Expression of the ABC transporter BcatrD from Botrytis cinerea reduces sensitivity to sterol demethylation inhibitor fungicides

Pesticide Biochemistry and Physiology

Volumn 73, Issue 2, 2002, Pages 110-121

  Hayashi, Keisuke ^a   Schoonbeek, Henk Jan ^a   De Waard, Maarten A ^a  

^a WAGENINGEN UNIVERSITY   (Netherlands)

Author keywords

ABC transporters; Azole fungicides; BcatrD; Botrytis cinerea; DMI fungicides; Oxpoconazole; Pyrifenox; Tebuconazole

Indexed keywords

BOTRYOTINIA FUCKELIANA; BOTRYTIS;

EID: 0036383101     PISSN: 00483575     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0048-3575(02)00015-9     Document Type: Article

References (36)

1. J.R. Coley-Smith, W.R. Jarvis, K. Verhoeff, The Biology of Botrytis, Academic Press, London, 1980.
2. P. Leroux, F. Chapeland, D. Desbrosses, M. Gredt, Patterns of cross-resistance to fungicides in Botryotinia fuckeliana (Botrytis cinerea) isolates from French vineyards, Crop Prot. 18 (1999) 687.
3. Y. Uesugi, Fungicide classes: chemistry, uses and mode of action, in: D.H. Hutson, J. Miyamoto (Eds.), Fungicidal activity: chemical and biological approaches to plant protection, John Wiley & Sons Ltd., Chichester, 1998, pp. 23-56.
4. M.A. De Waard, Resistance to fungicides which inhibit sterol 14α-demethylation, an historical perspective, in: S. Heaney, D. Slawson, D.W. Hollomon, M. Smith, P.E. Russell, D.W. Parry (Eds.), Fungicide resistance, BCPC Monograph, vol. 60, British Crop Protection Council, Surrey, 1994, pp. 3-10.
5. D.C. Lamb, D.E. Kelly, T.C. White, S.L. Kelly, The R467K amino acid substitution in Candida albicans sterol 14 alpha-demethylase causes drug resistance through reduced affinity, Antimicrob. Agents Chemother. 44 (2000) 63.
6. D.C. Lamb, D.E. Kelly, W.H. Schunck, A.Z. Shyadehi, M. Akhtar, D.J. Lowe, B.C. Baldwin, S.L. Kelly, The mutation T315A in Candida albicans sterol 14 alpha-demethylase causes reduced enzyme activity and fluconazole resistance through reduced affinity, J. Biol. Chem. 272 (1997) 5682.
7. H. Hamamoto, K. Hasegawa, R. Nakaune, Y.J. Lee, Y. Makizumi, K. Akutsu, T. Hibi, Tandem repeat of a transcriptional enhancer upstream of the sterol 14 alpha-demethylase gene (CYP51) in Penicillium digitatum, Appl. Environ. Microbiol. 66 (2000) 3421.
8. M.A. De Waard, J.G.M. Van Nistelrooy, Mechanism of resistance to fenarimol in Aspergillus nidulans, Pestic. Biochem. Physiol. 10 (1979) 219.
9. M.A. De Waard, J.G.M. Van Nistelrooy, Accumulation of SBI fungicides in wild-type and fenarimol-resistant isolates of Penicillium italicum, Pestic. Sci. 22 (1988) 371.
10. G. Del Sorbo, H. Schoonbeek, M.A. De Waard, Fungal transporters involved in efflux of natural toxic compounds and fungicides, Fungal Genet. Biol. 30 (2000) 1.
11. A.J.M. Driessen, B.P. Rosen, W.N. Konings, Diversity of transport mechanisms: common structural principles, Trends Biochem. Sci. 25 (2000) 397.
12. G. Del Sorbo, A.C. Andrade, J.G.M. Van Nistelrooy, J.A.L. Van Kan, E. Balzi, M.A. De Waard, Multidrug resistance in Aspergillus nidulans involves novel ATP-binding cassette transporters, Mol. Gen. Genet. 254 (1997) 417.
13. R. Prasad, P. De Wergifosse, A. Goffeau, E. Balzi, Molecular cloning and characterization of a novel gene of Candida albicans, CDR1, conferring multiple resistance to drugs and antifungals, Curr. Genet. 27 (1995) 320.
14. L.-H. Zwiers, M.A. De Waard, Characterization of the ABC transporter genes MgAtr1 and MgAtr2 from the wheat pathogen Mycosphaerella graminicola, Fungal Genet. Biol. 30 (2000) 115.
15. R. Nakaune, K. Adachi, O. Nawata, M. Tomiyama, K. Akutsu, T. Hibi, A novel ATP-binding cassette transporter involved in multidrug resistance in the phytopathogenic fungus Penicillium digitatum, Appl. Environ. Microbiol. 64 (1998) 3983.
16. F. Chapeland, R. Fritz, C. Lanen, M. Gredt, P. Leroux, Inheritance and mechanisms of resistance to anilinopyrimidine fungicides in Botrytis cinerea (Botryotinia fuckeliana), Pestic. Biochem. Physiol. 64 (1999) 85.
17. A.M. Alarco, I. Balan, D. Talibi, N. Mainville, M. Raymond, AP1-mediated multidrug resistance in Saccharomyces cerevisiae requires FLR1 encoding a transporter of the major facilitator superfamily, J. Biol. Chem. 272 (1997) 19304.
18. M.A. De Waard, Significance of ABC transporters in fungicide sensitivity and resistance, Pestic. Sci. 51 (1997) 271.
19. A.C. Andrade, G. Del Sorbo, J.G.M. Van Nistelrooy, M.A. De Waard, The ABC transporter AtrB from Aspergillus nidulans mediates resistance to all major classes of fungicides and some natural toxic compounds, Microbiology 146 (2000) 1987.
20. H. Schoonbeek, G. Del Sorbo, M.A. De Waard, The ABC transporter BcatrB affects the sensitivity of Botrytis cinerea to the phytoalexin resveratrol and the fungicide fenpiclonil, Mol. Plant-Microbe Interact. 14 (2001) 562.
21. C. Stehmann, J.C. Kapteyn, M.A. De Waard, Development of a cell-free assay from Botrytis cinerea as a biochemical screen for sterol biosynthesis inhibitors, Pestic. Sci. 40 (1994) 1.
22. C. Stehmann, M.A. De Waard, Factors influencing activity of triazole fungicides towards Botrytis cinerea, Crop Prot. 15 (1996) 39.
23. K. Hayashi, H. Schoonbeek, H. Sugiura, M.A. De Waard, Multidrug resistance in Botrytis cinerea associated with decreased accumulation of the azole fungicide oxpoconazole and increased transcription of the ABC transporter gene BcatrD, Pestic. Biochem. Physiol. 70 (2001) 168.
24. T. Vermeulen, H. Schoonbeek, M.A. De Waard, The ABC transporter BcatrB from Botrytis cinerea is a determinant of the activity of the phenylpyrrole fungicide fludioxonil, Pest. Manag. Sci. 57 (2001) 393.
25. J. Sambrook, E.F. Fritsch, T. Maniatis, Molecular Cloning: A laboratory Manual, second ed., Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York, 1989.
26. J.D. Thompson, D.G. Higgins, T.J. Gibson, Clustal W-improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice, Nucleic Acids Res. 11 (1994) 4673.
27. J.A.L. Van Kan, J.W. Van't Klooster, C.A.M. Wagemakers, D.C.T. Dees, C.J.B. Van der Vlugt-Bergmans, Cutinase A of Botrytis cinerea is expressed, but not essential during penetration of gerbera and tomato, Mol. Plant-Microbe Interact. 10 (1997) 30.
28. A. Drenth, S.B. Goodwin, W.E. Fry, L.C. Davidse, Genotypic diversity of Phytophthora infestans in the Netherlands revealed by DNA polymorphisms, Phytopathology 83 (1993) 1087.
29. S.E. Unkles, Gene organization in industrial filamentous fungi, in: J.R. Kinghorn, G. Turner (Eds.), Applied molecular genetics of filamentous fungi, Blackie, Glasgow, 1992, pp. 28-53.
30. V. Gavrias, A. Andrianopoulos, C.J. Gimeno, W.E. Timberlake, Saccharomyces cerevisiae TEC1 is required for pseudohyphal growth, Mol. Microbiol. 19 (1996) 1255.
31. J. Kyte, R.F. Doolittle, A simple method for displaying the hydropathic character of a protein, J. Mol. Biol. 157 (1982) 105.
32. J.E. Walker, M. Saraste, M.J. Runswick, N.J. Gay, Distantly related sequences in the alpha- and beta-subunits of ATP synthase, myosin, kinases and other ATP-requiring enzymes and a common nucleotide binding fold, EMBO J. 1 (1982) 945.
33. M. Urban, T. Bhargava, J.E. Hamer, An ATP-driven efflux pump is a novel pathogenicity factor in rice blast disease, EMBO J. 18 (1999) 512.
34. A.C. Andrade, Ph.D. Thesis, Wageningen University, 2000.
35. M.M. Gottesman, I. Pastan, The multidrug transporter, a double-edged sword, J. Biol. Chem. 263 (1988) 12163.
36. C. Stehmann, M.A. De Waard, Sensitivity of populations of Botrytis cinerea to triazoles, benomyl and vinclozolin, Eur. J. Plant Pathol. 102 (1996) 171.