Genome-wide association study identifies novel candidate genes for aggressiveness, deoxynivalenol production, and azole sensitivity in natural field populations of Fusarium graminearum

Molecular Plant-Microbe Interactions

Volumn 29, Issue 5, 2016, Pages 417-430

  Talas, Firas ^a   Kalih, Rasha ^a   Miedaner, Thomas ^a   McDonald, Bruce A ^a  

^a NONE

Author keywords

[No Author keywords available]

Indexed keywords

FUNGAL PROTEIN; FUNGICIDE; PROPICONAZOLE; TRIAZOLE DERIVATIVE; TRICHOTHECENE DERIVATIVE; VOMITOXIN;

BIOSYNTHESIS; DRUG EFFECTS; FUSARIUM; GENE EXPRESSION REGULATION; GENETICS; GENOME-WIDE ASSOCIATION STUDY; METABOLISM; PHYSIOLOGY; QUANTITATIVE TRAIT LOCUS;

FUNGAL PROTEINS; FUNGICIDES, INDUSTRIAL; FUSARIUM; GENE EXPRESSION REGULATION, FUNGAL; GENOME-WIDE ASSOCIATION STUDY; QUANTITATIVE TRAIT LOCI; TRIAZOLES; TRICHOTHECENES;

EID: 84968649151     PISSN: 08940282     EISSN: None     Source Type: Journal    
DOI: 10.1094/MPMI-09-15-0218-R     Document Type: Article

References (82)

1. Baird, N. A., Etter, P. D., Atwood, T. S., Currey, M. C., Shiver, A. L., Lewis, Z. A., Selker, E. U., Cresko, W. A., and Johnson, E. A. 2008. Rapid SNP discovery and genetic mapping using sequenced RAD markers. PLoS One 3:e3376.
2. Barrett, R. D. H., and Hoekstra, H. E. 2011. Molecular spandrels: Tests of adaptation at the genetic level. Nat. Rev. Genet. 12:767-780.
3. Bartels, D. J., Mitchell, D. A., Dong, X., and Deschenes, R. J. 1999. Erf2, a novel gene product that affects the localization and palmitoylation of Ras2 in Saccharomyces cerevisiae. Mol. Cell. Biol. 19:6775-6787.
4. Becher, R., Miedaner, T., and Wirsel, S. G. R. 2013. Biology, diversity, and management of FHB-causing Fusarium species in small-grain cereals. Page 199-241 in: Agricultural Applications. F. Kempken, ed. Springer, Heidelberg.
5. Becher, R., Weihmann, F., Deising, H. B., and Wirsel, S. G. 2011. Development of a novel multiplex DNA microarray for Fusarium graminearum and analysis of azole fungicide responses. BMC Genomics 12:52.
6. Belenky, P., Camacho, D., and Collins, J. J. 2013. Fungicidal drugs induce a common oxidative-damage cellular death pathway. Cell Reports 3:350-358.
7. Benjamini, Y., and Hochberg, Y. 1995. Controlling the false discovery rate-A practical and powerful approach to multiple testing. J. R. Stat. Soc. 57:289-300.
8. Bluhm, B. H., Zhao, X., Flaherty, J. E., Xu, J. R., and Dunkle, L. D. 2007. RAS2 regulates growth and pathogenesis in Fusarium graminearum. Mol. Plant-Microbe Interact. 20:627-636.
9. Boenisch, M. J., and Schäfer, W. 2011. Fusarium graminearum forms mycotoxin producing infection structures on wheat. BMC Plant Biol. 11: 110.
10. Bolger, A. H., Lohse, M., and Usadel, B. 2014. Trimmomatic A flexible trimmer for illumina sequence data. Bioinformatics 30:2114-2120.
11. Brinkmann, U., Brinkmann, E., Gallo, M., Scherf, U., and Pastan, I. 1996. Role of CAS, a human homologue to the yeast chromosome segregation gene CSE1, in toxin and tumor necrosis factor mediated apoptosis. Biochemistry 35:6891-6899.
12. Brunner, P. C., Stefanato, F. L., and McDonald, B. A. 2008. Evolution of the CYP51 gene in Mycosphaerella graminicola: Evidence for intragenic recombination and selective replacement. Mol. Plant Pathol. 9:305-316.
13. Burke, M. K., King, E. G., Shahrestani, P., Rose, M. R., and Long, A. D. 2014. Genome-wide association study of extreme longevity in Drosophila melanogaster. Genome Biol. Evol. 6:1-11.
14. Cannon, R. D., Lamping, E., Holmes, A. R., Niimi, K., Baret, P. V., Keniya, M. V., Tanabe, K., Niimi, M., Goffeau, A., and Monk, B. C. 2009. Effluxmediated antifungal drug resistance. Clin. Microbiol. Rev. 22:291-321.
15. Chayakulkeeree, M., Rude, T. H., Toffaletti, D. L., and Perfect, J. R. 2007. Fatty acid synthesis is essential for survival of Cryptococcus neoformans and a potential fungicidal target. Antimicrob. Agents Chemother. 51: 3537-3545.
16. Coleman, J. J., and Mylonakis, E. 2009. Efflux in fungi: La pièce de résistance. PLoS Pathog. 5:e1000486.
17. Cuomo, C. A., Güldener, U., Xu, J. R., Trail, F., Turgeon, B. G., Di Pietro, A., Walton, J. D., Ma, L. J., Baker, S. E., Rep, M., Adam, G., Antoniw, J., Baldwin, T., Calvo, S., Chang, Y. L., Decaprio, D., Gale, L. R., Gnerre, S., Goswami, R. S., Hammond-Kosack, K., Harris, L. J., Hilburn, K., Kennell, J. C., Kroken, S., Magnuson, J. K., Mannhaupt, G., Mauceli, E., Mewes, H. W., Mitterbauer, R., Muehlbauer, G., Münsterkötter, M., Nelson, D., O'donnell, K., Ouellet, T., Qi, W., Quesneville, H., Roncero, M. I., Seong, K. Y., Tetko, I. V., Urban, M., Waalwijk, C., Ward, T. J., Yao, J., Birren, B. W., and Kistler, H. C. 2007. The Fusarium graminearum genome reveals a link between localized polymorphism and pathogen specialization. Science 317:1400-1402.
18. da Silva, M. V. G. B., Van Tassell, C. P., Sonstegard, T. S., Cobuci, J. A., and Gasbarre, L. C. 2011. Box-Cox transformation and random regression models for fecal egg count data. Front. Genet. 2:112.
19. Dalman, K., Himmelstrand, K., Olson, Å., Lind, M., Brandstrom-Durling, M., and Stenlid, J. 2013. A genome-wide association study identifies genomic regions for virulence in the non-model organism Heterobasidion annosum s.s. PLoS One 8:e53525.
20. Danecek, P., Auton, A., Abecasis, G., Albers, C. A., Banks, E., DePristo, M. A., Handsaker, R. E., Lunter, G., Marth, G. T., Sherry, S. T., McVean, G., and Durbin, R.; 1000 Genomes Project Analysis Group. 2011. The variant call format and VCFtools. Bioinformatics 27:2156-2158.
21. Dubos, T., Pasquali, M., Pogoda, F., Hoffmann, L., and Beyer, M. 2011. Evidence for natural resistance towards trifloxystrobin in Fusarium graminearum. Eur. J. Plant Pathol. 130:239-248.
22. Fehr, W. R. 1987. Principles of Cultivar Development. Macmillan, New York.
23. Finn, R. D., Bateman, A., Clements, J., Coggill, P., Eberhardt, R. Y., Eddy, S. R., Heger, A., Hetherington, K., Holm, L., Mistry, J., Sonnhammer, E. L. L., Tate, J., and Punta, M. 2014. Pfam: The protein families database. Nucleic Acids Res. 42:D222-D230.
24. Floyd, J. L., Smith, K. P., Kumar, S. H., Floyd, J. T., and Varela, M. F. 2010. LmrS is a multidrug efflux pump of the major facilitator superfamily from Staphylococcus aureus. Antimicrob. Agents Chemother. 54:5406-5412.
25. Frazer, K. A., Murray, S. S., Schork, N. J., and Topol, E. J. 2009. Human genetic variation and its contribution to complex traits. Nat. Rev. Genet. 10:241-251.
26. Frishman, D., Mokrejs, M., Kosykh, D., Kastenmüller, G., Kolesov, G., Zubrzycki, I., Gruber, C., Geier, B., Kaps, A., Albermann, K., Volz, A., Wagner, C., Fellenberg, M., Heumann, K., and Mewes, H. W. 2003. The PEDANT genome database. Nucleic Acids Res. 31:207-211.
27. Frohner, I. E., Bourgeois, C., Yatsyk, K., Majer, O., and Kuchler, K. 2009. Candida albicans cell surface superoxide dismutases degrade hostderived reactive oxygen species to escape innate immune surveillance. Mol. Microbiol. 71:240-252.
28. Gaffoor, I., Brown, D. W., Plattner, R., Proctor, R. H., Qi, W., and Trail, F. 2005. Functional analysis of the polyketide synthase genes in the filamentous fungus Gibberella zeae (anamorph: Fusarium graminearum). Eukaryot. Cell 4:1926-1933.
29. Grose, J. H., Smith, T. L., Sabic, H., and Rutter, J. 2007. Yeast PAS kinase coordinates glucose partitioning in response to metabolic and cell integrity signaling. EMBO (Eur. Mol. Biol. Organ.) J. 26:4824-4830.
30. Harashima, T., Anderson, S., Yates, J. R., 3rd, and Heitman, J. 2006. The kelch proteins Gpb1 and Gpb2 inhibit Ras activity via association with the yeast RasGAP neurofibromin homologs Ira1 and Ira2. Mol. Cell 22:819-830.
31. Hochberg, Y. 1988. A sharper Bonferroni procedure for multiple tests of significance. Biometrika 75:800-802.
32. Hohenlohe, P. A., Bassham, S., Etter, P. D., Stiffler, N., Johnson, E. A., and Cresko, W. A. 2010. Population genomics of parallel adaptation in threespine stickleback using sequenced RAD tags. PLoS Genet. 6:e1000862.
33. Hou, Z., Xue, C., Peng, Y., Katan, T., Kistler, H. C., and Xu, J.-R. 2002. A mitogen-activated protein kinase gene (MGV1) in Fusarium graminearum is required for female fertility, heterokaryon formation, and plant infection. Mol. Plant-Microbe Interact. 15:1119-1127.
34. Hunt, M. C., and Alexson, S. E. H. 2002. The role Acyl-CoA thioesterases play in mediating intracellular lipid metabolism. Prog. Lipid Res. 41: 99-130.
35. Kang, H. M., Zaitlen, N. A., Wade, C. M., Kirby, A., Heckerman, D., Daly, M. J., and Eskin, E. 2008. Efficient control of population structure in model organism association mapping. Genetics 178:1709-1723.
36. King, R., Urban, M., Hammond-Kosack, M. C. U., Hassani-Pak, K., and Hammond-Kosack, K. E. 2015. The completed genome sequence of the pathogenic ascomycete fungus Fusarium graminearum. BMC Genomics 16:544.
37. Langmead, B., and Salzberg, S. 2012. Fast gapped-read alignment with Bowtie 2. Nat. Method 9:357-359.
38. Lawler, K., Hammond-Kosack, K., Brazma, A., and Coulson, R. M. R. 2013. Genomic clustering and co-regulation of transcriptional networks in the pathogenic fungus Fusarium graminearum. BMC Syst. Biol. 7:52.
39. Lee, N., and Kronstad, J. W. 2002. ras2 Controls morphogenesis, pheromone response, and pathogenicity in the fungal pathogen Ustilago maydis. Eukaryot. Cell 1:954-966.
40. Legrand, M., Chan, C. L., Jauert, P. A., and Kirkpatrick, D. T. 2007. Role of DNA mismatch repair and double-strand break repair in genome stability and antifungal drug resistance in Candida albicans. Eukaryot. Cell 6:2194-2205.
41. Li, H., Handsaker, B., Wysoker, A., Fennell, T., Ruan, J., Homer, N., Marth, G., Abecasis, G., Durbin, R., and 1000 Genome Project Data Processing Subgroup. 2009. The sequence alignment/map (SAM) format and SAMtools. Bioinformatics 25:2078-2079.
42. Lipka, A. E., Tian, F., Wang, Q., Peiffer, J., Li, M., Bradbury, P. J., Gore, M. A., Buckler, E. S., and Zhang, Z. 2012. GAPIT: Genome association and prediction integrated tool. Bioinformatics 28:2397-2399.
43. Massman, J., Cooper, B., Horsley, R., Neate, S., Dill-Macky, R., Chao, S., Dong, Y., Schwarz, P., Muehlbauer, G. J., and Smith, K. P. 2010. Genome-wide association mapping of Fusarium head blight resistance in contemporary barley breeding germplasm. Mol. Breed. 27:439-454.
44. McCarthy, M. I., Abecasis, G. R., Cardon, L. R., Goldstein, D. B., Little, J., Ioannidis, J. P. A., and Hirschhorn, J. N. 2008. Genome-wide association studies for complex traits: Consensus, uncertainty and challenges. Nat. Rev. Genet. 9:356-369.
45. McCormick, S. P., Harris, L. J., Alexander, N. J., Ouellet, T., Saparno, A., Allard, S., and Desjardins, A. E. 2004. Tri1 in Fusarium graminearum encodes a P450 oxygenase. Appl. Environ. Microbiol. 70:2044-2051.
46. McCormick, S. P., Stanley, A. M., Stover, N. A., and Alexander, N. J. 2011. Trichothecenes: From simple to complex mycotoxins. Toxins (Basel) 3:802-814.
47. McKenna, A., Hanna, M., Banks, E., Sivachenko, A., Cibulskis, K., Kernytsky, A., Garimella, K., Altshuler, D., Gabriel, S., Daly, M., and DePristo, M. A. 2010. The genome analysis toolkit: A MapReduce framework for analyzing next-generation DNA sequencing data. Genome Res. 20:1297-1303.
48. Meek, I. B., Peplow, A. W., Jr., Ake, C., Jr., Phillips, T. D., and Beremand, M. N. 2003. Tri1 encodes the cytochrome P450 monooxygenase for C-8 hydroxylation during trichothecene biosynthesis in Fusarium sporotrichioides and resides upstream of another new Tri gene. Appl. Environ. Microbiol. 69:1607-1613.
49. Menke, J., Dong, Y., and Kistler, H. C. 2012. Fusarium graminearum Tri12p influences virulence to wheat and trichothecene accumulation. Mol. Plant-Microbe Interact. 25:1408-1418.
50. Muller, L. A. H., Lucas, J. E., Georgianna, D. R., and McCusker, J. H. 2011. Genome-wide association analysis of clinical vs. nonclinical origin provides insights into Saccharomyces cerevisiae pathogenesis. Mol. Ecol. 20:4085-4097.
51. Nelson, R. M., Pettersson, M. E., Li, X., and Carlborg, Ö. 2013. Variance heterogeneity in Saccharomyces cerevisiae expression data: Transregulation and epistasis. PLoS One 8:e79507.
52. Palma-Guerrero, J., Hall, C. R., Kowbel, D., Welch, J., Taylor, J.W., Brem, R. B., and Glass, N. L. 2013. Genome wide association identifies novel loci involved in fungal communication. PLoS Genet. 9:e1003669.
53. Pettit, L. J., Browne, H. P., Yu, L., Smits, W. K., Fagan, R. P., Barquist, L., Martin, M. J., Goulding, D., Duncan, S. H., Flint, H. J., Dougan, G., Choudhary, J. S., and Lawley, T. D. 2014. Functional genomics reveals that Clostridium difficile Spo0A coordinates sporulation, virulence and metabolism. BMC Genomics 15:160.
54. Pohl, C. H., Kock, J., and Thibane, V. S. 2011. Antifungal free fatty acids: A review. Pages 693-1348 in: Science Against Microbial Pathogens: Communicating Current Research and Technology Advances. A. Mendez-Vilas, ed. Formatex Research Center, Badajoz, Spain.
55. Purcell, S., Neale, B., Todd-Brown, K., Thomas, L., Ferreira, M. A. R., Bender, D., Maller, J., Sklar, P., de Bakker, P. I. W., Daly, M. J., and Sham, P. C. 2007. PLINK: A tool set for whole-genome association and population-based linkage analyses. Am. J. Hum. Genet. 81:559-575.
56. Qin, J., Wang, G., Jiang, C., Xu, J.-R., and Wang, C. 2015. Fgk3 glycogen synthase kinase is important for development, pathogenesis, and stress responses in Fusarium graminearum. Sci. Rep. 5:8504.
57. Rietveld, C. A., Medland, S. E., Derringer, J., Yang, J., Esko, T., Martin, N. W., Westra, H.-J., Shakhbazov, K., Abdellaoui, A., Agrawal, A., Albrecht, E., Alizadeh, B. Z., Amin, N., Barnard, J., Baumeister, S. E., Benke, K. S., Bielak, L. F., Boatman, J. A., Boyle, P. A., Davies, G., de Leeuw, C., Eklund, N., Evans, D. S., Ferhmann, R., Fischer, K., Gieger, C., Gjessing, H. K., Hägg, S., Harris, J. R., Hayward, C., Holzapfel, C., Ibrahim-Verbaas, C. A., Ingelsson, E., Jacobsson, B., Joshi, P. K., Jugessur, A., Kaakinen, M., Kanoni, S., Karjalainen, J., Kolcic, I., Kristiansson, K., Kutalik, Z., Lahti, J., Lee, S. H., Lin, P., Lind, P. A., Liu, Y., Lohman, K., Loitfelder, M., McMahon, G., Vidal, P. M., Meirelles, O., Milani, L., Myhre, R., Nuotio, M. L., Oldmeadow, C. J., Petrovic, K. E., Peyrot, W. J., Polasek, O., Quaye, L., Reinmaa, E., Rice, J. P., Rizzi, T. S., Schmidt, H., Schmidt, R., Smith, A. V., Smith, J. A., Tanaka, T., Terracciano, A., van der Loos, M. J., Vitart, V., Völzke, H., Wellmann, J., Yu, L., Zhao, W., Allik, J., Attia, J. R., Bandinelli, S., Bastardot, F., Beauchamp, J., Bennett, D. A., Berger, K., Bierut, L. J., Boomsma, D. I., Bültmann, U., Campbell, H., Chabris, C. F., Cherkas, L., Chung, M. K., Cucca, F., de Andrade, M., De Jager, P. L., De Neve, J. E., Deary, I. J., Dedoussis, G. V., Deloukas, P., Dimitriou, M., Eiríksdóttir, G., Elderson, M. F., Eriksson, J. G., Evans, D. M., Faul, J. D., Ferrucci, L., Garcia, M. E., Grönberg, H., Gudnason, V., Hall, P., Harris, J. M., Harris, T. B., Hastie, N. D., Heath, A. C., Hernandez, D. G., Hoffmann, W., Hofman, A., Holle, R., Holliday, E. G., Hottenga, J. J., Iacono, W. G., Illig, T., Järvelin, M. R., Kähönen, M., Kaprio, J., Kirkpatrick, R. M., Kowgier, M., Latvala, A., Launer, L. J., Lawlor, D. A., Lehtimäki, T., Li, J., Lichtenstein, P., Lichtner, P., Liewald, D. C., Madden, P. A., Magnusson, P. K., Mäkinen, T. E., Masala, M., McGue, M., Metspalu, A., Mielck, A., Miller, M. B., Montgomery, G. W., Mukherjee, S., Nyholt, D. R., Oostra, B. A., Palmer, L. J., Palotie, A., Penninx, B. W., Perola, M., Peyser, P. A., Preisig, M., Räikkönen, K., Raitakari, O. T., Realo, A., Ring, S. M., Ripatti, S., Rivadeneira, F., Rudan, I., Rustichini, A., Salomaa, V., Sarin, A. P., Schlessinger, D., Scott, R. J., Snieder, H., St Pourcain, B., Starr, J. M., Sul, J. H., Surakka, I., Svento, R., Teumer, A., Tiemeier, H., van Rooij, F. J., Van Wagoner, D. R., Vartiainen, E., Viikari, J., Vollenweider, P., Vonk, J. M., Waeber, G., Weir, D. R., Wichmann, H. E., Widen, E., Willemsen, G., Wilson, J. F., Wright, A. F., Conley, D., Davey-Smith, G., Franke, L., Groenen, P. J., Hofman, A., Johannesson, M., Kardia, S. L., Krueger, R. F., Laibson, D., Martin, N. G., Meyer, M. N., Posthuma, D., Thurik, A. R., Timpson, N. J., Uitterlinden, A. G., van Duijn, C. M., Visscher, P. M., Benjamin, D. J., Cesarini, D., and Koellinger, P. D.; LifeLines Cohort Study. 2013. GWAS of 126,559 individuals identifies genetic variants associated with educational attainment. Science 340:1467-1471.
58. Riley, M. L., Schmidt, T., Artamonova, I. I., Wagner, C., Volz, A., Heumann, K., Mewes, H.-W., and Frishman, D. 2007. PEDANT genome database: 10 years online. Nucleic Acids Res. 35:D354-D357.
59. Robinson, M. R., Wray, N. R., and Visscher, P. M. 2014. Explaining additional genetic variation in complex traits. Trends Genet. 30:124-132.
60. Shlezinger, N., Goldfinger, N., and Sharon, A. 2012. Apoptotic-like programed cell death in fungi: The benefits in filamentous species. Front. Oncol. 2:97.
61. Sieber, C. M. K., Lee, W., Wong, P., Münsterkötter, M., Mewes, H.-W., Schmeitzl, C., Varga, E., Berthiller, F., Adam, G., and Güldener, U. 2014. The Fusarium graminearum genome reveals more secondary metabolite gene clusters and hints of horizontal gene transfer. PLoS One 9:e110311.
62. Stephens, A. E., Gardiner, D. M., White, R. G., Munn, A. L., and Manners, J. M. 2008. Phases of infection and gene expression of Fusarium graminearum during crown rot disease of wheat. Mol. Plant-Microbe Interact. 21:1571-1581.
63. Sun, G., Zhu, C., Kramer, M. H., Yang, S.-S., Song, W., Piepho, H. P., and Yu, J. 2010. Variation explained in mixed-model association mapping. Hered. Edinb 105:333-340.
64. Sun, J., Kale, S. P., Childress, A. M., Pinswasdi, C., and Jazwinski, S. M. 1994. Divergent roles of RAS1 and RAS2 in yeast longevity. J. Biol. Chem. 269:18638-18645.
65. Talas, F., Kalih, R., and Miedaner, T. 2012a. Within-field variation of Fusarium graminearum isolates for aggressiveness and deoxynivalenol production in wheat head blight. Phytopathology 102:128-134.
66. Talas, F., and McDonald, B. A. 2015a. Significant variation in sensitivity to a DMI fungicide in field populations of Fusarium graminearum. Plant Pathol. 64:664-670.
67. Talas, F., and McDonald, B. A. 2015b. Genome-wide analysis of Fusarium graminearum field populations reveals hotspots of recombination. BMC Genomics 16:996.
68. Talas, F., Parzies, H. K., and Miedaner, T. 2011. Diversity in genetic structure and chemotype composition of Fusarium graminearum sensu stricto populations causing wheat head blight in individual fields in Germany. Eur. J. Plant Pathol. 131:39-48.
69. Talas, F., Würschum, T., Reif, J. C., Parzies, H. K., and Miedaner, T. 2012b. Association of single nucleotide polymorphic sites in candidate genes with aggressiveness and deoxynivalenol production in Fusarium graminearum causing wheat head blight. BMC Genet. 13:14.
70. Taylor, B. L., and Zhulin, I. B. 1999. PAS domains: Internal sensors of oxygen, redox potential, and light. Microbiol. Mol. Biol. Rev. 63:479-506.
71. Varga, E., Wiesenberger, G., Hametner, C., Ward, T. J., Dong, Y., Schöfbeck, D., McCormick, S., Broz, K., Stückler, R., Schuhmacher, R., Krska, R., Kistler, H. C., Berthiller, F., and Adam, G. 2015. New tricks of an old enemy: Isolates of Fusarium graminearum produce a type A trichothecene mycotoxin. Environ. Microbiol. 17:2588-2600.
72. Voigt, C. A., Schäfer, W., and Salomon, S. 2005. A secreted lipase of Fusarium graminearum is a virulence factor required for infection of cereals. Plant J. 42:364-375.
73. Wagacha, J. M., and Muthomi, J. W. 2007. Fusarium culmorum: Infection process, mechanisms of mycotoxin production and their role in pathogenesis in wheat. Crop Prot. 26:877-885.
74. Wang, C., Zhang, S., Hou, R., Zhao, Z., Zheng, Q., Xu, Q., Zheng, D., Wang, G., Liu, H., Gao, X., Ma, J. W., Kistler, H. C., Kang, Z., and Xu, J. R. 2011. Functional analysis of the kinome of the wheat scab fungus Fusarium graminearum. PLoS Pathog. 7:e1002460.
75. Weete, J. D., Sancholle, M., and Montant, C. 1985. Effects of triazoles on fungi. II. Composition of a plasma membrane-enriched fraction of Taphrina deformans. Biochim. Biophys. Acta 812:633-642.
76. Wong, P., Walter, M., Lee, W., Mannhaupt, G., Münsterkötter, M., Mewes, H.-W., Adam, G., and Güldener, U. 2011. FGDB: Revisiting the genome annotation of the plant pathogen Fusarium graminearum. Nucleic Acids Res. 39:D637-D639.
77. Xiao, B.-Z., Chen, X., Xiang, C.-B., Tang, N., Zhang, Q.-F., and Xiong, L.-Z. 2009. Evaluation of seven function-known candidate genes for their effects on improving drought resistance of transgenic rice under field conditions. Mol. Plant 2:73-83.
78. Yang, J., Lee, S. H., Goddard, M. E., and Visscher, P. M. 2011. GCTA: A tool for genome-wide complex trait analysis. Am. J. Hum. Genet. 88:76-82.
79. Zadoks, J. C., Chang, T. T., and Konzak, C. F. 1974. A decimal code for growth stages of cereals. Weed Res. 14:415-421.
80. Zhang, C., Wang, Y., Wang, J., Zhai, Z., Zhang, L., Zheng, W., Zheng, W., Yu, W., Zhou, J., Lu, G., Shim, W.-B., and Wang, Z. 2013. Functional characterization of Rho family small GTPases in Fusarium graminearum. Fungal Genet. Biol. 61:90-99.
81. Zhang, Z., Ersoz, E., Lai, C.-Q., Todhunter, R. J., Tiwari, H. K., Gore, M. A., Bradbury, P. J., Yu, J., Arnett, D. K., Ordovas, J. M., and Buckler, E. S. 2010. Mixed linear model approach adapted for genome-wide association studies. Nat. Genet. 42:355-360.
82. Zhao, C., Waalwijk, C., de Wit, P. J. G. M., Tang, D., and van der Lee, T. 2013. RNA-Seq analysis reveals new gene models and alternative splicing in the fungal pathogen Fusarium graminearum. BMC Genomics 14:21.