Signaling Governed by G Proteins and cAMP Is Crucial for Growth, Secondary Metabolism and Sexual Development in Fusarium fujikuroi

PLoS ONE

Volumn 8, Issue 2, 2013, Pages

  Studt, Lena ^a   Humpf, Hans Ulrich ^a   Tudzynski, Bettina ^a  

^a UNIVERSITY OF MÜNSTER   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ADENYLATE CYCLASE; BIKAVERIN; CYCLIC AMP; CYCLIC AMP DEPENDENT PROTEIN KINASE; FUSARUBIN; GIBBERELLIC ACID; GUANINE NUCLEOTIDE BINDING PROTEIN; GUANINE NUCLEOTIDE BINDING PROTEIN ALPHA SUBUNIT 1; GUANINE NUCLEOTIDE BINDING PROTEIN ALPHA SUBUNIT 3; PIGMENT; POLYKETIDE; UNCLASSIFIED DRUG;

ARTICLE; BIOSYNTHESIS; CONTROLLED STUDY; FUNGAL METABOLISM; FUNGUS GROWTH; FUSARIUM; FUSARIUM FUJIKUROI; NONHUMAN; NUCLEOTIDE SEQUENCE; SEXUAL DEVELOPMENT; SIGNAL TRANSDUCTION;

CYCLIC AMP; CYCLIC AMP-DEPENDENT PROTEIN KINASES; FUSARIUM; GTP-BINDING PROTEIN ALPHA SUBUNITS; PIGMENTS, BIOLOGICAL; POLYKETIDES; SEXUAL DEVELOPMENT; SIGNAL TRANSDUCTION;

EID: 84874580221     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0058185     Document Type: Article

References (87)

1. Kurosawa E, (1926) Experimental studies on the nature of the substance excreted by the "bakanae" fungus. Trans Nat Hist Soc Formosa 16: 213-227.
2. Ito S, Kimura J, (1931) Studies on the 'bakanae' disease of rice plant. Rep Hokkaido Nat Agric Exp Stn 27: 1-99.
3. Yabuta T, Hayashi T, (1939) Biochemical studies on the bakanae fungus of rice. II. Isolation of "Gibberellin", the active principle which makes the rice seedlings grow slenderly. J Agric Chem Soc Japan 15: 257-266.
4. Sun S, Snyder WC (1981) The bakanae disease of the rice plant, p. 104-113. In Fusarium: Diseases, Biology and Taxonomy, P. E. Nelson, T. A. Toussoun, and R. J., Cook (ed.), The Pennsylvania State University Press, University Park.
5. Barrero AF, Sánchez JF, Oltra JE, Tamayo N, Cerdá-Olmedo E, et al. (1991) Fusarin C and 8Z-Fusarin C from Gibberella fujikuroi. Phytochemistry 30: 2259-2263.
6. Bacon CW, Porter JK, Norred WP, Leslie JF, (1996) Production of fusaric acid by Fusarium species. Appl Environ Microbiol 62: 4039-4043.
7. Proctor RH, Plattner RD, Brown DW, Seo JA, Lee YW, (2004) Discontinuous distribution of fumonisin biosynthetic genes in the Gibberella fujikuroi species complex. Mycol Res 108: 815-822.
8. Kjær D, Kjær A, Pederson C, Bu'Lock JD, Smith JR, (1971) Bikaverin and norbikaverin, benzoxanthentrione pigments of Gibberella fujikuroi. J Chem Soc 1971: 2792-2797.
9. Brock NL, Tudzynski B, Dischat JS, (2011) Biosynthesis of sesqui- and diterpenes by the gibberellins producer Fusarium fujikuroi. ChemBioChem 12: 2667-2676.
10. Bohm A, Gaudet R, Sigler PB, (1997) Structural aspects of heterotrimeric G-protein Signaling. Curr Opin Biotechnol 8: 480-487.
11. Li L, Wright SJ, Krystofova S, Park G, Borkovich KA, (2007) Heterotrimeric G Protein Signaling in Filamentous Fungi. Annu Rev Microbiol 61: 423-452.
12. Bölker M, (1998) Sex and Crime: Heterotrimeric G proteins in fungal mating and pathogenesis. Fungal Genet Biol 25: 143-156.
13. Lengeler KB, Davidson RC, D'Souza C, Harashima T, Shen WC, et al. (2000) Signal transduction cascades regulating fungal development and virulence. Microbiol Mol Biol Rev 64: 746-785.
14. Hicks JK, Yu JH, Keller NP, (1997) Aspergillus sporulation and mycotoxin production both require inactivation of the FadA Gα protein-dependent signaling pathway. EMBO J 16: 4916-4923.
15. Yu JH, Keller NP, (2005) Regulation of secondary metabolism in filamentous fungi. Annu Rev Phytopathol 43: 437-458.
16. Tag A, Hicks J, Garifullina G, Ake Jr C, Philipps TD, et al. (2000) G-protein signaling mediates differential production of toxic secondary metabolites. Mol Microbiol 38: 658-665.
17. Schulze-Gronover C, Kasulke D, Tudzynski P, Tudzynski B, (2001) The Role of G Protein Aplha Subunits in the Infection Process of the Gray Mold Fungus Botrytis cinerea. MPMI 14: 1293-1302.
18. Gao S, Nuss DL, (1996) Distinct roles for two G protein α subunits in fungal virulence, morphology, and reproduction revealed by targeted gene disruption. Proc Natl Acad Sci USA. 93: 14122-14127.
19. Yu HY, Seo JA, Kim JE, Han KH, Shim WB, et al. (2008) Functional analyses of heterotrimeric G protein Ga and Gb subunits in Gibberella zeae. Microbiology 154: 392-401.
20. Yang Q, Borkovich KA, (1999) Mutational activation of a Gαi causes uncontrolled proliferation of aerial hyphae and increased sensitivity to heat and oxidative stress in Neurospora crassa. Genetics 151: 107-117.
21. García-Rico R, Fierro F, Mauriz E, Gómez A, Fernandéz-Bodega MA, et al. (2008) Heterotrimeric Ga protein Pga1 regulates biosynthesis of penicillin, chrysogenin and roquefortine in Penicillium chrysogenum. Microbiology 154: 3567-3578.
22. Zuber S, Hynes MJ, Andrianopoulos A, (2002) G-protein signaling mediates asexual development at 25 degrees C but has no effect on yeast-like growth at 37 degrees C in the dimorphic fungus Penicillium marneffei. Eukaryot Cell 1: 440-447.
23. Reithner B, Brunner K, Schuhmacher R, Peissl I, Seidl V, et al. (2005) The G protein alpha subunit Tga1 of Trichoderma atroviride is involved in chitinase formation and differential production of antifungal metabolites. Fungal Genet Biol 42: 749-760.
24. Chang MH, Chae KS, Han DM, Jahng KY, (2004) The GanB Gα-Protein negatively regulates asexual sporulation and plays a positive rolte in conidial germination in Aspergillus nidulans. Genetics 167: 1305-1315.
25. Lafon A, Seo JA, Han KH, Yu JH, d'Enfert C, (2005) The heterotrimeric G-protein GanB(alpha)-SfaD(beta)-GpgA(gamma) is a carbon source sensor involved in early cAMP-dependent germination in Aspergillus nidulans. Genetics. 171: 71-80.
26. Doehlemann G, Berndt P, Hahn M, (2006) Different signalling pathways involving a G protein, cAMP and a MAP kinase control germination of Botrytis cinerea conidia. Mol Microbiol 59: 821-836.
27. Liu S, Dean RA, (1997) G Protein α Subunit genes control growth, development and pathogenicity of Magnaporthe grisea. MPMI 9: 1075-1086.
28. Studt L, Wiemann P, Kleigrewe K, Humpf HU, Tudzynski B, (2012) Biosynthesis of fusarubins accounts for pigmentation of perithecia in Fusarium fujikuroi. Appl Environ Microbiol 78: 4468-4480.
29. Darken MA, Jensen AAL, Shu P, (1959) Production of gibberellic acid by fermentation. Appl Microbiol 7: 301-303.
30. Geissman TA, Verbiscar AJ, Phinney BO, Cragg G, (1966) Studies on the biosynthesis of gibberellins from (-)-kaurenoic acid in cultures of Gibberella fujikuroi. Phytochemistry 5: 933-947.
31. Pontecorvo GV, Roper JA, Hemmons LM, MacDonald KD, Bufton AWJ, (1953) The genetics of Aspergillus nidulans. Adv Genet 5: 141-238.
32. Schumacher J, Kokkelink L, Huesmann C, Jimenez-Teja D, Collado I, et al. (2008) The cAMP-dependent signalling pathway and its role in conidial germination, growth and virulence of the grey mould fungus Botrytis cinerea. MPMI 21: 1443-1459.
33. Klittich CJR, Leslie JF, (1988) Nitrate reduction mutants of Fusarium moniliforme (Gibberella fujikuroi). Genetics 118: 417-413.
34. Malonek S, Roja MC, Hedden P, Gaskin P, Hopkins P, et al. (2004) The NADPH-cytochrome P450 Reductase Gene from Gibberella fujikuroi is essential for Gibberellin Biosynthesis. J Biol Chem 279: 25075-25084.
35. Colot HV, Park G, Truner GE, Ringelberg C, Crew CM, et al. (2006) A high-throughput gene knockout procedure for Neurospora reveals functions for multiple transcription factors. Proc Natl Acad Sci USA 103: 10352-10357.
36. Gritz L, Davies LJ, (1983) Plasmid-encoded hygromycin B resistance: the sequence of hygromycin B phosphotransferase gene and its expression in Escherichia coli and Saccharomyces cerevisiae. Gene 25: 179-188.
37. Schumacher J, (2012) Tools for Botrytis cinerea: New expression vectors make the gray mold fungus more accessible to cell biology approaches, Fungal Genet Biol. 49: 483-497.
38. Cenis JL, (1992) Rapid extraction of fungal DNA for PCR amplification. Nucleic Acids Res 20: 2380.
39. Sambrook J, Fritsch EF, Maniatis T (1989) Molecular Cloning: A Laboratory Manual. Cold Spring Harbor Laboratory Press, 2nd ed. Cold Spring Harbor, NY.
40. Church GM, Gilbert W, (1984) Genomic sequencing. Proc Natl Acad Sci USA 81: 1991-1995.
41. Dereeper A, Guignon V, Blanc G, Audic S, Buffet S, et al. (2008) Phylogeny.fr: robust phylogenetic analysis for the non-specialist. Nucleic Acids Res 36: 465-469.
42. Tudzynski B, Mende K, Weltring KM, Kinghorn JR, Unkles SE, (1996) The Gibberella fujikuroi niaD gene encoding nitrate reductase: isolation, sequence, homologous transformation and electrophoretic karyotype location. Microbiology 142: 533-539.
43. Tudzynski B, Homann V, Feng B, Marzluf GA, (1999) Isolation, characterization and disruption of the areA nitrogen regulatory gene of Gibberella fujikuroi. Mol Gen Genet 261: 106-114.
44. Wiemann P, Albermann S, Niehaus E-M, Studt L, von Bargen KW, et al. (2012) The Sfp-Type 4′-Phosphopantetheinyl Transferase Ppt1 of Fusarium fujikuroi Controls Development, Secondary Metabolism and Pathogenicity. PLoS ONE 7(5): e37519.
45. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ, (1990) Basic local alignment search tool. J Mol Biol 215: 403-410.
46. Yu JH, Wieser J, Adams TH, (1996) The Aspergillus FlbA RGS domain protein antagonizes G protein signaling to block proliferation and allow development. EMBO J 19: 5184-5190.
47. Turner GE, Borkovich KA, (1993) Identification of a G protein subunit from Neurospora crassa that is a member of the Gi family. J Biol Chem 268: 14805-14811.
48. Jain S, Akiyama K, Mae K, Ohguchi T, Takata R, (2002) Targeted disruption of a G protein alpha subunit gene results in reduced pathogenicity in Fusarium oxysporum. Curr Genet 41: 407-413.
49. Kays AM, Rowley PS, Baasiri RA, Borkovich KA, (2000) Regulation of conidiation and adenylyl cyclase levels by the G alpha protein GNA-3 in Neurospora crassa. Mol Cell Biol 20: 7693-7705.
50. Jain S, Akiyama K, Takata R, Ohguchi T, (2005) Signalling via the G protein alpha subunit FGA2 is necessary for pathogenesis in Fusarium oxysporum. FEMS Microbiol Lett 243: 165-172.
51. Linnemannstöns P, Schulte J, del Mar Prado M, Proctor RH, Avalos J, et al. (2002) The polyketide synthase gene pks4 from Gibberella fujikuroi encodes a key enzyme in the biosynthesis of the red pigment bikaverin. Fungal Genet Biol 37: 134-148.
52. Wiemann P, Willmann A, Straeten M, Kleigrewe K, Beyer M, et al. (2009) Biosynthesis of the red pigment bikaverin in Fusarium fujikuroi: genes, their function and regulation. Mol Microbiol 72: 931-946.
53. Klimpel A, Schulze-Gronover C, Williamson B, Stewart JA, Tudzynski B, (2002) The adenylate cyclase (BAC) in Botrytis cinerea is required for full pathogenicity. Mol Plant Pathol 3: 439-450.
54. Wiemann P, Brown DW, Kleigrewe K, Bok JW, Keller NP, et al. (2010) FfVel1 and FfLae1, components of a Velvet-like complex in Fusarium fujikuroi, affect differentiation, secondary metabolism and virulence. Mol Microbiol 77: 972-994.
55. Horwitz BA, Sharon A, Lu SW, Ritter V, Sandrock TM, et al. (1999) A G protein alpha subunit from Cochliobolus heterostrophus involved in mating and appressorium formation. Fungal Genet Biol 26: 19-32.
56. Degani O, Maor R, Hadar R, Sharon A, Horwitz BA, (2004) Host physiology and pathogenic variation of Cochliobolus heterostrophus strains with mutations in the G protein alpha subunit, CGA1. Appl Environ Microbiol 70: 5005-5009.
57. Ivey FD, Hodge PN, Turner GE, Borkovich KA, (1996) The Gαi homologue gna-1 controls multiple differentiation pathways in Neurospora crassa. Mol Biol Cell 7: 1283-1297.
58. Liebmann B, Gattung S, Jahn B, Brakhage AA, (2003) cAMP signaling in Aspergillus fumigatus is involved in the regulation of the virulence gene pksP and in defense against killing by macrophages. Mol Genet Genomics 269: 420-435.
59. Zuber S, Hynes MJ, Andrianopoulos A, (2003) The G-protein alpha-subunit GasC plays a major role in germination in the dimorphic fungus Penicillium marneffei. Genetics 164: 487-499.
60. Shimizu K, Keller NP, (2001) Genetic involvement of a cAMP-dependent protein kinase in a G protein signaling pathway regulating morphological and chemical transitions in Aspergillus nidulans. Genetics 157: 591-600.
61. Shimizu K, Hicks JK, Huang TP, Keller NP, (2003) Pka, Ras and RGS protein interactions regulate activity of AflR, a Zn(II)2Cys6 transcription factor in Aspergillus nidulans. Genetics 165: 1095-1104.
62. Mukherjee M, Mukherjee PK, Kale SP, (2007) cAMP signalling is involved in growth, germination, mycoparasitism and secondary metabolism in Trichoderma virens. Microbiology 153: 1734-1742.
63. Choi YE, Brown JA, Williams CB, Canales LL, Shim WB, (2008) GAC1, a gene encoding a putative GTPase-activating protein regulates bikaverin biosynthesis in Fusarium verticillioides. Mycologia 100: 701-709.
64. Choi YE, Xu JR, (2010) The cAMP Signaling Pathway in Fusarium verticillioides is important for conidiation, plant infection, and stress response but not fumonisin production. MPMI 23 4: 522-533.
65. Kohut G, Oláh B, Ádám AL, García-Martínez J, Hornok L, (2010) Adenylyl cyclase regulates heavy metal sensitivity, bikaverin production and plant tissue colonization in Fusarium proliferatum. J Basic Microbiol 50: 59-71.
66. Garcia-Martinez J, Ádám AL, Avalos J, (2012) Adenylyl cyclase plays a regulatory role in development, stress resistence and secondary metabolism in Fusarium fujikuroi. PLoS One 7(1): e28849.
67. Studt L, Troncoso C, Gong F, Hedden P, Toomajian C, et al. (2012) Seqgregation of secondary metabolite biosynthesis in hybrids of Fusarium fujikuroi and Fusarium proliferatum. Fung Gen Biol 49: 567-577.
68. Brown DW, Butchko RAE, Busman M, Proctor RH, (2012) Identification of the gene clusters associated with fusaric acid, fusarin and perithecial pigment production in Fusarium verticillioides. Fungal Genet Biol 49: 521-532.
69. Choi W, Dean RA, (1997) The adenylate cyclase gene MAC1 of Magnaporthe grisea controls appressorium formation and other aspects of growth and development. Plant Cell 9: 1973-1983.
70. Xu JR, Urban M, Sweigard JA, Hamer JE, (1997) The cPKA gene of Magnaporthe grisea is essential for appressorial penetration. Mol Plant-Microbe Interact 10: 187-194.
71. Chen C, Dickman MB, (2005) cAMP blocks MAPK activation and sclerotial development via Rap-1 in a PKA-independent manner in Sclerotinia sclerotiorum. Mol Microbiol 55: 299-311.
72. Santangelo GM, (2006) Glucose signaling in Saccharomyces cerevisiae. Microbiol Mol Biol Rev 70: 253-282.
73. Klengel T, Liang WJ, Chaloupka J, Ruoff C, Schröppel K, et al. (2005) Fungal Adenylyl Cyclase Integrates CO2 Sensing with cAMP Signaling and Virulence. Current Biol 15: 2021-2026.
74. Mogensen EG, Janbon G, Chaloupka J, Steegborn C, Fu AS, et al. (2006) Cryptococcus neoformans Senses CO2 through the Carbonic Anhydrase Can2 and the Adenylyl Cyclase Cac1. Eukaryot Cell 5: 103-111.
75. Bahn YS, Mühlschlegel FA, (2006) CO2 sensing in fungi and beyond. Curr Opin Microbiol 9: 572-578.
76. Fuller KK, Richie DL, Fen X, Krishan K, Stephens TJ, et al. (2011) Divergent Protein Kinase A isoforms co-ordinately regulate conidial germination, carbohydrate metabolism and virulence in Aspergillus fumigatus. Mol Microbiol 79: 1045-1062.
77. Ni M, Rierson S, Seo JA, Yu JH, (2005) The pkaB gene encoding the secondary protein kinase A catalytic subunit has a synthetic lethal interaction with PkaA and plays overlapping and opposite roles in Aspergillus nidulans. Eukaryot Cell 4: 1465-1476.
78. Fillinger S, Chaveroche MK, Shimizu K, Keller N, d'Enfert C, (2002) cAMP and ras signalling independently control spore germination in the filamentous fungus Aspergillus nidulans. Mol Microbiol 44: 1001-1016.
79. Liebmann B, Müller M, Braun A, Brakhage AA, (2004) The cyclic AMP-dependent protein kinase a network regulates development and virulence in Aspergillus fumigatus. Infect Immun 72: 5193-5203.
80. Terenzi HF, Flawia MM, Tellez-Inon MT, Torres HN, (1976) Control of Neurospora crassa morphology by cyclic adenosine 3′, 5′-monophosphate and dibutyryl cyclic adenosine 3′, 5′-monophosphate. J Bacteriol 126: 91-99.
81. Rosén S, Yu JH, Adams TH, (1999) The Aspergillus nidulans sfaD gene encodes a G protein beta subunit that is required for normal growth and repression of sporulation. EMBO J 18: 5592-5600.
82. Seo JA, Han KH, Yu JH, (2005) Multiple roles of a heterotrimeric G-protein gamma-subunit in governing growth and development of Aspergillus nidulans. Genetics 171: 81-89.
83. Zeilinger S, Reithner B, Scala V, Peissl I, Lorito M, et al. (2005) Signal transduction by Tga3, a novel G protein alpha subunit of Trichoderma atroviride. Appl Environ Microbiol 71: 1591-1597.
84. Debuchy R, Turgeon BG (2006) Mating-type structure, evolution, and function in Euascomycetes. The Mycota (Kues U & Fischer R, eds), 293-323. Springer, Berlin.
85. Lee J, Park C, Kim JC, Kim JE, Lee YW, (2010) Identification and functional characterization of genes involved in the sexual reproduction of the ascomycete fungus Gibberella zeae. Biochem Biophys Res Commun 401: 48-52.
86. Nakafuku M, Itoh H, Nakamura S, Kaziro Y, (1987) Occurence in Saccharomyces cerevisiae of a gene homologous tot he cDNA coding fort he a subunit of mammalian G proteins. Proc Natl Acad Sci USA 84: 2140-2144.
87. Regenfelder E, Spellig T, Hartmann A, Lauenstein S, Bölker M, et al. (1997) G proteins in Ustilago maydis: transmission of multiple signals? EMBO J 16: 1934-1942.