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Gene transcription profiling of Fusarium graminearum treated with an azole fungicide tebuconazole

  • Genomics and Proteomics
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Abstract

Using a deep serial analysis of gene expression (DeepSAGE) sequencing approach, we profiled the transcriptional response of Fusarium graminearum to tebuconazole, a most widely used azole fungicide. By comparing the expression of genes in F. graminearum treated and untreated with tebuconazole, we identified 324 and 155 genes showing more than a 5-fold increase and decrease, respectively, in expression upon tebuconazole treatment. These genes are involved in a variety of cell functions including egrosterol biosynthesis, transcription, and cellular metabolism. The validity of DeepSAGE results were confirmed by real-time PCR analysis of expression of 20 genes with different expression levels in the DeepSAGE analysis. The results from this study provide useful information in understanding the mechanisms for the responses of F. graminearum to azole fungicides.

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References

  • Audic S, Claverie JM (1997) The significance of digital gene expression profiles. Genome Res 7:986–995

    CAS  Google Scholar 

  • Bammert GF, Fostel JM (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

    Article  CAS  Google Scholar 

  • Blandino M, Minelli L, Reyneri A (2006) Strategies for the chemical control of Fusarium head blight: effect on yield, alveographic parameters and deoxynivalenol contamination in winter wheat grain. Eur J Agron 25:193–201

    Article  CAS  Google Scholar 

  • Cools HJ, Fraaije BA, Bean TP, Antoniw J, Lucas JA (2007) Transcriptome profiling of the response of Mycosphaerella graminicola isolates to an azole fungicide using cDNA microarrays. Mol Plant Pathol 5:639–650

    Article  Google Scholar 

  • Cuomo CA, Guldener U, Xu JR, Trail F, Turgeon BG, Di Pietro A, Walton DJ, Ma LJ, Baker SE, Rep M, Adam G, Antoniw J, Baldwin T, Calvo S, Chang Y, DeCaprio D, Gale LR, Gnerre S, Goswami RS, Hammond-Kosack K, Harris LJ, Hilburn K, Kennell JC, Kroken S, Magnuson JK, Mannhaupt G, Mauceli E, Mewes H, Mitterbauer R, Muehlbauer G, Münsterkötter M, Nelson D, O’Donnell K, Ouellet T, Qi W, Quesneville H, Roncero MIG, Seong K, Tetko IV, Urban M, Waalwijk C, Ward TJ, Yao J, Birren BW, Kistler HC (2007) The Fusarium graminearum genome reveals a link between localized polymorphism and pathogen specialization. Science 317:1400–1402

    Article  CAS  Google Scholar 

  • De Backer MD, Ilyina T, Ma X, Vandoninck S, Luyten WHM, Bossche HV (2001) Genomic profiling of the response of Candida albicans to itraconazole treatment using a DNA microarray. Antimicrob Agents Chemother 45:1660–1670

    Article  Google Scholar 

  • De Waard MA, Andrade AC, Hayashi K, Schoonbeek H, Stergiopoulos I, Zwiers L (2006) Impact of fungal drug transporters on fungicide sensitivity, multidrug resistance and virulence. Pest Mange Sci 62:195–207

    Article  Google Scholar 

  • Ferreira MED, Malavazi I, Savoldi M, Brakhage AA, Goldman MHS, Kim HS, Nierman WC, Goldman GH (2006) Transcriptome analysis of Aspergillus fumigatus exposed to voriconazole. Curr Genet 50:32–44

    Article  CAS  Google Scholar 

  • Hanriot L, Keime C, Gay N, Faure C, Dossat C, Wincker P, Scoté-Blachon C, Peyron C, Gandrillon O (2008) A combination of LongSAGE with Solexa sequencing is well suited to explore the depth and the complexity of transcriptome. BMC Genomics 9:418

    Article  Google Scholar 

  • Hoen PAC, Ariyurek Y, Thygesen HH, Vreugdenhil E, Vossen RHA, de Menezes RX, Boer J, van Ommen GB, den Dunnen JT (2008) Deep sequencing-based expression analysis shows major advances in robustness, resolution and inter-lab portability over five microarray platforms. Nucleic Acids Res 36:e141

    Article  Google Scholar 

  • Irizarry RA, Warren D, Spencer F, Kim IF, Biswal S, Frank BC, Gabrielson E, Garcia JG, Geoghegan J, Germino G et al (2005) Multiple-laboratory comparison of microarray platforms. Nat Methods 2:345–350

    Article  CAS  Google Scholar 

  • Jensen-Pergakes KL, Kennedy MA, Lees ND, Baruuch R, Koegel C, Bard M (1998) Sequencing, disruption, and characterization of the Candida albicans sterol methyltransferase (ERG6) gene: drug susceptibility studies in erg6 mutants. Antimicrob Agents Chemother 42:1160–1167

    CAS  Google Scholar 

  • Jongeneel CV, Iseli C, Stevenson BJ, Riggins GJ, Lal A, Mackay A, Harris RA, Ơhare MJ, Neville AM, Simpson AJG, Strausberg RL (2003) Comprehensive sampling of gene expression in human cell lines with massively parallel signature sequencing. Proc Natl Acad Sci USA 100:4702–4705

    Article  CAS  Google Scholar 

  • Kagan IA, Michel A, Prause A, Scheffler BE, Pace P, Duke SO (2005) Gene transcription profiles of Saccharomyces cerevisiae after treatment with plant protection fungicides that inhibit ergosterol biosynthesis. Pesticide Biochem Physiol 82:133–153

    Article  CAS  Google Scholar 

  • Khan R, Tan R, Mariscal AG, Straney D (2003) A binuclear zinc transcription factor binds the host isoflavonoid-responsive element in a fungal cytochrome p450 gene responsible for detoxification. Mol Microbiol 49:117–130

    Article  CAS  Google Scholar 

  • Lechoczki-Krsjak S, Toth B, Kotai C, Martonosi I, Farady L, Kondrak L, Szabo-Hever A, Mesterhazy A (2008) Chemical control of FHB in wheat with different nozzle types and fungicides. Cereal Res Commun 36:677–681

    Article  CAS  Google Scholar 

  • Leroux P, Albertini C, Gautier A, Gredt M, Walker AS (2007) Mutations in the CYP51 gene correlated with changes in sensitivity to sterol 14 α-demethylation inhibitors in field isolates of Mycosphaerella graminicola. Pest Manag Sci 63:688–698

    Article  CAS  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2–ΔΔCt method. Methods 25:402–408

    Article  CAS  Google Scholar 

  • Luo CX, Schnabel G (2007) The cytochrome P450 lanosterol 14 α-demethylase gene is a demethylation inhibitor fungicide resistance determinant in Monilinia fructicola field isolates from Georgia. Appl Environ Microbiol 74:359–366

    Article  Google Scholar 

  • Lupetti A, Danesi R, Campa M, del Tacca M, Kelly S (2002) Molecular basis of resistance to azole antifungals. Trends Mol Med 8:76–81

    Article  CAS  Google Scholar 

  • Ma Z, Michailides TJ (2005) Advances in understanding molecular mechanisms of fungicide resistance and molecular detection of resistant genotypes in phytopathogenic fungi. Crop Prot 24:853–863

    Article  CAS  Google Scholar 

  • MacPherson S, Akache B, Weber S, De Deken W, Raymond M, Turcotte B (2005) Candida albicans zinc cluster protein Upc2p confers resistance to antifungal drugs and is an activator of ergosterol biosynthetic genes. Antomicrob Agent Chemother 49:1745–1752

    Article  CAS  Google Scholar 

  • Margulies M, Egholm M, Altman WE, Attiya S, Bader JS, Bemben LA, Berka J, Braverman MS, Chen YJ, Chen Z et al (2005) Genome sequencing in microfabricated high-density picolitre reactors. Nature 437:376–380

    CAS  Google Scholar 

  • Morozova O, Marra MA (2008) Applications of next-generation sequencing technologies in functional genomics. Genomics 92:255–264

    Article  CAS  Google Scholar 

  • Nicot N, Hausman JF, Hoffmann L, Evers D (2005) Housekeeping gene selection for real-time RT-PCR normalization in potato during biotic and abiotic stress. J Exp Bot 421:2907–2914

    Article  Google Scholar 

  • Nielsen K, Høgh AL, Emmersen J (2006) DeepSAGE-digital transcriptomics with high sensitivity, simple experimental protocol and multiplexing of samples. Nucleic Acids Res 34:e133

    Article  Google Scholar 

  • Romualdi C, Bortoluzzi S, d’Alessi F, Danieli A (2003) IDEG6: a web tool for detection of differentially expressed genes in multiple tag sampling experiments. Physiol Genomics 12:159–162

    CAS  Google Scholar 

  • Shendure J, Porreca GJ, Reppas NB, Lin X, McCutcheon JP, Rosenbaum AM, Wang MD, Zhang K, Mitra RD, Church GM (2005) Accurate multiplex polony sequencing of an evolved bacterial genome. Science 309:1728–1732

    Article  CAS  Google Scholar 

  • Snijders CHA (2004) Resistance in wheat to Fusarium infection and trichothecene formation. Toxicol Lett 153:37–46

    Article  CAS  Google Scholar 

  • Vik A, Rine J (2001) Upc2p and Ecm22p, dual regulators of sterol biosynthesis in Saccharomyces cerevisiae. Mol Cell Biol 21:6395–6405

    Article  CAS  Google Scholar 

  • Wyand RA, Brown JKM (2005) Sequence variation in the CYP51 gene of Blumeria graminis associated with resistance to sterol demethylase inhibiting fungicides. Fungal Genet Biol 42:726–735

    Article  CAS  Google Scholar 

  • Xu X, Nicholson P (2009) Community ecology of fungal pathogens causing wheat head blight. Annu Rev Phytopathol 47:83–103

    Article  CAS  Google Scholar 

  • Yan L, Zhang J, Li M, Cao Y, Xu Z, Cao Y, Gao P, Wang Y, Jiang Y (2008) DNA microarray analysis of fluconazole resistance in a laboratory Candida albicans strain. Acta Biochim Biophys Sin 40:1048–1060

    Article  CAS  Google Scholar 

  • Yin Y, Liu X, Li B, Ma Z (2009) Characterization of sterol demethylation inhibitor-resistant isolates of Fusarium asiaticum and F. graminearum collected from wheat in China. Phytopathology 99:487–497

    Article  CAS  Google Scholar 

  • Yu L, Zhang W, Wang L, Yang J, Liu T, Peng J, Leng W, Chen L, Li R, Jin Q (2007) Transcriptional profiles of the response to ketoconazole and amphotericin B in Trichophyton rubrum. Antimicrob Agents Chemother 51:144–153

    Article  CAS  Google Scholar 

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Acknowledgments

The research was supported by the Special Program for Agricultural Research (nyhyzx07-048), the 863 program (2007AA10Z422), and the grant MATS from Department of Agriculture to Z. Ma.

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Correspondence to Zhonghua Ma.

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Supplementary Table 1

A list of genes up-regulated in expression by more than 5 folds in F. graminearum treated with tebuconazole at 2.5 μg/ml for six hours (DOC 57 kb)

Supplementary Table 2

A list of genes down-regulated in expression by more than 5 folds in F. graminearum treated with tebuconazole at 2.5 μg/ml for six hours (DOC 41 kb)

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Liu, X., Jiang, J., Shao, J. et al. Gene transcription profiling of Fusarium graminearum treated with an azole fungicide tebuconazole. Appl Microbiol Biotechnol 85, 1105–1114 (2010). https://doi.org/10.1007/s00253-009-2273-4

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  • DOI: https://doi.org/10.1007/s00253-009-2273-4

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