High resistance of Isaria fumosorosea to carbendazim arises from the overexpression of an ATP-binding cassette transporter (ifT1) rather than tubulin mutation

Journal of Applied Microbiology

Volumn 112, Issue 1, 2012, Pages 175-184

  Song, T T ^a   Ying, S H ^a   Feng, M G ^a  

^a ZHEJIANG UNIVERSITY   (China)

Author keywords

ATP binding cassette transporter; Carbendazim resistance; Drug efflux pump; Entomopathogenic fungi; Isaria fumosorosea; Multidrug resistance; Transcription factors

Indexed keywords

BINDING SITES; CLONING; FUNGI; SODIUM COMPOUNDS; TRANSCRIPTION; TRANSCRIPTION FACTORS;

ATP BINDING CASSETTE TRANSPORTERS; BINDING-SITES; CARBENDAZIM RESISTANCE; DRUG EFFLUX PUMPS; ENTOMOPATHOGENIC FUNGUS; ISARIUM FUMOSOROSEA; MULTIDRUG RESISTANCE; OVEREXPRESSIONS; POINT MUTATIONS; WILD-TYPE STRAIN;

FUNGICIDES;

ABC TRANSPORTER; ABF1 PROTEIN; ALPHA TUBULIN; AZOXYSYROBIN; BETA TUBULIN; CARBENDAZIM; CYMOXANYL; FUNGICIDE; IMIDACLOPRID; IPRODIONE; PEPTIDES AND PROTEINS; PHOSPHINOTHRICIN; RAF PROTEIN; RHODAMINE; SHENQINMYCIN; THIOPHANATE METHYL; TRANSCRIPTION FACTOR GAL4; TRICYCLEAZOLE; UNCLASSIFIED DRUG;

BIOCONTROL AGENT; BIOLOGICAL CONTROL; BIOPESTICIDE; CARBENDAZIM; CHEMICAL BINDING; ENTOMOPATHOGENIC ORGANISM; FUNGUS; GENE EXPRESSION; INSECTICIDE; MUTATION; PESTICIDE RESISTANCE; PROTEIN; SPORE;

AMINO ACID SEQUENCE; ARTICLE; BINDING SITE; CONTROLLED STUDY; ENTOMOPATHOGENIC FUNGUS; FUNGAL STRAIN; FUNGICIDE RESISTANCE; FUNGUS GROWTH; FUNGUS MUTATION; ISARIA FUMOSOROSEA; MULTIDRUG RESISTANCE; NONHUMAN; NUCLEOTIDE SEQUENCE; PROTEIN EXPRESSION; WILD TYPE;

FUNGI; ISARIA;

EID: 83555179077     PISSN: 13645072     EISSN: 13652672     Source Type: Journal    
DOI: 10.1111/j.1365-2672.2011.05188.x     Document Type: Article

References (38)

1. Alenquer, M., Tenreiro, S. and Sá-Correia, I. (2006) Adaptive response to the antimalarial drug artesunate in yeast involves Pdr1p/Pdr3p-mediated transcriptional activation of the resistance determinants TPO1 and PDR5. FEMS Yeast Res 6, 1130-1139.
2. Andrade, A.C., Del Sorbo, G., Van Nistelrooy, J.G.M. and De Waard, M.A. (2000a) The ABC transporter AtrB from Aspergillus nidulans mediates resistance to all major classes of fungicides and some natural toxic compounds. Microbiol-SGM 146, 1987-1997.
3. Andrade, A.C., Van Nistelrooy, J.G., Peery, R.B., Skatrud, P.L. and De Waard, M.A. (2000b) The role of ABC transporters from Aspergillus nidulans in protection against cytotoxic agents and in antibiotic production. Mol Gen Genet 263, 966-977.
4. Balzi, E., Wang, M., Leterme, S., Van Dyck, L. and Goffau, A. (1994) PDR5, a novel yeast multidrug resistance-conferring transporter controlled by the transcription regulator PDR1. J Biol Chem 269, 2206-2214.
5. Brand, A. and Perrimon, N. (1993) Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 118, 401-415.
6. Butters, J.A., Devi, K.U., Mohan, C.M. and Sridevi, V. (2003) Screening for tolerance to bavistin, a benzimidazole fungicide containing methyl benzimidazol-2-yl carbamate (MBC), in Beauveria bassiana: sequence analysis of the beta-tubulin gene to identify mutations conferring tolerance. Mycol Res 107, 260-266.
7. Clark, F.S., Parkinson, T., Hitchcock, C.A. and Gow, N.A. (1996) Correlation between rhodamine 123 accumulation and azole sensitivity in Candida species: possible role for drug efflux in drug resistance. Antimicrob Agents Chemother 40, 419-425.
8. Davison, J.M., Akitake, C.M., Goll, M.G., Rhee, J.M., Gosse, N., Baier, H., Halpern, M.E., Leach, S.D. et al. (2007) Transactivation from Gal4-VP16 transgenic insertions for tissue-specific cell labeling and ablation in zebrafish. Dev Biol 304, 811-824.
9. Fardeau, V., Lelandais, G., Oldfield, A., Salin, H., Lemoine, S., Garcia, M., Tanty, V., Le Crom, S. et al. (2007) The central role of PDR1 in the foundation of yeast drug resistance. J Biol Chem 282, 5063-5074.
10. Faria, M. and Wraight, S.P. (2001) Biological control of Bemisia tabaci with fungi. Crop Protect 20, 767-778.
11. Gupta, A. and Chattoo, B.B. (2008) Functional analysis of a novel ABC transporter ABC4 from Magnaporthe grisea. FEMS Microbiol Lett 278, 22-28.
12. Kiso, T., Fujita, K.I., Ping, X., Tanaka, T. and Taniguchi, M. (2004) Screening for microtubule-disrupting antifungal agents by using a mitotic-arrest mutant of Aspergillus nidulans and novel action of phenylalanine derivatives accompanying tubulin loss. Antimicrob Agents Chemother 48, 1739-1748.
13. Li, P., Wood, K., Mamon, H., Haser, W. and Roberts, T. (1991) Raf-1: a kinase currently without a cause but not lacking in effects. Cell 64, 479-482.
14. -ΔΔ CT. Methods 25, 402-408.
15. Lucau-Danila, A., Lelandais, G., Kozovska, Z., Tanty, V., Delaveau, T., Devaux, F. and Jacq, C. (2005) Early expression of yeast genes affected by chemical stress. Mol Cell Biol 25, 1860-1868.
16. Ludescher, C., Thaler, J., Drach, D., Drach, J., Spitaler, M., Gattringer, C., Huber, H. and Hofmann, J. (1992) Detection of activity of P-glycoprotein in human tumour samples using rhodamine 123. Br J Haematol 82, 161-168.
17. Ma, Z.H., Yoshimura, M.A. and Michailides, T.J. (2003) Identification and characterization of benzimidazole resistance in Monilinia fructicola from stone fruit orchards in California. Appl Environ Microbiol 69, 7145-7152.
18. Ma, Z.H., Yoshimura, M.A. and Michailides, T.J. (2005) Characterization and PCR-based detection of benzimidazole-resistant isolates of Monilinia laxa in California. Pest Manag Sci 61, 449-457.
19. Mamnun, Y.M., Schuller, C. and Kuchler, K. (2004) Expression regulation of the yeast PDR5 ATP-binding cassette (ABC) transporter suggests a role in cellular detoxification during the exponential growth phase. FEBS Lett 559, 111-117.
20. Michalkova-Papajova, D., Obernauerova, M. and Subik, J. (2000) Role of the PDR gene network in yeast susceptibility to the antifungal antibiotic mucidin. Antimicrob Agents Chemother 44, 418-420.
21. Miyake, T., Loch, C.M. and Li, R. (2002) Identification of a multifunctional domain in autonomously replicating sequence-binding factor 1 required for transcriptional activation, DNA replication, and gene silencing. Mol Cell Biol 22, 505-516.
22. Nakaune, R., Hamamoto, H., Imada, J., Akutsu, K. and Hibi, T. (1998) A novel ATP-binding cassette transporter involved in multidrug resistance in the phytopathogenic fungus Penicillium digitatum. Appl Environ Microbiol 64, 3983-3988.
23. Nakaune, R., Hamamoto, H., Imada, J., Akutsu, K. and Hibi, T. (2002) A novel ABC transporter gene, PMR5, is involved in multidrug resistance in the phytopathogenic fungus Penicillium digitatum. Mol Genet Genomics 267, 1617-4615.
24. Parkinson, T., Falconer, D.J. and Hitchcock, C.A. (1995) Fluconazole resistance due to energy-dependent drug efflux in Candida glabrata. Antimicrob Agents Chemother 39, 1696-1699.
25. Prasad, R., Wergifosse, P., Goffeau, A. and Balzi, E. (1995) Molecular cloning and characterization of a novel gene of Candida albicans, CDR1 conferring multiple resistance to drugs and antifungals. Curr Genet 27, 320-329.
26. Sanglard, D., Ischer, F., Monod, M. and Bille, J. (1997) Cloning of Candida albicans genes conferring resistance to azole antifungal agents: characterization of CDR2, a new multidrug ABC transporter gene. Microbiol-SGM 143, 405-416.
27. Schlecht, U., Erb, I., Demougin, P., Robine, N., Borde, V., van Nimwegen, E., Nicolas, A. and Primig, M. (2008) Genome-wide expression profiling, in vivo DNA binding analysis, and probabilistic motif prediction reveal novel Abf1 target genes during fermentation, respiration, and sporulation in yeast. Mol Biol Cell 19, 2193-2207.
28. Skatrud, P.L. (2002) The impact of multiple drug resistance (MDR) proteins on chemotherapy and drug discovery. Prog Drug Res 58, 99-131.
29. Sridhar, S.S., Hedley, D. and Siu, L.L. (2005) Raf kinase as a target for anticancer therapeutics. Mol Cancer Ther 4, 677-685.
30. Taglicht, D. and Michaelis, S. (1998) Saccharomyces cerevisiae ABC proteins and their relevance to human health and disease. Methods Enzymol 292, 130-162.
31. Terai, K. and Matsuda, M. (2005) Ras binding opens c-Raf to expose the docking site for mitogen-activated protein kinase kinase. EMBO Rep 6, 251-255.
32. Thakur, J.K., Arthanari, H., Yang, F., Pan, S.J., Fan, X.C., Breger, J., Frueh, D.P., Gulshan, K. et al. (2008) A nuclear receptor-like pathway regulating multidrug resistance in fungi. Nature 452, 604-609.
33. Turi, T.G. and Rose, J.K. (1995) Characterization of a novel Schizosaccharomyces pombe multidrug resistance transporter conferring brefeldin A resistance. Biochem Biophys Res Commun 213, 410-418.
34. Urban, M., Bhargava, T. and Hamer, J.E. (1999) An ATP-driven efflux pump is a novel pathogenicity factor in rice blast disease. EMBO J 18, 512-521.
35. Vermitsky, J.P., Earhar, K.D., Smith, W.L., Smith, W.L., Homayouni, R., Edlind, T.D. and Rogers, P.D. (2006) Pdr1 regulates multidrug resistance in Candida glabrata: gene disruption and genome-wide expression studies. Mol Microbiol 61, 704-722.
36. Yan, K. and Dickman, M.B. (1996) Isolation of a beta-tubulin gene from Fusarium moniliforme that confers cold-sensitive benomyl resistance. Appl Environ Microbiol 62, 3053-3056.
37. Ying, S.H. and Feng, M.G. (2004) Relationship between thermotolerance and hydrophobin-like proteins in aerial conidia of Beauveria bassiana and Paecilomyces fumosoroseus as fungal biocontrol agents. J Appl Microbiol 97, 323-331.
38. Zou, G., Ying, S.H., Shen, Z.H. and Feng, M.G. (2006) Multi-sited mutations of beta-tubulin are involved in benzimidazole resistance and thermotolerance of fungal biocontrol agent Beauveria bassiana. Environ Microbiol 8, 2096-2105.