2007) A chitin synthase with a myosin-like motor domain is essential for hyphal growth, appressorium differentiation, and pathogenicity of the Maize Anthracnose Fungus Colletotrichum graminicola. Mol Plant Microbe Interact 20(12):1555–1567

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This work was supported by a grant from the Scientific Research Foundation of Zhejiang Province (No. LY12C14008) and National Nature Science Foundation of China (No. 31272002).

Author information

Authors and Affiliations

  1. College of Biological and Environmental Engineering, Zhejiang University of Technology, Hangzhou, 310032, People’s Republic of China

    Zhifeng Cui, Yanhua Wang, Na Lei, Kun Wang & Tingheng Zhu

Authors
  1. Zhifeng Cui
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Yanhua Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Na Lei
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Kun Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Tingheng Zhu
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Tingheng Zhu.

Additional information

Communicated by B. Cormack.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Cui, Z., Wang, Y., Lei, N. et al. Botrytis cinerea chitin synthase BcChsVI is required for normal growth and pathogenicity. Curr Genet 59, 119–128 (2013). https://doi.org/10.1007/s00294-013-0393-y

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00294-013-0393-y

Keywords

Search

Navigation