Skip to main content
SpringerLink
Log in

Field strains of Stemphylium vesicarium with a resistance to dicarboximide fungicides correlated with changes in a two-component histidine kinase

  • Published:
European Journal of Plant Pathology Aims and scope Submit manuscript

Abstract

In Stemphylium vesicarium, four phenotypes were recognized according to their in vitro responses to dicarboximide fungicides: S (sensitive), S+ (low resistant to iprodione and procymidone but moderately resistant to vinclozolin), R1 (moderately resistant to iprodione and vinclozolin but highly resistant to procymidone), R2 (highly resistant to all dicarboximides). Cross-resistance was observed between dicarboximides and aromatic hydrocarbon fungicides in all cases while cross-resistance to phenylpyrroles was only detected in R2 phenotype. Moreover, no changes were noted in sensitivity to oxidative and osmotic stress inducers. An osmosensing histidine kinase gene, homologous to OS1 from Neurospora crassa, was sequenced from several field isolates of Stemphylium vesicarium. This gene is predicted to encode a 1,329 amino acid protein, comprising a conserved histidine-kinase domain in the C-terminal region and six tandem repeats of about 90 amino acids at the N-terminal end. In S+ and R1 phenotype isolates, a single amino acid substitution was observed in the first amino acid repeat; F267L and L290S respectively. For the R2 isolates, the exchanges T765R or Q777R were located within the histidine-kinase domain.

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

Similar content being viewed by others

References

  • Alberoni, G., Collina, M., Pancaldi, D., & Brunelli, A. (2005). Resistance to dicarboximide fungicides in Stemphylium vesicarium of Italian pear orchards. European Journal of Plant Pathology, 113, 211–219.

    Article  CAS  Google Scholar 

  • Alberoni, G., Collina, M., & Brunelli, A. (2006). Biological characteristics of dicarboximides resistant isolates of Stemphylium vesicarium from Italian pear orchards. IOBC/wprs Bulletin, 29, 109–115.

    Google Scholar 

  • Alberoni, G., Collina, M., Cavallini, D., & Brunelli, A. (2008). Stemphylium vesicarium resistance to fungicides on pear in Italy. In H. W. Dehne, H. B. Deising, U. Gisi, K. H. Kuck, P. E. Russell, & H. Lyr (Eds.), Modern fungicides and antifungal compounds (pp. 167–172). Bonn: Lebenshilfe Braunschweig.

    Google Scholar 

  • Appleyard, M. V. C. L., McPheat, W. L., & Stark, M. J. R. (2000). A novel “two-component” protein containing histidine kinase and response regulator domains required for sporulation in Aspergillus nidulans. Current Genetics, 37, 364–372.

    Article  CAS  PubMed  Google Scholar 

  • Avenot, H., Simoneau, P., Iacomi-Vasilescu, B., & Betaillé-Simoneau, N. (2005). Characterization of mutations in the two-component histidine kinase gene AbNIK1 from Alternaria brassicicola that confer high dicarboximide and phenylpyrrole resistance. Current Genetics, 47, 234–243.

    Article  CAS  PubMed  Google Scholar 

  • Beever, R. E., & Brien, H. M. R. (1983). A survey of resistance to the dicarboximide fungicides in Botrytis cinerea. New Zealand Journal of Agricultural Research, 26, 391–400.

    CAS  Google Scholar 

  • Brunelli, A., Gherardi, I., & Adani, N. (1997). Reduced sensitivity of Stemphylium vesicarium, causal agent of pear brown spot, to dicarboximide fungicides. Informatore Fitopatologico, 9, 44–48.

    Google Scholar 

  • Catlett, N. L., Yoder, O. C., & Turgeon, B. G. (2003). Whole-genome analysis of two-component signal transduction genes in fungal pathogens. Eukaryotic Cell, 2, 1151–1161.

    Article  CAS  PubMed  Google Scholar 

  • Cui, W., Beever, R. E., Parkes, S. L., Weeds, P. L., & Templeton, M. D. (2002). An osmosensing histidine kinase mediates dicarboximide fungicide resistance in Botryotinia fuckeliana (Botrytis cinerea). Fungal Genetics and Biology, 36, 187–198.

    Article  CAS  PubMed  Google Scholar 

  • Cui, W., Beever, R. E., Parkes, S. L., & Templeton, M. D. (2004). Evolution of an osmosensing histidine kinase in field strains of Botryotinia fuckeliana (Botrytis cinerea) in response to dicarboximide fungicide usage. Phytopathology, 94, 1129–1135.

    Article  CAS  PubMed  Google Scholar 

  • Dry, I. B., Yuan, K. H., & Hutton, D. G. (2004). Dicarboximide resistance in field isolates of Alternaria alternata is mediated by a mutation in a two-component histidine kinase gene. Fungal Genetics and Biology, 41, 102–108.

    Article  CAS  PubMed  Google Scholar 

  • Faretra, F., & Pollastro, S. (1991). Genetic basis of resistance to benzimidazole and dicarboximide fungicides in Botryotinia fuckeliana (Botrytis cinerea). Mycological Research, 95, 943–951.

    Article  CAS  Google Scholar 

  • Fujimura, M., Ochiai, N., Ichiishi, A., Usami, R., Horikoshi, K., & Yamaguchi, I. (2000). Fungicide resistance and osmotic stress sensitivity in os mutants of Neurospora crassa. Pesticide Biochemistry and Physiology, 67, 125–133.

    Article  CAS  Google Scholar 

  • Iacomi-Vasilescu, B., Avenot, H., Bataillé-Simoneau, N., Laurent, E., Guénard, M., & Simoneau, P. (2004). In vitro fungicide sensitivity of Alternaria species pathogenic to crucifers and identification of Alternaria brassicicola field isolates highly resistant to both dicarboximides and phenylpyrroles. Crop Protection, 23, 481–488.

    Article  CAS  Google Scholar 

  • Leroux, P. (2004). Chemical control of Botrytis and its resistance to chemical fungicides. In Y. Elad, B. Williamson, P. Tudzynski, & N. Delen (Eds.), Botrytis: biology, pathology and control (pp. 195–222). Dordrecht: Kluwer Academic Publishers.

    Google Scholar 

  • Leroux, P., & Fritz, R. (1984). Antifungal activity of dicarboximides and aromatic hydrocarbons and resistance to these fungicides. In A. P. J. Trinci & J. F. Ryley (Eds.), Mode of action of antifungal agents (pp. 207–237). Cambridge: Cambridge University Press.

    Google Scholar 

  • Leroux, P., Lanen, C., & Fritz, R. (1992). Similarities in the antifungal activities of fenpiclonil, iprodione and tolclofos-methyl against Botrytis cinerea and Fusarium nivale. Pesticide Science, 36, 255–261.

    Article  CAS  Google Scholar 

  • Leroux, P., Fritz, R., Debieu, D., Albertini, C., Lanen, C., Bach, J., et al. (2002). Mechanisms of resistance to fungicides in field strains of Botrytis cinerea. Pest Management Science, 58, 876–888.

    Article  CAS  PubMed  Google Scholar 

  • Ma, Z., & Michailides, T. J. (2004). Characterization of iprodione-resistant Alternaria isolates from pistachio in California. Pesticide Biochemistry and Physiology, 80, 75–84.

    Article  CAS  Google Scholar 

  • Miller, T. K., Renault, S., & Selitrennikoff, C. P. (2002). Molecular dissection of alleles of the osmotic-1 locus of Neurospora crassa. Fungal Genetics and Biology, 35, 147–155.

    Article  CAS  PubMed  Google Scholar 

  • Ochiai, N., Fujimura, M., Motoyama, T., Ichiishi, A., Usami, R., Horikoshi, K., et al. (2001). Characterization of mutations in the two-component histidine kinase gene that confer fludioxonil resistance and osmotic sensitivity in the os-1 mutants of Neurospora crassa. Pest Management Science, 57, 437–442.

    Article  CAS  PubMed  Google Scholar 

  • Oshima, M., Fujimura, M., Banno, S., Hashimoto, C., Motoyama, T., Ichiishi, A., et al. (2002). A point mutation in the two-component histidine kinase BcOS-1 gene confers dicarboximide resistance in field isolates of Botrytis cinerea. Phytopathology, 92, 75–80.

    Article  CAS  PubMed  Google Scholar 

  • Oshima, M., Banno, S., Okada, K., Takeuchi, T., Kimura, M., Ichiishi, A., et al. (2006). Survey of mutations of a histidine kinase gene BcOS1 in dicarboximides-resistant field isolates of Botrytis cinerea. Journal of General Plant Pathology, 72, 65–73.

    Article  CAS  Google Scholar 

  • Pillonel, C., & Meyer, T. (1997). Effect of phenylpyrroles on glycerol accumulation and protein kinase activity of Neurospora crassa. Pesticide Science, 49, 229–236.

    Article  CAS  Google Scholar 

  • Viaud, M., Fillinger, S., Liu, W., Polepalli, J. S., Le Pêcheur, P., Kunduru, A. R., et al. (2006). A class III histidine kinase acts as a novel virulence factor in Botrytis cinerea. Molecular Plant-Microbe Interactions, 19, 1042–1050.

    Article  CAS  PubMed  Google Scholar 

  • West, A. H., & Stock, A. M. (2001). Histidine kinases and response regulator proteins in two-component signaling systems. Trends in Biochemical Sciences, 26, 369–376.

    Article  CAS  PubMed  Google Scholar 

  • Yoshimi, A., Imanishi, J., Gafur, A., Tanaka, C., & Tsuda, M. (2003). Characterization and genetic analysis of laboratory mutants of Cochliobolus heterostrophus resistant to dicarboximide and phenylpyrrole fungicides. Journal of General Plant Pathology, 69, 101–108.

    CAS  Google Scholar 

  • Yoshimi, A., Tsuda, M., & Tanaka, C. (2004). Cloning and characterization of the histidine kinase gene Dic1 from Cochliobolus heterostrophus that confers dicarboximide resistance and osmotic adaptation. Molecular Genetics and Genomics, 271, 228–236.

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We thank all the researchers and technicians of the UMR Bioger.CPP working within the fungicide group for their encouragement and helpful discussions.

Author information

Authors and Affiliations

  1. Department of Agri-food Protection and Improvement, University of Bologna, Viale G. Fanin, 46, 40127, Bologna, Italy

    Giulia Alberoni, Marina Collina & Agostino Brunelli

  2. UMR 1290 Bioger CPP, INRA, Avenue Lucien Brétignières, BP01, 78850, Thiverval-Grignon, France

    Catherine Lanen & Pierre Leroux

Authors
  1. Giulia Alberoni
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Marina Collina
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Catherine Lanen
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Pierre Leroux
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Agostino Brunelli
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Marina Collina.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Alberoni, G., Collina, M., Lanen, C. et al. Field strains of Stemphylium vesicarium with a resistance to dicarboximide fungicides correlated with changes in a two-component histidine kinase. Eur J Plant Pathol 128, 171–184 (2010). https://doi.org/10.1007/s10658-010-9642-9

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10658-010-9642-9

Keywords

Search

Navigation