Two separate key enzymes and two pathway-specific transcription factors are involved in fusaric acid biosynthesis in Fusarium fujikuroi

Environmental Microbiology

Volumn 18, Issue 3, 2016, Pages 936-956

  Studt, Lena ^a,d   Janevska, Slavica ^a   Niehaus, Eva Maria ^a   Burkhardt, Immo ^b   Arndt, Birgit ^a   Sieber, Christian M K ^c   Humpf, Hans Ulrich ^a   Dickschat, Jeroen S ^b   Tudzynski, Bettina ^a  

^a UNIVERSITY OF MÜNSTER   (Germany)

^b UNIVERSITY OF BONN   (Germany)

^c DOE JOINT GENOME INSTITUTE   (United States)

^d UNIVERSITY OF NATURAL RESOURCES AND LIFE SCIENCES   (Austria)

Author keywords

[No Author keywords available]

Indexed keywords

FUSARIC ACID; FUSARINOLIC ACID; POLYKETIDE SYNTHASE; TRANSCRIPTION FACTOR;

ANALOGS AND DERIVATIVES; BIOSYNTHESIS; ENZYMOLOGY; FUSARIUM; GENETICS; METABOLISM; MOLECULAR GENETICS; MULTIGENE FAMILY; ORYZA; TRANSPORT AT THE CELLULAR LEVEL;

BIOLOGICAL TRANSPORT; BIOSYNTHETIC PATHWAYS; FUSARIC ACID; FUSARIUM; MOLECULAR SEQUENCE DATA; MULTIGENE FAMILY; ORYZA; POLYKETIDE SYNTHASES; TRANSCRIPTION FACTORS;

EID: 84961136551     PISSN: 14622912     EISSN: 14622920     Source Type: Journal    
DOI: 10.1111/1462-2920.13150     Document Type: Article

References (73)

1. Arndt, B., Studt, L., Wiemann, P., Osmanov, H., Kleigrewe, K., Köhler, J., etal. (2015) Genetic engineering, high resolution mass spectrometry and nuclear magnetic resonance spectroscopy elucidate the bikaverin biosynthetic pathway in Fusarium fujikuroi. Fungal Genet Biol 84: 26-36.
2. Avalos, J., and Estrada, A.F. (2010) Regulation by light in Fusarium. Fungal Genet Biol 47: 930-938.
3. Backes, W.L., and Kelley, R.W. (2003) Organization of multiple cytochrome P450s with NADPH-cytochrome P450 reductase in membranes. Pharmacol Ther 98: 221-233.
4. Bailey, T.L., Williams, N., Misleh, C., and Li, W.W. (2006) MEME: discovering and analyzing DNA and protein sequence motifs. Nucleic Acids Res 34: W369-W373.
5. von Bargen, K.W., Niehaus, E.M., Bergander, K., Brun, R., Tudzynski, B., and Humpf, H.U. (2013) Structure elucidation and antimalarial activity of apicidin F: an apicidin-like compound produced by Fusarium fujikuroi. J Nat Prod 76: 2136-2140.
6. von Bargen, K.W., Niehaus, E.M., Krug, I., Bergander, K., Würthwein, E.U., Tudzynski, B., and Humpf, H.U. (2015) Isolation and structure elucidation of fujikurins A-D: products of the PKS19 gene cluster in Fusarium fujikuroi. J Nat Prod 78: 1809-1815.
7. Bluhm, B.H., Kim, H., Butchko, R.A.E., and Woloshuk, C.P. (2008) Involvement of ZFR1 of Fusarium verticillioides in kernel colonization and the regulation of FST1, a putative sugar transporter gene required for fumonisin biosynthesis on maize kernels. Mol Plant Pathol 9: 203-211.
8. Boonman, N., Prachya, S., Boonmee, A., Kittakoop, P., Wiyakrutta, S., Sriubolmas, N., etal. (2012) In vitro acanthamoebicidal activity of fusaric acid and dehydrofusaric acid from an endophytic fungus Fusarium spTlau3. Planta Med 78: 1562-1567.
9. Bömke, C., and Tudzynski, B. (2009) Diversity, regulation, and evolution of the gibberellin biosynthetic pathway in fungi compared to plants and bacteria. Phytochemistry 70: 1876-1893.
10. Brown, D.W., Lee, S., Kim, L., Ryu, J., Lee, S., Seo, Y., etal. (2015) Identification of a 12-gene fusaric acid biosynthetic gene cluster in Fusarium species through comparative and functional genomics. Mol Plant Microbe Interact 28: 319-332.
11. Bushley, K.E., and Turgeon, B.G. (2010) Phylogenomics reveals subfamilies of fungal nonribosomal peptide synthetases and their evolutionary relationships. BMC Evol Biol 10: 26.
12. Cenis, J.L. (1992) Rapid extraction of fungal DNA for PCR amplification. Nucleic Acids Res 20: 2380.
13. Chen, H., Lee, M.H., Daub, M.E., and Chung, K.R. (2007) Molecular analysis of the cercosporin biosynthetic gene cluster in Cercospora nicotianae. Mol Microbiol 64: 755-770.
14. Chiang, Y.M., Szewczyk, E., Nayak, T., Davidson, A.D., Sanchez, J.F., Lo, H.C., etal. (2008) Molecular genetic mining of the Aspergillus secondary metabolome: discovery of the emericellamide biosynthetic pathway. Chem Biol 15: 527-532.
15. Chooi, Y.H., Cacho, R., and Tang, Y. (2010) Identification of the viridicatumtoxin and griseofulvin gene clusters from Penicillium aethiopicum. Chem Biol 17: 483-494.
16. Christianson, T.W., Sikorski, R.S., Dante, M., Shero, J.H., and Hieter, P. (1992) Multifunctional yeast high-copy-number shuttle vectors. Gene 110: 119-122.
17. Colot, H.V., Park, G., Turner, G.E., Ringelberg, C., Crew, C.M., Litvinkova, L., etal. (2006) A high-throughput gene knockout procedure for Neurospora crassa reveals functions for multiple transcription factors. PNAS 113: 10352-10357.
18. Cramer, R.A., Gamcsik, M.P., Brooking, R.M., Najvar, L.K., Kirkpatrick, W.R., Patterson, T.F., etal. (2006) Disruption of a nonribosomal peptide synthetase in Aspergillus fumigatus eliminates gliotoxin production. Eukaryot Cell 5: 972-980.
19. Crutcher, F.K., Liu, J., Puckhaber, L.S., Stipanovic, R.D., Bell, A.A., and Nichols, R.L. (2015) FUBT, a putative MFS transporter, promotes secretion of fusaric acid in the cotton pathogen Fusarium oxysporum f. sp. vasinfectum. Microbiology 161: 875-883.
20. Darken, M.A., Jensen, A.L., and Shu, P. (1959) Production of gibberellic acid by fermentation. Appl Microbiol 7: 301-303.
21. Dickschat, J.S., Wenzel, S.C., Bode, H.B., Müller, R., and Schulz, S. (2004) Biosynthesis of volatiles by the myxobacterium Myxococcus xanthus. Chembiochem 5: 778-787.
22. Dolan, S.K., Owens, R.A., O'Keeffe, G., Hammel, S., Fitzpatrick, D.A., Jones, G.W., and Doyle, S. (2014) Regulation of nonribosomal peptide synthesis: bis-thiomethylation attenuates gliotoxin biosynthesis in Aspergillus fumigatus. Chem Biol 21: 999-1012.
23. Dregus, M., and Engel, K.H. (2003) Volatile constituents of uncooked rhubarb (Rheum rhabarbarum L.) stalks. J Agric Food Chem 51: 6530-6536.
24. Du, L., and Lou, L. (2010) PKS and NRPS release mechanisms. Nat Prod Rep 27: 255-278.
25. Ehrlich, K.C., and Mack, B.M. (2014) Comparison of expression of secondary metabolite biosynthesis cluster genes in Aspergillus flavus, A.parasiticus, and A.oryzae. Toxins (Basel) 6: 1916-1928.
26. Forseth, R.R., Amaike, S., Schwenk, D., Affeldt, K.J., Hoffmeister, D., Schroeder, F.C., and Keller, N.P. (2013) Homologous NRPS-like gene clusters mediate redundant small-molecule biosynthesis in Aspergillus flavus. Angew Chem Int Ed Engl 52: 1590-1594.
27. Gardiner, D.M., Jarvis, R.S., and Howlett, B.J. (2005) The ABC transporter gene in the sirodesmin biosynthetic gene cluster of Leptosphaeria maculans is not essential for sirodesmin production but facilitates self-protection. Fungal Genet Biol 42: 257-263.
28. Geissman, T.A., Verbiscar, A.J., Phinney, B.O., and Cragg, G. (1966) Studies on the biosynthesis of gibberellins from (-)-kaurenoic acid in cultures of Gibberella fujikuroi. Phytochemistry 5: 933-947.
29. Gritz, L., and Davies, J. (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.
30. Hansen, B.G., Genee, H.J., Kaas, C.S., Nielsen, J.B., Regueira, T.B., Mortensen, U.H., etal. (2011) A new class of IMP dehydrogenase with a role in self-resistance of mycophenolic acid producing fungi. BMC Microbiol 11: 202.
31. Kalb, D., Lackner, G., and Hoffmeister, D. (2014) Functional and phylogenetic divergence of fungal adenylate-forming reductases. Appl Environ Microbiol 80: 6175-6183.
32. Keller, N.P., and Hohn, T. (1997) Metabolic pathway gene clusters in filamentous fungi. Fungal Genet Biol 21: 17-29.
33. Keller, N.P., Turner, G., and Bennett, J.W. (2005) Fungal secondary metabolism - from biochemistry to genomics. Nat Rev Microbiol 3: 937-947.
34. Kimura, M., Shingo, Y., Yoneyama, K., and Yamaguchi, I. (1998) Features of Tri101, the trichothecene 3-O-acetyltransferase gene, related to the self-defense mechanism in Fusarium graminearum. Biosci Biotechnol Biochem 62: 1033-1036.
35. Liu, S., and Liebeskind, L.S. (2008) A simple, modular synthesis of substituted pyridines. J Am Chem Soc 130: 6918-6919.
36. Malonek, S., Rojas, M.C., Hedden, P., Gaskin, P., Hopkins, P., and Tudzynski, B. (2004) The NADPH-cytochrome P450 reductase gene from Gibberella fujikuroi is essential for gibberellin biosynthesis. J Biol Chem 279: 25075-25084.
37. Marrè, M.T., Vergani, P., and Albergoni, F.G. (1993) Relationship between fusaric acid uptake and its binding to cell structures by leaves of Egeria densa and its toxic effects on membrane permeability and respiration. Physiol Mol Plant Pathol 42: 141-157.
38. Menke, J., Dong, Y., and Kistler, H.C. (2012) Tri12p influences virulence to wheat and trichothecene accumulation. Mol Plant Microbe Interact 25: 1408-1418.
39. Michielse, C.B., Pfannmüller, A., Macios, M., Rengers, P., Dzikowska, A., and Tudzynski, B. (2014a) The interplay between the GATA transcription factors AreA, the global nitrogen regulator and AreB in Fusarium fujikuroi. Mol Microbiol 91: 472-493.
40. Michielse, C.B., Studt, L., Janevska, S., Sieber, C.M.K., Arndt, B., Espino, J.J., etal. (2014b) The global regulator FfSge1 is required for expression of secondary metabolite gene clusters but not for pathogenicity in Fusarium fujikuroi. Environ Microbiol 17: 2690-2708.
41. Mihlan, M., Homann, V., Liu, T.W.D., and Tudzynski, B. (2003) AREA directly mediates nitrogen regulation of gibberellin biosynthesis in Gibberella fujikuroi, but its activity is not affected by NMR. Mol Microbiol 47: 975-991.
42. Miwa, T. (1979) Studies on the association of cytochrome P-450 and NADPH-cytochrome c reductase during catalysis in a reconstituted hydroxylating system. J Biol Chem 254: 5695-5700.
43. Niehaus, E.M., Kleigrewe, K., Wiemann, P., Studt, L., Sieber, C.M.K., Connolly, L.R., etal. (2013) Genetic manipulation of the Fusarium fujikuroi fusarin gene cluster yields insight into the complex regulation and fusarin biosynthetic pathway. Chem Biol 20: 1055-1066.
44. Niehaus, E.M., von Bargen, K.W., Espino, J.J., Pfannmüller, A., Humpf, H.U., and Tudzynski, B. (2014a) Characterization of the fusaric acid gene cluster in Fusarium fujikuroi. Appl Microbiol Biotechnol 98: 1749-1762.
45. Niehaus, E.M., Díaz-Sánchez, V., von Bargen, K.W., Kleigrewe, K., Humpf, H.U., Limón, M.C., and Tudzynski, B. (2014b) Fusarins and fusaric acid in fusaria. In Biosynthesis and Molecular Genetics of Fungal Secondary Metabolites, Fungal Biology. Martín, J.F., García-Estrada, C., and Zeilinger, S. (eds). New York, NY, USA: Springer, pp. 239-262.
46. Niehaus, E.M., Janevska, S., von Bargen, K.W., Sieber, C.M.K., Harrer, H., Humpf, H.U., and Tudzynski, B. (2014c) Apicidin F: characterization and genetic manipulation of a new secondary metabolite gene cluster in the rice pathogen Fusarium fujikuroi. PLoS ONE 9: e103336.
47. Norman, A.W. (1998) Sunlight, season, skin pigmentation, vitamin D, and 25-hydroxyvitamin D: integral components of the vitamin D endocrine system. Am J Clin Nutr 67: 1108-1110.
48. Pavesi, G., Mereghetti, P., Mauri, G., and Pesole, G. (2004) Weeder Web: discovery of transcription factor binding sites in a set of sequences from co-regulated genes. Nucleic Acids Res 32: W199-W203.
49. Pfaffl, M.W. (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29: e45.
50. Pluskal, T., Castillo, S., Villar-Briones, A., and Oresic, M. (2010) MZmine 2: modular framework for processing, visualizing, and analyzing mass spectrometry-based molecular profile data. BMC Bioinformatics 11: 395-406.
51. Pontecorvo, G., Roper, J.A., Hemmons, L.M., MacDonald, K.D., and Bufton, A.W.J. (1953) The genetics of Aspergillus nidulans. Adv Genet 5: 141-238.
52. Riclea, R., and Dickschat, J.S. (2015) Identification of intermediates in the biosynthesis of PR toxin by Penicillium roqueforti. Angew Chem Int Ed Engl 54: 1-5.
53. Sambrook, J., Fritsch, E.F., and Maniatis, T. (1989) Molecular Cloning: A Laboratory Manual. Cold Spring Harbor, N.Y.: Cold Spring Harbor Laboratory Press.
54. Scharf, D.H., Remme, N., Heinekamp, T., Hortschansky, P., Brakhage, A.A., and Hertweck, C. (2010) Transannular disulfide formation in gliotoxin biosynthesis and its role in self-resistance of the human pathogen Aspergillus fumigatus. J Am Chem Soc 132: 10136-10141.
55. Schrettl, M., Carberry, S., Kavanagh, K., Haas, H., Jones, G.W., O'Brien, J., etal. (2010) Self-protection against gliotoxin - a component of the gliotoxin biosynthetic cluster, GliT, completely protects Aspergillus fumigatus against exogenous gliotoxin. PLoS Pathog 6: e1000952.
56. 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.
57. Schumacher, J. (2015) DHN melanin biosynthesis in the plant pathogenic fungus Botrytis cinerea is based on two developmentally regulated key enzyme (PKS)-encoding genes. Mol Microbiol doi: 10.1111/mmi.13262. [Epub ahead of print].
58. Sørensen, J.L., Sondergaard, T.E., Covarelli, L., Fuertes, P.R., Hansen, F.T., Frandsen, R.J.N., etal. (2014) Identification of the biosynthetic gene clusters for the lipopeptides fusaristatin A and W493 B in Fusarium graminearum and F.pseudograminearum. J Nat Prod 77: 2619-2625.
59. Staben, C., Jensen, B., Singer, M., Pollock, J., Schechtman, M.J.K., and Selker, E.U. (1989) Use of a bacterial Hygromycin B resistance gene as a dominant selectable marker in N.crassa transformation. Fungal Genet Newsl 36: 79-81.
60. Stack, D., Neville, C., and Doyle, S. (2007) Nonribosomal peptide synthesis in Aspergillus fumigatus and other fungi. Microbiology 153: 1297-1306.
61. Stipanovic, R.D., Puckhaber, L.S., Liu, J., and Bell, A.A. (2011a) Phytotoxicity of fusaric acid and analogs to cotton. Toxicon 57: 176-178.
62. Stipanovic, R.D., Wheeler, M.H., Puckhaber, L.S., Liu, J., Bell, A.A., and Williams, H.J. (2011b) Nuclear magnetic resonance (NMR) studies on the biosynthesis of fusaric acid from Fusarium oxysporum f. sp. vasinfectum. J Agric Food Chem 59: 5351-5356.
63. Studt, L., Wiemann, P., Kleigrewe, K., Humpf, H.U., and Tudzynski, B. (2012) Biosynthesis of fusarubins accounts for pigmentation of Fusarium fujikuroi perithecia. Appl Environ Microbiol 78: 4468-4480.
64. Teichert, S., Schönig, B., Richter, S., and Tudzynski, B. (2004) Deletion of the Gibberella fujikuroi glutamine synthetase gene has significant impact on transcriptional control of primary and secondary metabolism. Mol Microbiol 53: 1661-1675.
65. Tudzynski, B., Mende, K., Weltring, K.M., Kinghorn, J.R., and Unkles, S.E. (1996) The Gibberella fujikuroi niaD gene encoding nitrate reductase: isolation, sequence, homologous transformation and electrophoretic karyotype location. Microbiology 142: 533-539.
66. Tudzynski, B., Homann, V., Feng, B., and Marzluf, G.A. (1999) Isolation, characterization and disruption of the areA nitrogen regulatory gene of Gibberella fujikuroi. Mol Gen Genet 261: 106-114.
67. Wang, D.N., Toyotome, T., Muraosa, Y., Watanabe, A., Wuren, T., Bunsupa, S., etal. (2014) GliA in Aspergillus fumigatus is required for its tolerance to gliotoxin and affects the amount of extracellular and intracellular gliotoxin. Med Mycol 52: 506-518.
68. Wang, H., and Ng, T.B. (1999) Pharmacological activities of fusaric acid (5-butylpicolinic acid). Life Sci 65: 849-856.
69. Wiemann, P., Willmann, A., Straeten, M., Kleigrewe, K., Beyer, M., Humpf, H.U., and Tudzynski, B. (2009) Biosynthesis of the red pigment bikaverin in Fusarium fujikuroi: genes, their function and regulation. Mol Microbiol 72: 931-946.
70. Wiemann, P., Brown, D.W., Kleigrewe, K., Bok, J.W., Keller, N.P., Humpf, H.U., and Tudzynski, B. (2010) FfVel1 and FfLae1, components of a velvet-like complex in Fusarium fujikuroi, affect differentiation, secondary metabolism and virulence. Mol Microbiol 77: 972-994.
71. Wiemann, P., Sieber, C.M.K., von Bargen, K.W., Studt, L., Niehaus, E.M., Espino, J.J., etal. (2013) Deciphering the cryptic genome: genome-wide analyses of the rice pathogen Fusarium fujikuroi reveal complex regulation of secondary metabolism and novel metabolites. PLoS Pathog 9: e1003475.
72. Wingender, E., Chen, X., Fricke, E., Geffers, R., Hehl, R., Liebich, I., etal. (2001) The TRANSFAC system on gene expression regulation. Nucleic Acids Res 29: 281-283.
73. Winston, F., Dollard, C., and Ricupero-Hovasse, S.L. (1995) Construction of a set of convenient Saccharomyces cerevisiae strains that are isogenic to S288C. Yeast 11: 53-55.