The Wor1-like protein Fgp1 regulates pathogenicity, toxin synthesis and reproduction in the phytopathogenic fungus Fusarium graminearum

PLoS Pathogens

Volumn 8, Issue 5, 2012, Pages

  Jonkers, Wilfried ^a,b   Dong, Yanhong ^a   Broz, Karen ^b   Kistler, H Corby ^a,b  

^a UNIVERSITY OF MINNESOTA   (United States)

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

Author keywords

[No Author keywords available]

Indexed keywords

FUNGAL PROTEIN; MYCOTOXIN; PROTEIN FGP1; TRICHOTHECENE; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ARTICLE; BIOSYNTHESIS; CARBOXY TERMINAL SEQUENCE; CONIDIUM; CONTROLLED STUDY; FUNGAL REPRODUCTION; FUNGAL STRAIN; FUSARIUM GRAMINEARUM; FUSARIUM OXYSPORUM; GENE DELETION; GENE EXPRESSION; GENETIC CONSERVATION; IN VITRO STUDY; NONHUMAN; PATHOGENESIS; PATHOGENICITY; REPRODUCTION; TOXIN SYNTHESIS; WHEAT; AMINO ACID SEQUENCE; FOOD CONTAMINATION; FUNGAL GENE; FUNGUS SPORE; FUSARIOSIS; FUSARIUM; GENE EXPRESSION REGULATION; GENE SILENCING; GENETICS; HOST PATHOGEN INTERACTION; IMMUNOLOGY; METABOLISM; MICROBIOLOGY; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PHYSIOLOGY; SEQUENCE ANALYSIS; SPECIES DIFFERENCE;

CANDIDA ALBICANS; FUNGI; FUSARIUM; FUSARIUM OXYSPORUM; GIBBERELLA ZEAE; TRITICUM AESTIVUM;

AMINO ACID SEQUENCE; CONSERVED SEQUENCE; FOOD CONTAMINATION; FUNGAL PROTEINS; FUSARIOSIS; FUSARIUM; GENE EXPRESSION REGULATION, FUNGAL; GENE SILENCING; GENES, FUNGAL; HOST-PATHOGEN INTERACTIONS; MOLECULAR SEQUENCE DATA; MYCOTOXINS; REPRODUCTION; SEQUENCE ANALYSIS, PROTEIN; SPECIES SPECIFICITY; SPORES, FUNGAL; TRITICUM;

EID: 84863687977     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1002724     Document Type: Article

References (63)

1. Goswami RS, Kistler HC, (2004) Heading for disaster: Fusarium graminearum on cereal crops. Mol Plant Pathol 5: 515-525.
2. Trail F, (2009) For blighted waves of grain: Fusarium graminearum in the postgenomics era. Plant Physiol 149: 103-110.
3. Ilgen P, Hadeler B, Maier FJ, Schafer W, (2009) Developing kernel and rachis node induce the trichothecene pathway of Fusarium graminearum during wheat head infection. Mol Plant Microbe Interact 22: 899-908.
4. Jansen C, von Wettstein D, Schafer W, Kogel KH, Felk A, et al. (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.
5. Kimura M, Tokai T, Takahashi-Ando N, Ohsato S, Fujimura M, (2007) Molecular and genetic studies of fusarium trichothecene biosynthesis: pathways, genes, and evolution. Biosci Biotechnol Biochem 71: 2105-2123.
6. Merhej J, Richard-Forget F, Barreau C, (2011) Regulation of trichothecene biosynthesis in Fusarium: recent advances and new insights. Appl Microbiol Biotechnol 91: 519-528.
7. Michielse CB, Rep M, (2009) Pathogen profile update: Fusarium oxysporum. Mol Plant Pathol 10: 311-324.
8. Takken F, Rep M, (2010) The arms race between tomato and Fusarium oxysporum. Mol Plant Pathol 11: 309-314.
9. Michielse CB, van Wijk R, Reijnen L, Manders EM, Boas S, et al. (2009) The nuclear protein Sge1 of Fusarium oxysporum is required for parasitic growth. PLoS Pathog 5: e1000637.
10. Michielse CB, Becker M, Heller J, Moraga J, Collado IG, et al. (2011) The Botrytis cinerea Reg1 protein, a putative transcriptional regulator, is required for pathogenicity, conidiogenesis, and the production of secondary metabolites. Mol Plant Microbe Interact 24: 1074-1085.
11. Nguyen VQ, Sil A, (2008) Temperature-induced switch to the pathogenic yeast form of Histoplasma capsulatum requires Ryp1, a conserved transcriptional regulator. Proc Natl Acad Sci U S A 105: 4880-4885.
12. Huang G, Wang H, Chou S, Nie X, Chen J, et al. (2006) Bistable expression of WOR1, a master regulator of white-opaque switching in Candida albicans. Proc Natl Acad Sci U S A 103: 12813-12818.
13. Lohse MB, Johnson AD, (2009) White-opaque switching in Candida albicans. Curr Opin Microbiol 12: 650-654.
14. Holbrook ED, Rappleye CA, (2008) Histoplasma capsulatum pathogenesis: making a lifestyle switch. Curr Opin Microbiol 11: 318-324.
15. Caspari T, (1997) Onset of gluconate-H+ symport in Schizosaccharomyces pombe is regulated by the kinases Wis1 and Pka1, and requires the gti1+ gene product. J Cell Sci 110 (Pt 20): 2599-2608.
16. Kunitomo H, Sugimoto A, Wilkinson CR, Yamamoto M, (1995) Schizosaccharomyces pombe pac2+ controls the onset of sexual development via a pathway independent of the cAMP cascade. Curr Genet 28: 32-38.
17. Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, et al. (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25: 3389-3402.
18. Lohse MB, Zordan RE, Cain CW, Johnson AD, (2010) Distinct class of DNA-binding domains is exemplified by a master regulator of phenotypic switching in Candida albicans. Proc Natl Acad Sci U S A 107: 14105-14110.
19. Huang G, Yi S, Sahni N, Daniels KJ, Srikantha T, et al. (2010) N-acetylglucosamine induces white to opaque switching, a mating prerequisite in Candida albicans. PLoS Pathog 6: e1000806.
20. Michielse CB, van Wijk R, Reijnen L, Cornelissen BJ, Rep M, (2009) Insight into the molecular requirements for pathogenicity of Fusarium oxysporum f. sp. lycopersici through large-scale insertional mutagenesis. Genome Biol 10: R4.
21. Maier FJ, Miedaner T, Hadeler B, Felk A, Salomon S, et al. (2006) Involvement of trichothecenes in fusarioses of wheat, barley and maize evaluated by gene disruption of the trichodiene synthase (Tri5) gene in three field isolates of different chemotype and virulence. Mol Plant Pathol 7: 449-461.
22. Gardiner DM, Kazan K, Manners JM, (2009) Nutrient profiling reveals potent inducers of trichothecene biosynthesis in Fusarium graminearum. Fungal Genet Biol 46: 604-613.
23. Dyer RB, Plattner RD, Kendra DF, Brown DW, (2005) Fusarium graminearum TRI14 is required for high virulence and DON production on wheat but not for DON synthesis in vitro. J Agric Food Chem 53: 9281-9287.
24. Gardiner DM, Kazan K, Manners JM, (2009) Novel genes of Fusarium graminearum that negatively regulate deoxynivalenol production and virulence. Mol Plant Microbe Interact 22: 1588-1600.
25. Seong KY, Pasquali M, Zhou X, Song J, Hilburn K, et al. (2009) Global gene regulation by Fusarium transcription factors Tri6 and Tri10 reveals adaptations for toxin biosynthesis. Mol Microbiol 72: 354-367.
26. Lysoe E, Seong KY, Kistler C, (2011) The transcriptome of Fusarium graminearum during the infection of wheat. Mol Plant Microbe Interact 24: 995-1000.
27. Ma L-J, van der Does HC, Borkovich KA, Coleman JJ, Daboussi M-J, et al. (2010) Comparative genomics reveals mobile pathogenicity chromosomes in Fusarium. Nature 464: 367-373.
28. Harris LJ, Alexander NJ, Saparno A, Blackwell B, McCormick SP, et al. (2007) A novel gene cluster in Fusarium graminearum contains a gene that contributes to butenolide synthesis. Fungal Genet Biol 44: 293-306.
29. Malz S, Grell MN, Thrane C, Maier FJ, Rosager P, et al. (2005) Identification of a gene cluster responsible for the biosynthesis of aurofusarin in the Fusarium graminearum species complex. Fungal Genet Biol 42: 420-433.
30. Gaffoor I, Brown DW, Plattner R, Proctor RH, Qi W, et al. (2005) Functional analysis of the polyketide synthase genes in the filamentous fungus Gibberella zeae (anamorph Fusarium graminearum). Eukaryot Cell 4: 1926-1933.
31. Tobiasen C, Aahman J, Ravnholt KS, Bjerrum MJ, Grell MN, et al. (2007) Nonribosomal peptide synthetase (NPS) genes in Fusarium graminearum, F. culmorum and F. pseudograminearium and identification of NPS2 as the producer of ferricrocin. Curr Genet 51: 43-58.
32. Ohara T, Inoue I, Namiki F, Kunoh H, Tsuge T, (2005) REN1 is required for development of microconidia and macroconidia, but not of chlamydospores, in the plant pathogenic fungus Fusarium oxysporum. Genetics 166: 113-124.
33. Busby TM, Miller KY, Miller BL, (1996) Suppression and enhancement of the Aspergillus nidulans medusa mutation by altered dosage of the bristle and stunted genes. Genetics 143: 155-163.
34. Sewall TC, Mims CW, Timberlake WE, (1990) abaA controls phialide differentiation in Aspergillus nidulans. Plant Cell 2: 731-739.
35. Kwon NJ, Garzia A, Espeso EA, Ugalde U, Yu JH, (2010) FlbC is a putative nuclear C2H2 transcription factor regulating development in Aspergillus nidulans. Mol Microbiol 77: 1203-1219.
36. Jonkers W, van Kan JA, Tijm P, Lee YW, Tudzynski P, et al. (2011) The FRP1 F-box gene has different functions in sexuality, pathogenicity and metabolism in three fungal pathogens. Mol Plant Pathol 12: 548-563.
37. Reyes-Dominguez Y, Boedi S, Sulyok M, Wiesenberger G, Stoppacher N, et al. (2011) Heterochromatin influences the secondary metabolite profile in the plant pathogen Fusarium graminearum. Fungal Genet Biol 49: 39-47.
38. Rittenour WR, Harris SD, (2010) An in vitro method for the analysis of infection-related morphogenesis in Fusarium graminearum. Mol Plant Pathol 11: 361-369.
39. Boddu J, Cho S, Kruger WM, Muehlbauer GJ, (2006) Transcriptome analysis of the barley-Fusarium graminearum interaction. Mol Plant Microbe Interact 19: 407-417.
40. Boenisch MJ, Schaefer W, (2011) Fusarium graminearum forms mycotoxin producing infection structures on wheat. BMC Plant Biol 11: 110.
41. Gravelat FN, Ejzykowicz DE, Chiang LY, Chabot JC, Urb M, et al. (2010) Aspergillus fumigatus MedA governs adherence, host cell interactions and virulence. Cell Microbiol 12: 473-488.
42. Borneman AR, Hynes MJ, Andrianopoulos A, (2000) The abaA homologue of Penicillium marneffei participates in two developmental programmes: conidiation and dimorphic growth. Mol Microbiol 38: 1034-1047.
43. Tao L, Yu JH, (2011) AbaA and WetA govern distinct stages of Aspergillus fumigatus development. Microbiology 157: 313-326.
44. Son H, Seo YS, Min K, Park AR, Lee J, et al. (2011) A Phenome-Based Functional Analysis of Transcription Factors in the Cereal Head Blight Fungus, Fusarium graminearum. PLoS Pathog 7: e1002310.
45. Sylvain MA, Liang XB, Hellauer K, Turcotte B, (2011) Yeast zinc cluster proteins Dal81 and Uga3 cooperate by targeting common coactivators for transcriptional activation of gamma-aminobutyrate responsive genes. Genetics 188: 523-534.
46. van Helden J, (2003) Regulatory sequence analysis tools. Nucleic Acids Res 31: 3593-3596.
47. Di Pietro A, Garcia-Maceira FI, Meglecz E, Roncero MI, (2001) A MAP kinase of the vascular wilt fungus Fusarium oxysporum is essential for root penetration and pathogenesis. Mol Microbiol 39: 1140-1152.
48. Jenczmionka NJ, Maier FJ, Lösch AP, Schäfer W, (2003) Mating, conidiation and pathogenicity of Fusarium graminearum, the main causal agent of the head-blight disease of wheat, are regulated by the MAP kinase gpmk1. Curr Genet 43: 87-95.
49. Kim HS, Park SY, Lee S, Adams EL, Czymmek K, et al. (2011) Loss of cAMP-dependent protein kinase A affects multiple traits important for root pathogenesis by Fusarium oxysporum. Mol Plant Microbe Interact 24: 719-732.
50. Lohse MB, Johnson AD, (2010) Temporal anatomy of an epigenetic switch in cell programming: the white-opaque transition of C. albicans. Mol Microbiol 78: 331-343.
51. Lysoe E, Pasquali M, Breakspear A, Kistler HC, (2011) The transcription factor FgStuAp influences spore development, pathogenicity, and secondary metabolism in Fusarium graminearum. Mol Plant Microbe Interact 24: 54-67.
52. Ohara T, 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.
53. Hood EE, Gelvin SB, Melchers LS, Hoekema A, (1993) New Agrobacterium helper plasmids for gene transfer to plants. Transgen Res 2: 208-218.
54. Goswami RS, Kistler HC, (2005) Pathogenicity and In Planta Mycotoxin Accumulation Among Members of the Fusarium graminearum Species Complex on Wheat and Rice. Phytopathology 95: 1397-1404.
55. Houterman PM, Cornelissen BJC, Rep M, (2008) Suppression of plant resistance gene-based immunity by a fungal effector. PLoS Pathog 4: e1000061.
56. Hou Z, Xue C, Peng Y, Katan T, Kistler HC, et al. (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.
57. Zhang A, Lu P, Dahl-Roshak AM, Paress PS, Kennedy S, et al. (2003) Efficient disruption of a polyketide synthase gene (pks1) required for melanin synthesis through Agrobacterium-mediated transformation of Glarea lozoyensis. Mol Genet Genomics 268: 645-655.
58. Takken FL, Van Wijk R, Michielse CB, Houterman PM, Ram AF, et al. (2004) A one-step method to convert vectors into binary vectors suited for Agrobacterium-mediated transformation. Curr Genet 45: 242-248.
59. Rosewich UL, Pettway RE, Katan T, Kistler HC, (1999) Population Genetic Analysis Corroborates Dispersal of Fusarium oxysporum f. sp. radicis-lycopersici from Florida to Europe. Phytopathology 89: 623-630.
60. Pasquali M, Kistler C, (2006) Gibberella zeae ascospore production and collection for microarray experiments. J Vis Exp pp. 115.
61. Güldener U, Seong K-Y, Boddu J, Cho S, Trail F, et al. (2006) Development of a Fusarium graminearum Affymetrix GeneChip for profiling fungal gene expression in vitro and in planta. Fungal Genet Biol 43: 316-325.
62. Wong P, Walter M, Lee W, Mannhaupt G, Munsterkotter M, et al. (2010) FGDB: revisiting the genome annotation of the plant pathogen Fusarium graminearum. Nucleic Acids Res 39: D637-639.
63. Dash S, Van Hemert J, Hong L, Wise RP, Dickerson JA, (2012) PLEXdb: gene expression resources for plants and plant pathogens. Nucleic Acids Res 40: D1194-1201.