Transcriptome profiling of the response of Mycosphaerella graminicola isolates to an azole fungicide using cDNA microarrays

Molecular Plant Pathology

Volumn 8, Issue 5, 2007, Pages 639-651

  Cools, Hans J ^a   Fraaije, Bart A ^a   Bean, Tim P ^a   Antoniw, John ^a   Lucas, John A ^a  

^a ROTHAMSTED RESEARCH   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

FUNGI; MYCOSPHAERELLA GRAMINICOLA; TRITICUM AESTIVUM;

EID: 34548136160     PISSN: 14646722     EISSN: 13643703     Source Type: Journal    
DOI: 10.1111/j.1364-3703.2007.00411.x     Document Type: Article

References (47)

1. Agarwal, A.K., Rogers, P.D., Baerson, S.R., Jacob, M.R., Barker, K.S., Cleary, J.D., Walker, L.A., Nagle, D.G. Clark, A.M. (2003) Genome-wide expression profiling of the response to polyene, pyrimidine, azole, and echinocandin antifungal agents in Saccharomyces cerevisiae. J. Biol. Chem. 278, 34998 35015.
2. Bammert, G.F. Fostel, J.M. (2000) Genome-wide expression patterns in Saccharomyces cerevisiae: comparison of drug treatments and genetic alterations affecting biosynthesis of ergosterol. Antimicrob. Agents Chemother. 44, 1255 1265.
3. Boshoff, H.I.M., Myers, T.G., Copp, B.R., McNeil, M.R., Wilson, M.A. Barry, C.E. III (2004) The transcriptional responses of Mycobacterium tuberculosis to inhibitors of metabolism. Novel insights into drug mechanisms of action. J. Biol. Chem. 279, 40174 40184.
4. Brun, S., Bergeìs, T., Poupard, P., Vauzelle-Moreau, C., Renier, G., Chabasse, D. Bouchara, J.-P. (2004) Mechanisms of azole resistance in petite mutants of Candida glabrata. Antimicrob. Agents Chemother. 48, 1788 1796.
5. Clark, W.S. (2006) Septoria tritici and azole performance. Fungicide resistance: are we winning the battle but losing the war? Aspects Appl. Biol. 78, 127 132.
6. Cools, H.J., Fraaije, B.A., Kim, S.H. Lucas, J.A. (2006) Impact of changes in the target P450 CYP51 enzyme associated with altered triazole-senstivity in fungal pathogens of cereal crops. Biochem. Soc. Trans. 34, 1219 1222.
7. Cools, H.J., Fraaije, B.A. Lucas, J.A. (2005a) Molecular examination of Septoria tritici isolates with reduced sensitivities to triazoles. In : Modern Fungicides and Antifungal Compounds IV (Dehne, H.W., Gisi, U., Kuck, K.-H., Russell, P.E. Lyr, H., eds), pp. 103 114. Alton, UK : BCPC.
8. Cools, H.J., Fraaije, B.A. Lucas, J.A. (2005b) Molecular mechanisms correlated with changes in triazole sensitivity in isolates of Mycosphaerella graminicola. In : Proceedings of the BCPC Congress, Crop Science and Technology 2005, 1, pp. 267 274. Alton, UK : BCPC.
9. Daum, G., Lees, N.D., Bard, M. Dickson, R. (1998) Biochemistry, and cell biology of lipids of Saccharomyces cerevisiae. Yeast, 14, 1471 1510.
10. De Backer, M.D., Ilyina, T., Ma, X.-J., Vandoninck, S., Luyten, W.H.M.L. Bossche, H.V. (2001) Genomic profiling of the response of Candida albicans to itraconazole treatment using a DNA microarray. Antimicrob. Agents Chemother. 45, 1660 1670.
11. De Waard, M.A., Andrade, A.C., Hayashi, K., Schoonbeek, H.-J., Stergiopoulos, I. Zwiers, L.-H. (2006) Impact of fungal drug transporters on fungicide sensitivity, multidrug resistance and virulence. Pest Manag. Sci. 62, 195 207.
12. Delye, C., Bousset, L. Corio-Costet, M.F. (1998) PCR cloning and detection of point mutations in the eburicol 14a-demethylase (CYP51) gene from Erysiphe graminis f. sp. hordei, a 'recalcitrant' fungus. Curr. Genet. 34, 399 403.
13. Delye, C., Laigret, F. Corio-Costet, M.F. (1997) A mutation in the sterol 14a-demethylase gene in Uncinular necator that correlates with resistance to sterol biosynthesis inhibitors. Appl. Environ. Microbiol. 63, 2966 2970.
14. Eisen, M.B., Spellman, P.T., Brown, P.O. Botstein, D. (1998) Cluster analysis and display of genome-wide expression patterns. Proc. Natl Acad. Sci. USA, 95, 14863 14868.
15. Ferreira, M.E.D.S., Malavazi, I., Savoldi, M., Brakhage, A.A., Goldman, M.H.S., Kim, H.S., Nierman, W.C. Goldman, G.H. (2006) Transcriptome analysis of Aspergillus fumigatus exposed to voriconazole. Curr. Genet. 50, 32 44.
16. Fraaije, B.A., Cools, H.J., Fountaine, J., Lovell, D.J., Motteram, J., West, J.S. Lucas, J.A. (2005) The role of ascospores in further spread of QoI-resistant cytochrome b alleles (G143A) in field populations of Mycosphaerella graminicola. Phytopathology, 95, 933 941.
17. Fraaije, B.A., Cools, H.J., Kim, S.-H., Motteram, J., Clark, W.S. Lucas, J.A. (2007) A novel substitution I381V in the sterol 14a-demethylase (CYP51) of Mycosphaerella graminicola is differentially selected by azole fungicides. Mol. Plant Pathol, 8, 245 254.
18. Fraaije, B.A., Lucas, J.A., Clark, W.S. Burnett, F.J. (2003) QoI resistance development in populations of cereal pathogens in the UK. In : Proceedings of the BCPC Congress, Crop Science and Technology 2005, 2. Alton, UK : BCPC, pp. 689 694.
19. Hamamoto, H., Hasegawa, K., Nakaune, R., Lee, J.L., Makizumi, Y., Akutsu, K. Hibi, T. (2000) Tandem repeat of a transcriptional enhancer upstream of the sterol 14a-demethylase gene (CYP51) in Penicillium digitatum. Appl. Environ. Microbiol. 66, 3421 3426.
20. Hardwick, N.V., Jones, D.R. Royle, D.J. (2001) Factors affecting diseases of winter wheat in England and Wales, 1989-1998. Plant Pathol. 50, 453 462.
21. Hernaez, M.L., Gil, C., Pla, J. Nombela, C. (1998) Induced expression of the Candia albicans multidrug resistance gene CDR1 in response to fluconazole and other antifungals. Yeast, 14, 517 526.
22. Jia, M.H., Larossa, R.A., Lee, J.-M., Rafalski, A., DeRose, E., Gonje, G. Xue, Z. (2000) Global expression profiling of yeast treated with an inhibitor of amino acid biosynthesis, sulfometuron methyl. Physiol. Genom. 3, 83 82.
23. Kelly, S.L., Lamb, D.C. Kelly, D.E. (1999) Y132H substitution in Candida albicans sterol 14a-demethylase confers fluconazole resistance by preventing binding to haem. FEMS Microbiol. Lett. 180, 171 175.
24. Kenna, S., Bligh, H.F.J., Watson, P.F. Kelly, S.L. (1989) Genetic and physiological analysis of azole sensitivity in Saccharomyces cerevisiae. J. Med. Vet. Mycol. 27, 397 406.
25. Keon, J., Rudd, J.J., Antoniw, J., Skinner, W., Hargreaves, J. Hammond-Kosack, K. (2005a) Analysis of expressed sequence tags from the wheat leaf blotch pathogen Mycosphaerella graminicola (anamorph Septoria tritici). Fungal Genet. Biol. 42, 376 389.
26. Keon, J., Rudd, J.J., Antoniw, J., Skinner, W., Hargreaves, J. Hammond-Kosack, K. (2005b) Metabolic and stress adaptation by Mycosphaerella graminicola during sporulation in its host revealed through microarray transcription profiling. Mol. Plant. Pathol. 6, 527 540.
27. Kontoyiannis, D.P. May, G.S. (2001) Identification of azole-responsive genes by microarray technology: why are we missing all the efflux transporter genes? Antimicrob. Agents Chemother. 45, 3674 3676.
28. Lamb, D.C., Kelly, D.E., White, T.C. Kelly, S.L. (2000) The R467K amino acid substitution in Candida albicans sterol 14a-demethylase causes drug resistance through reduced affinity. Antimicrob. Agents Chemother. 44, 63 67.
29. Lengeler, K.B., Fox, D.S., Fraser, J.A., Allen, A., Forrester, K., Dietrich, F.S. Heitman, J. (2002) Mating-type locus of Cryptococcus neoformans: a step in the evolution of sex chromosomes. Eukaryot. Cell, 1, 704 718.
30. Liu, T.T., Lee, R.E.B., Barker, K.S., Lee, R.E., Wei, L., Homayouni, R. Rogers, P.D. (2005) Genome-wide expression profiling of the response to azole, polyene, echinocandin, and pyrimidine antifungal agents in Candida albicans. Antimicrob. Agents Chemother. 49, 2226 2236.
31. Ludin, K.M., Hilti, N. Schweingruber, M.E. (1995) Schizosaccharomyces- pombe rds1, an adenine-repressible gene regulated by glucose, ammonium, phosphate, carbon-dioxide and temperature. Mol. Gen. Genet. 248, 439 445.
32. Melin, P., Schnurer, J. Wagner, E.G. (2002) Proteome analysis of Aspergillus nidulans reveals proteins associated with the response to the antibiotic concanamycin A, produced by Streptomyces species. Mol. Genet. Genomics, 267, 695 702.
33. Muller, P.Y., Janovjak, H., Miserez, A.R. Dobbie, Z. (2002) Processing of gene expression data generated by quantitative real-time RT-PCR. Biotechniques, 32, 1372 1379.
34. Nakaune, R., Adachi, K., Nawata, O., Tomiyama, M., Akutsu, K. Hibi, H. (1998) A novel ATP-binding cassette transporter involved in multidrug resistance in the phytopathogenic fungus Penicillium digitatum. Appl. Environ. Microbiol. 64, 3983 3988.
35. Nourani, A., Wesolowski-Louvel, M., Delaveau, T., Jacq, C. Delahodde, A. (1997) Multiple-drug-resistance phenomenon in the yeast Saccharomyces cerevisiae: involvement of two hexose transporters. Mol. Cell. Biol. 17, 5453 5460.
36. Perea, S., Lopez-Ribot, J.L., Kirkpatrick, W.R., McAtee, R.K., Santillan, R.A., Martinez, M., Calabrese, D., Sanglard, D. Patterson, T.F. (2001) Prevalence of molecular mechanisms of resistance to azole antifungal agents in Candida albicans strains displaying high-level fluconazole resistance isolated from human immunodeficiency virus-infected patients. Antimicrob. Agents Chemother. 45, 2676 2684.
37. Qiu, X., Guan, P., Wang, M.-L., Moore, P.H., Zhu, Y.J., Hu, J., Borth, W. Albert, H.H. (2004) Identification and expression analysis of BTH induced genes in papaya. Physiol. Mol. Plant Pathol. 65, 21 30.
38. Rogers, P.D. Barker, K.S. (2003) Genome-wide expression profile analysis reveals coordinately regulated genes associated with stepwise acquisition of azole resistance in Candida albicans clinical isolates. Antimicrob. Agents Chemother. 47, 1220 1227.
39. Sanglard, D., Ischer, F. Bille, J. (2001) Role of ATP binding-cassette transporter genes in high-frequency acquisition of resistance to azole antifungals in Candida glabrata. Antimicrob. Agents Chemother. 45, 1174 1183.
40. Sanglard, D., Ischer, F., Koymans, L. Billie, J. (1998) Amino acid substitutions in the cytochrome P450 lanosterol 14a-demethylase (CYP51A1) from azole-resistant Candida albicans clinical isolates contribute to resistance to antifungal agents. Antimicrob. Agents Chemother. 42, 241 253.
41. Schnabel, G. Jones, A.L. (2001) The 14a-demethylase (CYP51A1) gene is overexpressed in Venturia inaequalis strains resistant to myclobutanil. Phytopathology, 91, 102 110.
42. Shigematsu, M.L., Uno, J. Arai, T. (1982) Effect of ketoconazole on isolated mitocondria from Candida albicans. Antimicrob. Agents Chemother. 21, 919 924.
43. Stergiopoulos, I., Van Nistelrooy, J.G.M., Kema, G.H.J. De Waard, M.A. (2003) Multiple mechanisms account for variation in base-line sensitivity to azole fungicides in field isolates of Mycosphaerella graminicola. Pest Manag. Sci. 59, 1333 1343.
44. Vera, J.C., Castillo, G.R. Rosen, O.M. (1991) A possible role for a mammalian facilitative hexose transporter in the development of resistance to drugs. Mol. Cell. Biol. 11, 3407 3418.
45. White, T.C. (1997) Increased mRNA levels of ERG16, CDR and MDR1 correlate with increases in azole resistance in Candida albicans isolates from a patient infected with human immunodeficiency virus. Antimicrob. Agents Chemother. 41, 1482 1487.
46. Wyand, R.A. Brown, J.K.M. (2005) Sequence variation in the CYP51 gene of Blumeria graminis associated with resistance to sterol demethylase inhibiting fungicides. Fungal Genet. Biol. 42, 726 735.
47. Zwiers, L.-H., Stergiopoulos, I., Van Nistelrooy, J.G.M. De Waard, M.A. (2002) ABC transporters and azole sensitivity in laboratory strains of the wheat pathogen Mycosphaerella graminicola. Antimicrob. Agents Chemother. 46, 3900 3906.