The transcription factor FgStuAp influences spore development, pathogenicity, and secondary metabolism in fusarium graminearum

Molecular Plant-Microbe Interactions

Volumn 24, Issue 1, 2011, Pages 54-67

  Lysøe, Erik ^a   Pasquali, Matias ^b,c   Breakspear, Andrew ^b   Kistler, H Corby ^b,d  

^a NORWEGIAN INSTITUTE OF BIOECONOMY RESEARCH   (Norway)

^b UNIVERSITY OF MINNESOTA   (United States)

^c Centre de Recherche Public   (Luxembourg)

^d USDA Agricultural Research Service Cereal Disease Laboratory   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHITINASE; TRANSCRIPTION FACTOR;

ARTICLE; CELL CYCLE; DNA MICROARRAY; FUNGAL GENOME; FUNGUS SPORE; FUSARIUM; GENETICS; METABOLISM; MICROBIOLOGY; NEUROSPORA CRASSA; PATHOGENICITY; PLANT DISEASE; PROMOTER REGION; SACCHAROMYCES CEREVISIAE; WHEAT;

CELL CYCLE; CHITINASE; FUSARIUM; GENOME, FUNGAL; NEUROSPORA CRASSA; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PLANT DISEASES; PROMOTER REGIONS, GENETIC; SACCHAROMYCES CEREVISIAE; SPORES, FUNGAL; TRANSCRIPTION FACTORS; TRITICUM;

ASPERGILLUS; FUNGI; GIBBERELLA ZEAE; TRITICUM AESTIVUM;

EID: 78650631005     PISSN: 08940282     EISSN: None     Source Type: Journal    
DOI: 10.1094/MPMI-03-10-0075     Document Type: Article

References (60)

1. Adams, T. H., Wieser, J. K., and Yu, J. H. 1998. Asexual sporulation in Aspergillus nidulans. Microbiol. Mol. Biol. Rev. 62:35-54.
2. Anderson, A. L. 1948. The development of Gibberella zeae head blight of wheat. Phytopathology 38:595-611.
3. +, a Neurospora crassa gene related to transcriptional regulators of fungal development. Genetics 144:991-1003.
4. Bai, G. H., and Shaner, G. 1996. Variation in Fusarium graminearum and cultivar resistance to wheat scab. Plant Dis. 80:975-979.
5. Borneman, A. R., Hynes, M. J., and Andrianopoulos, A. 2002. A basic helix- loop-helix protein with similarity to the fungal morphological regulators, Phd1p, Efg1p and StuA, controls conidiation but not dimorphic growth in Penicillium marneffei. Mol. Microbiol. 44:621-631.
6. Calvo, A. M., Wilson, R. A., Bok, J. W., and Keller, N. P. 2002. Relation ship between secondary metabolism and fungal development. Microbiol. Mol. Biol. Rev. 66:447-459.
7. Cappellini, R. A., and Peterson, J. L. 1965. Macroconidium formation in submerged cultures by a non-sporulating strain of Gibberella zeae. Mycologia 57:962-966.
8. Catlett, N. L., Lee, B. N., Yoder, O. C., and Turgeon, B. G. 2003. Splitmarker recombination for efficient targeted deletion of fungal genes. Fungal Genet. Newsl. 50:9-11.
9. Clutterbuck, A. J. 1969. A mutational analysis of conidial development in Aspergillus nidulans. Genetics 63:317-327.
10. Correll, J. C., Klittich, C. J. R., and Leslie, J. F. 1987. Nitrate non-utilizing mutants of Fusarium oxysporum and their use in vegetative compatibility tests. Phytopathology 77:1640-1646.
11. Cuomo, C. A., Gueldener, 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., Munsterkotter, M., Nelson, D., O'Donnell, K., Ouellet, T., Qi, W. H., Quesneville, H., Roncero, M. I. G., Seong, K. Y., Tetko, I. V., Urban, M., Waalwijk, C., Ward, T. J., Yao, J. Q., 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.
12. Dahlberg, K. R., and Vanetten, J. L. 1982. Physiology and biochemistry of fungal sporulation. Annu. Rev. Phytopathol. 20:281-301.
13. Doedt, T., Krishnamurthy, S., Bockmuhl, D. P., Tebarth, B., Stempel, C., Russell, C. L., Brown, A. J. P., and Ernst, J. F. 2004. APSES proteins regulate morphogenesis and metabolism in Candida albicans. Mol. Biol. Cell 15:3167-3180.
14. Dong, Y. H., Steffenson, B. J., and Mirocha, C. J. 2006. Analysis of ergosterol in single kernel and ground grain by gas chromatography-mass spectrometry. J. Agric. Food Chem. 54:4121-4125.
15. Dutton, J. R., Johns, S., and Miller, B. L. 1997. StuAp is a sequence-specific transcription factor that regulates developmental complexity in Aspergillus nidulans. EMBO (Eur. Mol. Biol. Organ.) J. 16:5710-5721.
16. Frandsen, R. J. N., Nielsen, N. J., Maolanon, N., Sorensen, J. C., Olsson, S., Nielsen, J., and Giese, H. 2006. The biosynthetic pathway for aurofusarin in Fusarium graminearum reveals a close link between the naphthoquinones and naphthopyrones. Mol. Microbiol. 61:1069-1080.
17. Fuchs, U., Czymmek, K. J., and Sweigard, J. A. 2004. Five hydrophobin genes in Fusarium verticillioides include two required for microconidial chain formation. Fungal Genet. Biol. 41:852-864.
18. Gimeno, C. J., and Fink, G. R. 1994. Induction of pseudohyphal growth by overexpression of Phd1, a Saccharomyces cerevisiae gene related to transcriptional regulators of fungal development. Mol. Cell. Biol. 14:2100-2112.
19. Goswami, R. S., and Kistler, H. C. 2004. Heading for disaster: Fusarium graminearum on cereal crops. Mol. Plant Pathol. 5:515-525.
20. Goswami, R. S., and Kistler, H. C. 2005. Pathogenicity and in planta mycotoxin accumulation among members of the Fusarium graminearum species complex on wheat and rice. Phytopathology 95:1397-1404.
21. Goswami, R. S., Xu, J. R., Trail, F., Hilburn, K., and Kistler, H. C. 2006. Genomic analysis of host-pathogen interaction between Fusarium graminearum and wheat during early stages of disease development. Microbiology 152:1877-1890.
22. Gravelat, F. N., Doedt, T., Chiang, L. Y., Liu, H., Filler, S. G., Patterson, T. F., and Sheppard, D. C. 2008. In vivo analysis of Aspergillus fumigatus developmental gene expression determined by real-time reverse transcription- PCR. Infect. Immun. 76:3632-3639.
23. Guldener, U., Mannhaupt, G., Munsterkotter, M., Haase, D., Oesterheld, M., Stumpflen, V., Mewes, H. W., and Adam, G. 2006a. FGDB: A comprehensive fungal genome resource on the plant pathogen Fusarium graminearum. Nucleic Acids Res. 34:456-458.
24. Guldener, U., Seong, K. Y., Boddu, J., Cho, S., Trail, F., Xu, J. R., Adam, G., Mewes, H. W., Muehlbauer, G. J., and Kistler, H. C. 2006b. Development of a Fusarium graminearum Affymetrix GeneChip for profiling fungal gene expression in vitro and in planta. Fungal Genet. Biol. 43:316-325.
25. Hou, Z. M., Xue, C. Y., Peng, Y. L., 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.
26. Iyer, L. M., Koonin, E. V., and Aravind, L. 2002. Extensive domain shuffling in transcription regulators of DNA viruses and implications for the origin of fungal APSES transcription factors. Genome Biol. 3(3).
27. Jansen, C., von Wettstein, D., Schafer, W., Kogel, K. H., Felk, A., and Maier, F. J. 2005. Infection patterns in barley and wheat spikes inoculated with wild-type and trichodiene synthase gene disrupted Fusarium graminearum. Proc. Natl. Acad. Sci. U.S.A. 102:16892-16897.
28. Koch, C., Moll, T., Neuberg, M., Ahorn, H., and Nasmyth, K. 1993. A role for the transcription factors Mbp1 and Swi4 in progression from G1 to S phase. Science 261:1551-1557.
29. Korting, H. C., Hube, B., Oberbauer, S., Januschke, E., Hamm, G., Albrecht, A., Borelli, C., and Schaller, M. 2003. Reduced expression of the hyphal-independent Candida albicans proteinase genes SAP1 and SAP3 in the efg1 mutant is associated with attenuated virulence during infection of oral epithelium. J. Med. Microbiol. 52:623-632.
30. Lee, T. I., Rinaldi, N. J., Robert, F., Odom, D. T., Bar-Joseph, Z., Gerber, G. K., Hannett, N. M., Harbison, C. T., Thompson, C. M., Simon, I., Zeitlinger, J., Jennings, E. G., Murray, H. L., Gordon, D. B., Ren, B., Wyrick, J. J., Tagne, J. B., Volkert, T. L., Fraenkel, E., Gifford, D. K., and Young, R. A. 2002. Transcriptional regulatory networks in Saccharomyces cerevisiae. Science 298:799-804.
31. Lengeler, K. B., Davidson, R. C., D'Souza, C., Harashima, T., Shen, W. C., Wang, P., Pan, X. W., Waugh, M., and Heitman, J. 2000. Signal transduction cascades regulating fungal development and virulence. Microbiol. Mol. Biol. Rev. 64:746-785.
32. Lo, H. J., Kohler, J. R., DiDomenico, B., Loebenberg, D., Cacciapuoti, A., and Fink, G. R. 1997. Nonfilamentous C. albicans mutants are avirulent. Cell 90:939-949.
33. Malz, S., Grell, M. N., Thrane, C., Maier, F. J., Rosager, P., Felk, A., Albertsen, K. S., Salomon, S., Bohn, L., Schäfer, W., and Giese, H. 2005. Identification of a gene cluster responsible for the biosynthesis of aurofusarin in the Fusarium graminearum species complex. Fungal Genet. Biol. 42:420-433.
34. McMullen, M., Jones, R., and Gallenberg, D. 1997. Scab of wheat and barley: A re-emerging disease of devastating impact. Plant Dis. 81:1340-1348.
35. Miller, J. D., and MacKenzie, S. 2000. Secondary metabolites of Fusarium venenatum strains with deletions in the Tri5 gene encoding trichodiene synthetase. Mycologia 92:764-771.
36. Miller, K. Y., Wu, J. G., and Miller, B. L. 1992. Stua is required for cell pattern formation in Aspergillus. Genes Dev. 6:1770-1782.
37. Mirocha, C. J., Kolaczkowski, E., Xie, W. P., Yu, H., and Jelen, H. 1998. Analysis of deoxynivalenol and its derivatives (batch and single kernel) using gas chromatography mass spectrometry. J. Agric. Food Chem. 46:1414-1418.
38. Noble, R. W., and Gibson, Q. H. 1970. The reaction of ferrous horseradish peroxidase with hydrogen peroxide. J. Biol. Chem. 245:2409-2413.
39. Ohara, T., and Tsuge, T. 2004. FoSTUA, encoding a basic helix-loop-helix protein, differentially regulates development of three kinds of asexual spores, macroconidia, microconidia, and chlamydospores, in the fungal plant pathogen Fusarium oxysporum. Eukaryot. Cell 3:1412-1422.
40. Olivain, C., and Alabouvette, C. 1999. Process of tomato root colonization by a pathogenic strain of Fusarium oxysporum f. sp. lycopersici in comparison with a non-pathogenic strain. New Phytol. 141:497-510.
41. Pasquali, M., and Kistler, H. C. 2006. Gibberella zeae ascospore production and collection for microarray experiments. J. Vis. Exp. Published online. doi: 10.3791/115.
42. Pasquali, M., Marena, L., Fiora, E., Piatti, P., Gullino, M. L., and Garibaldi, A. 2004. Real-time polymerase chain reaction for identification of a highly pathogenic group of Fusarium oxysporum f. sp. chrysanthemi on argyranthemum frutescens L. J. Plant Pathol. 86:53-59.
43. Pontecorvo, G., Roper, A. B., Hemmons, L. M., MacDonald, K. D., and Bufton, A. W. 1953. The genetics of Aspergillus nidulans. Adv. Genet. 5:141-238.
44. Ramirez-Zavala, B., and Dominguez, A. 2008. Evolution and phylogenetic relationships of APSES proteins from Hemiascomycetes. FEMS (Fed. Eur. Microbiol. Soc.) Yeast Res. 8:511-519.
45. Ruepp, A., Zollner, A., Maier, D., Albermann, K., Hani, J., Mokrejs, M., Tetko, I., Guldener, U., Mannhaupt, G., Munsterkotter, M., and Mewes, H. W. 2004. The FunCat, a functional annotation scheme for systematic classification of proteins from whole genomes. Nucleic Acids Res. 32:5539-5545.
46. Scherer, M., Wei, H. J., Liese, R., and Fischer, R. 2002. Aspergillus nidulans catalase-peroxidase gene (cpeA) is transcriptionally induced during sexual development through the transcription factor StuA. Eukaryot. Cell 1:725-735.
47. Schmit, J. C., and Brody, S. 1976. Biochemical genetics of Neurospora crassa conidial germination. Bacteriol. Rev. 40:1-41.
48. Seong, K. Y., Zhao, X., Xu, J. R., Guldener, U., and Kistler, H. C. 2008. Conidial germination in the filamentous fungus Fusarium graminearum. Fungal Genet. Biol. 45:389-399.
49. Sheppard, D. C., Doedt, T., Chiang, L. Y., Kim, H. S., Chen, D., Nierman, W. C., and Filler, S. G. 2005. The Aspergillus fumigatus StuA protein governs the up-regulation of a discrete transcriptional program during the acquisition of developmental competence. Mol. Biol. Cell 16:5866-5879.
50. Sohn, K., Urban, C., Brunner, H., and Rupp, S. 2003. EFG1 is a major regulator of cell wall dynamics in Candida albicans as revealed by DNA microarrays. Mol. Microbiol. 47:89-102.
51. Staib, P., Kretschmar, M., Nichterlein, T., Hof, H., and Morschhauser, J. 2002. Transcriptional regulators Cph1p and Efg1p mediate activation of the Candida albicans virulence gene SAP5 during infection. Infect. Immun. 70:921-927.
52. Stoldt, V. R., Sonneborn, A., Leuker, C. E., and Ernst, J. F. 1997. Efg1p, an essential regulator of morphogenesis of the human pathogen Candida albicans, is a member of a conserved class of bHLH proteins regulating morphogenetic processes in fungi. EMBO (Eur. Mol. Biol. Organ.) J. 16:1982-1991.
53. Talbot, N. J., Kershaw, M. J., Wakley, G. E., de Vries, O. M. H., Wessels, J. G. H., and Hamer, J. E. 1996. MPG1 encodes a fungal hydrophobin involved in surface interactions during infection-related development of Magnaporthe grisea. Plant Cell 8:985-999.
54. Tendulkar, S. R., Gupta, A., and Chattoo, B. B. 2003. A simple protocol for isolation of fungal DNA. Biotechnol. Lett. 25:1941-1944.
55. Tong, X. Z., Zhang, X. W., Plummer, K. M., Stowell, K. M., Sullivan, P. A., and Farley, P. C. 2007. GcSTUA, an APSES transcription factor, is required for generation of appressorial turgor pressure and full pathogenicity of Glomerella cingulata. Mol. Plant-Microbe Interact. 20:1102-1111.
56. Twumasi-Boateng, K., Yu, Y., Chen, D., Gravelat, F. N., Nierman, W. C., and Sheppard, D. C. 2009. Transcriptional profiling identifies a role for BrlA in the response to nitrogen depletion and for StuA in the regulation of secondary metabolite clusters in Aspergillus fumigatus. Eukaryot. Cell 8:104-115.
57. van Helden, J. 2003. Regulatory sequence analysis tools. Nucleic Acids Res. 31:3593-3596.
58. Verma, R., Smiley, J., Andrews, B., and Campbell, J. L. 1992. Regulation of the yeast DNA replication genes through the MluI cell cycle box is dependent on Swi6. Proc. Natl. Acad. Sci. U.S.A. 89:9479-9483.
59. Ward, M. P., Gimeno, C. J., Fink, G. R., and Garrett, S. 1995. Sok2 may regulate cyclic Amp-dependent protein kinase-stimulated growth and pseudohyphal development by repressing transcription. Mol. Cell. Biol. 15:6854-6863.
60. Wise, R., Caldo, R., Hong, L., Wu, S., Cannon, E., and Dickerson, J. 2006. PLEXdb: A unified expression profiling database for plants and plant pathogens. (Abstr.) Phytopathology 96:S161.