Advertisement

Applied Microbiology and Biotechnology

, Volume 66, Issue 6, pp 597–611 | Cite as

Gibberellin biosynthesis in fungi: genes, enzymes, evolution, and impact on biotechnology

  • Bettina Tudzynski
Mini-Review

Abstract

Gibberellins (GAs) constitute a large family of tetracyclic diterpenoid carboxylic acids, some members of which function as growth hormones in higher plants. As well as being phytohormones, GAs are also present in some fungi and bacteria. In recent years, GA biosynthetic genes from Fusarium fujikuroi and Arabidopsis thaliana have been cloned and well characterised. Although higher plants and the fungus both produce structurally identical GAs, there are important differences indicating that GA biosynthetic pathways have evolved independently in higher plants and fungi. The fact that horizontal gene transfer of GA genes from the plant to the fungus can be excluded, and that GA genes are obviously missing in closely related Fusarium species, raises the question of the origin of fungal GA biosynthetic genes. Besides characterisation of F. fujikuroi GA pathway genes, much progress has been made in the molecular analysis of regulatory mechanisms, especially the nitrogen metabolite repression controlling fungal GA biosynthesis. Basic research in this field has been shown to have an impact on biotechnology. Cloning of genes, construction of knock-out mutants, gene amplification, and regulation studies at the molecular level are powerful tools for improvement of production strains. Besides increased yields of the final product, GA3, it is now possible to produce intermediates of the GA biosynthetic pathway, such as ent-kaurene, ent-kaurenoic acid, and GA14, in high amounts using different knock-out mutants. This review concentrates mainly on the fungal biosynthetic pathway, the genes and enzymes involved, the regulation network, the biotechnological relevance of recent studies, and on evolutionary aspects of GA biosynthetic genes.

Keywords

Graminearum P450 Monooxygenases Fusaric Acid Bikaverin Neurosporaxanthin 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgements

I thank Barbara Berns for typing the manuscript and Paul Tudzynski for critical reading of the manuscript. I am very thankful for the excellent collaboration with Peter Hedden (Rothamsted Research, UK) and Cecilia Rojas (Universidad de Chile) for the past 6 years

References

  1. Andrianopoulos A, Kourambas S, Sharp JA, Davis MA, Hynes MJ (1998) Characterization of the Aspergillus nidulans nmrA gene involved in nitrogen metabolite repression. J Bacteriol 180:1973–1977PubMedGoogle Scholar
  2. Avalos J, Fernandez-Martin R, Prado MM, Cerda-Olmedo E (1999) Gibberellin biosynthesis in Gibberella. Acta Bot Gallica 146:55–65Google Scholar
  3. Avalos J, Sanchez-Fernandez R, Fernandez-Martin R, Candau R (1997) Regulation of gibberellin production in the fungus Gibberella fujikuroi. Recent Res Dev Plant Physiol 1:105–115Google Scholar
  4. Bacon CW, Porter JK, Norred WP, Leslie JF (1996) Production of fusaric acid by Fusarium species. Appl Environ Microbiol 62:4039–4043PubMedGoogle Scholar
  5. Barrero AF, Oltra JE, Cabrera E, Reyes F, Álvarez M (1999) Metabolism of gibberellins and ent-kaurenoids in mutants of Gibberella fujikuroi. Phytochemistry 50:1133–1140CrossRefGoogle Scholar
  6. Barrero AF, Oltra JE, Cerda-Olmedo E, Avalos J, Justicia J (2001) Microbial transformation of ent-kaurenoic acid and its 15-hydroxy derivatives by the SG138 mutant of Gibberella fujikuroi. J Nat Prod 64:222–225CrossRefPubMedGoogle Scholar
  7. Bearder JR (1983) In vivo diterpenoid biosynthesis in Gibberella fujikuroi: the pathway after ent-kaurene. In: Crozier A (ed) The biochemistry and physiology of gibberellins. Praeger, New YorkGoogle Scholar
  8. Bearder JR, MacMillan J, Wels CM, Chaffey MB, Phinney BO (1974) Position of the metabolic block for gibberellin biosynthesis in mutant B1-41a of Gibberella fujikuroi. Phytochemistry 13:911–917CrossRefGoogle Scholar
  9. Binks R, MacMillan J, Pryce R (1969) Combined gas chromatography-mass spectrometry of the methyl esters of gibberellins A1 toA24 and their trimethylsilyl ethers. Phytochemistry 8:271–284CrossRefGoogle Scholar
  10. Birch AJ, Richards RW, Smith H (1958) The biosynthesis of gibberellic acid. Proc Chem Soc 1:192–193Google Scholar
  11. Birch AJ, Richards RW, Smith H, Harris A, Whalley WB (1959) Studies in relation to biosynthesis: XII. Rosenonolactone and gibberellic acid. Tetrahedron 7:241–251CrossRefGoogle Scholar
  12. Borrow A, Brian PW, Chester VE, Curtis PJ, Hemming HG, Henehan C, Jefferys EG, Lloyd PB, Nixon IS, Norris GLF, Radley M (1955) Gibberellic acid, a metabolic product of the fungus Gibberella fujikuroi: some observations on its production and isolation. J Sci Food Agric 6:340–348Google Scholar
  13. Borrow A, Brown S, Jefferys EG, Kessel RJH, Lloyd PG, Rothwell A, Rothwell B, Swait JC (1964) Metabolism of Gibberella fujikuroi in stirred culture. Can J Microbiol 10:407–444PubMedGoogle Scholar
  14. Britz H, Coutinho TA, Wingfield MJ, Marasas WFO, Gordon TR, Leslie JF (1999) Fusarium subglutinans f. sp. pini represents a distinct mating population in the Gibberella fujikuroi species complex. Appl Environ Microbiol 65:1198–1201PubMedGoogle Scholar
  15. Brückner B, Blechschmidt D (1991) Nitrogen regulation of gibberellin biosynthesis in Gibberella fujikuroi. Appl Microbiol Biotechnol 53:646–650Google Scholar
  16. Caddick MX (1994) Nitrogen metabolite repression. Prog Ind Microbiol 29:323–353PubMedGoogle Scholar
  17. Candau R, Avalos J, Cerdá-Olmedo E (1992) Regulation of gibberellin biosynthesis in Gibberella fujikuroi. Plant Physiol 100:1184–1188Google Scholar
  18. Cassan FD, Lucangeli CD, Bottini R, Piccoli PN. (2001) Azospirillum spp. metabolize [17,17-2H2]gibberellin A20 to [17,17-2H2]gibberellin A1 in vivo in dy rice mutant seedlings. Plant Cell Physiol 42:763–767CrossRefPubMedGoogle Scholar
  19. Chapman DJ, Regan MA (1980) Evolution of a biochemical pathway: evidence from comparative biochemistry. Annu Rev Plant Physiol 31:639–645CrossRefGoogle Scholar
  20. Chappel J (1995) The biochemistry and molecular biology of the isoprenoid metabolism. Plant Physiol 107:1–6PubMedGoogle Scholar
  21. Coque JJ, Enguita FJ, Martin JF, Liras P (1995) A two-protein component 7 alpha-cephem-methoxylase encoded by two genes of the cephamycin C cluster converts cephalosporin C to 7-methoxycephalosporin C. J Bacteriol 177:2230–2235PubMedGoogle Scholar
  22. Cross BE, Grove JF, MacMillan J, Moffat JS, Mulholland TPC, Seaton JC, Sheppard N (1959) A revised structure for gibberellic acid. Proc Chem Soc 302–303Google Scholar
  23. Crozier A (1983) The biochemistry and physiology of gibberellins. Praeger, New YorkGoogle Scholar
  24. Darken MA, Jensen AAL, Shu P (1959) Production of gibberellic acid by fermentation. Appl Microbiol 7:301PubMedGoogle Scholar
  25. Desjardins AE (2003) Gibberella from A (venaceae) to Z (eae). Annu Rev Phytopathol 41:177–198CrossRefPubMedGoogle Scholar
  26. Desjardins AE, Plattner RD, Nelsen TC, Leslie JF (1995) Genetic analysis of fumonisin production and virulence of Gibberella fujikuroi mating population A (Fusarium moniliforme) on maize (Zea mays) seedlings. Appl Environ Microbiol 61:79–86PubMedGoogle Scholar
  27. Desjardins AE, Plattner RD, Nelson PE (1997) Production of fumonisin B1 and moniliformin by Gibberella fujikuroi from rice from various geographic areas. Appl Environ Microbiol 63:1838–1842Google Scholar
  28. Desjardins AE, Manandhar G, Plattner RD, Maragos CM, Shrestha K, McCormick SP (2000) Occurrence of Fusarium species and mycotoxins in Nepalese maize and wheat and the effect of traditional processing methods on mycotoxin levels. J Agric Food Chem 48:1377–1383CrossRefPubMedGoogle Scholar
  29. Domenech CE, Giordano W, Avalos J, Cerda-Olmedo E (1996) Separate compartments for the production of sterols, carotenoids and gibberellins in Gibberella fujikuroi. Eur J Biochem 239:720–725CrossRefPubMedGoogle Scholar
  30. El-Bahrawi S (1977) Survey of some Fusarium moniliforme strains from different host plants for compounds possessing gibberellin-like activity. Zentralbl Bakteriol Parasitenkd Infektionskr Hyg 132:178–183PubMedGoogle Scholar
  31. Feng B, Friedlin E, Marzluf GA (1995) Nuclear DNA-binding proteins which recognize the ditergenic control region of penicillin biosynthetic genes. Curr Genet 27:351–358CrossRefPubMedGoogle Scholar
  32. Fierro F, Barredo JL, Diez B, Gutierrez S, Fernandez FJ, Martin JF (1995) The penicillin gene cluster is amplified in tandem repeats linked by conserved hexanucleotide sequences. Proc Natl Acad Sci USA 92:6200–6204PubMedGoogle Scholar
  33. Fuska J, Kuhr I, Podojil M, Sevcik V (1961) The influence of the nitrogen source on the production of gibberellic acid in submerse cultivation of Gibberella fujikuroi. Folia Microbiol 6:18–20Google Scholar
  34. Geissman TA, Verbiscar AJ, Phinney BO, Cragg G (1966) Studies on the biosynthesis of gibberellins from (−)-kaurenoic acid in cultures of Gibberella fujikuroi. Phytochemistry 5:933–947CrossRefGoogle Scholar
  35. Graebe JE, Dennis DT, Upper CD, West CA (1965) Biosynthesis of gibberellins. I. The biosynthesis of (−)-kaurene, (−)-kauren-19-ol and trans-geranylgeraniol in endosperm nucellus of Echicocystis macrocarpa Greene. J Biol Chem 240:1847–1854PubMedGoogle Scholar
  36. Graebe JE, Hedden P, Gaskin P, MacMillan J (1974) Biosynthesis of gibberellins A12, A15, A24, A36, and A37 by a cell-free system from Cucurbita maxima. Phytochemistry 13:1433–1440CrossRefGoogle Scholar
  37. Hedden P, Hoad GV, Gaskin P, Lewis MJ, Green JR, Furber M, Mander LN (1993) Kaurenoids and gibberellins, including the newly characterized gibberellin-A88, in developing apple seeds. Phytochemistry 32:231–237CrossRefGoogle Scholar
  38. Hedden P, Phillips A (2000a) Gibberellin metabolism: new insights revealed by the genes. Trends Plant Sci 5:523–530CrossRefPubMedGoogle Scholar
  39. Hedden P, Phillips AL (2000b) Manipulation of hormone biosynthetic genes in transgenic plants. Curr Opin Biotechnol 11:130–137CrossRefPubMedGoogle Scholar
  40. Hedden P, MacMillan J, Phinney BO (1974) Fungal products. Part XII. Gibberellin A14-aldehyde, an intermediate in gibberellin biosynthesis in Gibberella fujikuroi. J Chem Soc Perkin Trans 1:587–592CrossRefGoogle Scholar
  41. Hedden P, Phillips AL, Rojas MC, Carrera E, Tudzynski B (2001) Gibberellin biosynthesis in plants and fungi: a case of convergent evolution? J Plant Growth Regul 20:319–331CrossRefPubMedGoogle Scholar
  42. Hedden P (2003) The genes of the Green Revolution. Trends Genet 19:5–9CrossRefPubMedGoogle Scholar
  43. Helliwell CA, Sheldon CC, Olive MR, Walker AR, Zeevaart JA, Peacock WJ, Dennis ES (1998) Cloning of the Arabidopsis ent-kaurene oxidase gene GA3. Proc Natl Acad Sci USA 95:9019–9024CrossRefPubMedGoogle Scholar
  44. Helliwell CA, Chandler PM, Poole A, Dennis ES, Peacock WJ (2001) The CYP88A cytochrome P450, ent-kaurenoic acid oxidase, catalyzes three steps of the gibberellin biosynthesis pathway. Proc Natl Acad Sci USA 98:2065–2070CrossRefPubMedGoogle Scholar
  45. Homann V, Mende K, Arntz C, Ilardi V, Macino G, Morelli G, Böse G, Tudzynski B (1996) The isoprenoid pathway: cloning and characterization of fungal FPPS genes. Curr Genet 30:232–239CrossRefPubMedGoogle Scholar
  46. Huang SS, Raman AS, Ream JE, Fujiwara H, Cerny RE, Brown SM (1998) Overexpression of 20-oxidase confers a gibberellin-overproduction phenotype in Arabidopsis. Plant Physiol 118:773–781CrossRefPubMedGoogle Scholar
  47. Jarai G, Marzluf GA (1990) Analysis of conventional and in vitro generated mutants of nmr, the negatively acting nitrogen regulatory gene of Neurospora crassa. Mol Gen Genet 222:233–240PubMedGoogle Scholar
  48. Kamiya Y, Graebe JE (1983) The biosynthesis of all major pea gibberellins in a cell-free system from Pisum sativum. Phytochemistry 22:681–689CrossRefGoogle Scholar
  49. Kawaide H, Sassa T, Kamiya Y (1995) Plant-like biosynthesis of gibberellin A1 in the fungus Phaeosphaeria sp. L487. Phytochemistry 39:305–310CrossRefGoogle Scholar
  50. Kawaide H, Imai R, Sassa T, Kamiya Y (1997) ent-Kaurene synthase from the fungus Phaeosphaeria sp. L487-cDNA isolation, characterization, and bacterial expression of a bidunctional diterpene cyclase in fungal gibberellin biosynthesis. J Biol Chem 272:21706–21712CrossRefPubMedGoogle Scholar
  51. Kedera CJ, Plattner RD, Desjardins AE (1999) Incidence of Fusarium spp. and levels of fumonisin B1 in maize in western Kenya. Appl Environ Microbiol 65:41–44PubMedGoogle Scholar
  52. Keller N, Hohn T (1997) Metabolic pathway gene cluster in filamentous fungi. Fungal Genet Biol 21:17–29CrossRefPubMedGoogle Scholar
  53. Kerényi Z, Zeller K, Hornok L, Leslie JF (1999) Standardization of mating type terminology in the Gibberella fujikuroi species complex. Appl Environ Microbiol 65:4071–4076Google Scholar
  54. Kosalkova K, Marcos AT, Martin JF (2001) A moderate amplification of the mecB gene encoding cystathionine-gamma-lyase stimulates cephalosporin biosynthesis in Acremonium chrysogenum. J Ind Microbiol Biotechnol 27:252–258CrossRefPubMedGoogle Scholar
  55. Lamb DC, Kelly DE, Manning NJ, Kaderbhai MA, Kelly SL (1990) Biodiversity of the P450 catalytic cycle: Yeast cytochrome b5/NADH cytochrome b5 reductase complex efficiently drives the entire sterol 14-demethylation (CYP51) reaction. FEBS Lett 462:283–288CrossRefGoogle Scholar
  56. Lang A (1956) Bolting and flowering in biennial Hyoscyamus niger, induced by gibberellic acid. Plant Physiol 31[Suppl]:XXXVGoogle Scholar
  57. Lange T (1998) Molecular biology of gibberellin synthesis. Planta 204:409–419CrossRefPubMedGoogle Scholar
  58. Lange T, Hedden P, Graebe JE, Lange T (1994) Expression cloning of a gibberellin 20-oxidase, a multifunctional enzyme involved in gibberellin biosynthesis. Proc Natl Acad Sci USA 91:8552–8556PubMedGoogle Scholar
  59. Lawrence JG (1997) Selfish operons and speciation by gene transfer. Trends Microbiol 5:355–359CrossRefPubMedGoogle Scholar
  60. Leslie JF (1995) Gibberella fujikuroi: available populations and variable traits. Can J Bot 73:S282–S291Google Scholar
  61. Leslie JF (1996) Introductory biology of Fusarium moniliforme. Adv Exp Med Biol 392:153–164PubMedGoogle Scholar
  62. Leslie JF, Doe RD, Plattner D, Shackelford D, Jonz J (1992) Fumonisin B1 production and vegetative compatibility of strains from Gibberella fujikuroi mating population “A” (Fusarium moniliforme). Mycopathology 117:37–46CrossRefGoogle Scholar
  63. Leslie JF, Marasas WFO, Shephard GS, Sydenham EW, Stockenström S, Thiel PG (1996b) Duckling toxicity and the production of fumonisin and moniliformin by isolates in the A and F mating populations of Gibberella fujikuroi (Fusarium moniliforme). Appl Environ Microbiol 62:1182–1187PubMedGoogle Scholar
  64. Leslie JF, Zeller KA, Logrieco A, Mule G, Moretti A, Ritieni A (2004) Species diversity of and toxin production by Gibberella fujikuroi species complex strains isolated from native prairie grasses in Kansas. Appl Environ Microbiol 70:2254–2262CrossRefPubMedGoogle Scholar
  65. Linnemannstöns P, Prado MM, Fernandez-Martin R, Tudzynski B, Avalos J (2002a) A carotenoid biosynthesis gene cluster in Fusarium fujikuroi: the genes carB and carRA. Mol Genet Genomics 267:593–602CrossRefPubMedGoogle Scholar
  66. Linnemannstöns P, Schulte J, del Mar Prado M, Proctor RH, Avalos J, Tudzynski B (2002b) The polyketide synthase gene pks4 from Gibberella fujikuroi encodes a key enzyme in the biosynthesis of the red pigment bikaverin. Fungal Genet Biol 37:143–148Google Scholar
  67. Logrieco A, Moretti A, Castella G, Kostecki M, Golinski P, Ritieni A, Chelkowski J (1998) Beauvericin production by Fusarium species. Appl Environ Microbiol 64:3084–3088PubMedGoogle Scholar
  68. MacMillan J (1997) Biosynthesis of the gibberellin plant hormones. Nat Prod Res 14:221–243Google Scholar
  69. MacMillan J (2001) Occurrence of gibberellins in vascular plants, fungi, and bacteria. J Plant Growth Regul 20:387–442CrossRefPubMedGoogle Scholar
  70. MacMillan J, Pryce R, Eglington G, McCormick A (1967) Identification of gibberellins in crude extracts by combined gas chromatography-mass spectrometry. Tetrahedron Lett 24:2241–2243CrossRefGoogle Scholar
  71. Malonek S, Rojas MC, Hedden P, Gaskin P, Hopkins P, Tudzynski B (2004) The NADPH:cytochrome P450 reductase gene from Gibberella fujikuroi is essential for gibberellin biosynthesis. J Biol Chem 279:25075–25084CrossRefPubMedGoogle Scholar
  72. Marasas WFO (2001) Discovery and occurrence of the fumonisins: a historical perspective. Environ Health Perspect 109[Suppl 2]:239–243Google Scholar
  73. Marasas WFO, Thiel PG, Rabie CJ, Nelson PE, Toussoun TA (1986) Moniliformin production in Fusarium section Liseola. Mycologia 78:242–247Google Scholar
  74. Mende K, Homann V, Tudzynski B (1997) The geranylgeranyl diphosphate synthase gene of Gibberella fujikuroi: isolation and expression. Mol Gen Genet 255:96–105CrossRefPubMedGoogle Scholar
  75. Mihlan M, Homann V, Liu TWD, Tudzynski B (2003) AREA directly mediates nitrogen regulation of gibberellin biosynthesis in Gibberella fujikuroi, but its activity is not affected by NMR. Mol Microbiol 47:975–991CrossRefPubMedGoogle Scholar
  76. Muñoz GA, Agosin E (1993) Glutamine involvement in nitrogen control of gibberellic acid production in Gibberella fujikuroi. Appl Environ Microbiol 59:4317–4322Google Scholar
  77. Muromtsev GS, Agnistova VN (1984) Gibberellins (in Russian). In: Letunova SV (ed) Nauka, MoscowGoogle Scholar
  78. Newbert RW, Barton B, Greaves P, Harper J, Turner G (1997) Analysis of a commercially improved Penicillium chrysogenum strain series: involvement of recombinogenic regions in amplification and deletion of the penicillin biosynthesis gene cluster. J Ind Microbiol Biotechnol 19:18–27CrossRefPubMedGoogle Scholar
  79. Niki T, Nishijima T, Nakayama M, Hisamatsu T, Oyama-Okubo N, Yamazaki H, Hedden P, Lange T, Mander LN, Koshioka M (2001) Production of dwarf lettuce by overexpressing a pumpkin gibberellin 20-oxidase gene. Plant Physiol 126:965–967CrossRefPubMedGoogle Scholar
  80. Nirenberg HI, O’Donnell K (1998) New Fusarium species and combinations within the Gibberella fujikuroi species complex. Mycologia 90:434–458Google Scholar
  81. Nirenberg HI, O’Donnell K, Kroschel J, Andrianaivo AP, Frank JM, Mubatanhema W (1998) Two new species of Fusarium: Fusarium brevicatenulatum from the noxious weed Striga asiatica in Madagascar and Fusarium speudoanthophilum from Zea mays in Zimbabwe. Mycologia 90:459–464Google Scholar
  82. O’Donnell K, Cigelnik E (1997) Two divergent intragenomic rDNA ITS2 types within a monophyletic lineage of the fungus Fusarium are nonorthologous. Mol Phylogenet Evol 7:103–116CrossRefPubMedGoogle Scholar
  83. O’Donnell K, Cigelnik E, Nirenberg HI (1998) Molecular systematics and phylogeography of the Gibberella fujikuroi species complex. Mycologia 90:465–493Google Scholar
  84. Perez-Llarena FJ, Liras P, Rodriguez-Garcia A, Martin JF (1997) A regulatory gene (ccaR) required for cephamycin and clavulanic acid production in Streptomyces clavuligerus: amplification results in overproduction of both beta-lactam compounds. J Bacteriol 179:2053–2059PubMedGoogle Scholar
  85. Phillips AL, Ward DA, Uknes A, Appleford NEJ, Lange T, Huttly AK, Gaskin P, Graebe JE, Hedden P (1995) Isolation and expression of three gibberellin 20-oxidase cDNA clones from Arabidopsis. Plant Physiol 108:1049–1057CrossRefPubMedGoogle Scholar
  86. Phinney BO (1983) The history of gibberellins. In: Crozier A (ed) The biochemistry and physiology of gibberellins. Praeger, New YorkGoogle Scholar
  87. Proctor RH, Desjardins AE, Plattner RD (1999) Biosynthetic and genetic relationships of B-series fumonisins produced by Gibberella fujikuroi mating population A. Nat Toxins 7:251–258CrossRefPubMedGoogle Scholar
  88. Proctor RH, Brown DW, Plattner RD, Desjardins AE (2003) Co-expression of 15 contiguous genes delineates a fumonisin biosynthetic gene cluster in Gibberella moniliformis. Fungal Genet Biol 38:237–249CrossRefPubMedGoogle Scholar
  89. Rademacher W (1994) Gibberellin formation in microorganisms. J Plant Growth Regul 15:303–314CrossRefGoogle Scholar
  90. Radley M (1956) Occurrences of substances similar to gibberellic acid in higher plants. Nature 178:1070–1071Google Scholar
  91. Rojas MC, Hedden P, Gaskin P, Tudzynski B (2001) The P450-1 gene of Gibberella fujikuroi encodes a multifunctional enzyme in gibberellin biosynthesis. Proc Natl Acad Sci USA 98:5838–5843CrossRefPubMedGoogle Scholar
  92. Rojas MC, Urrutia O, Cruz C, Gaskin P, Tudzynski B, Hedden P (2004) Kaurenolides and fujenoic acids are side products of the gibberellin P450-1 monooxygenase in Gibberella fujikuroi. Phytochemistry 65:821–830CrossRefPubMedGoogle Scholar
  93. Song Z, Cox RJ, Lazarus CM, Simpson TJ (2004) Fusarin C biosynthesis in Fusarium moniliforme and Fusarium venenatum. Chem Bio Chem 5:1196–1203PubMedGoogle Scholar
  94. Steenkamp ET, Wingfield BD, Coutinho TA, Wingfield MJ, Marasas WFO (1999) Differentiation of Fusarium subglutinans f. sp. pini by histone gene sequence data. Appl Environ Microbiol 65:3401–3406PubMedGoogle Scholar
  95. Steenkamp ET, Wingfield BD, Coutinho TA, Zeller KA, Wingfield MJ, Marasas WFO, Leslie JF (2000) PCR-based identification of MAT-1 and MAT-2 in the Gibberella fujikuroi species complex. Appl Environ Microbiol 66:4378–4382CrossRefPubMedGoogle Scholar
  96. Sun TP, Kamiya Y (1994) The Arabidopsis GA1 locus encodes the cyclase ent-kaurene synthetase A of gibberellin biosynthesis. Plant Cell 6:1509–1518CrossRefPubMedGoogle Scholar
  97. Sun TP, Kamiya Y (1997) Regulation and cellular localization of ent-kaurene synthesis. Physiol Plant 101:701–708CrossRefGoogle Scholar
  98. Sun T, Zhao Y, Nonaka Y, Okamoto M (1995) Cloning and expression of cytochrome P450(11b) of Porcine adrenal cortex. J Steroid Biochem Biol 52:227–232CrossRefGoogle Scholar
  99. Suzuki K, Sanga K, Chikaoka Y, Itagaki E (1993) Purification and properties of cytochrome P-450 (P-450lun) catalyzing steroid 11 beta-hydroxylation in Curvularia lunata. Biochim Biophys Acta 1203:215–223PubMedGoogle Scholar
  100. Teichert S, Schönig B, Richter S, Tudzynski B (2004) Deletion of the Gibberella fujikuroi glutamine synthetase gene has significant impact on transcriptional control of primary and secondary metabolism. Mol Microbiol 53:1661–1675CrossRefPubMedGoogle Scholar
  101. Theilgaard HA, van den Berg MA, Mulder CA, Bovenberg RAL, Nielsen J (2001) Quantitative analysis of Penicillium chrysogenum Wis54-1255 transformants overexpressing the penicillin biosynthetic genes. Biotechnol Bioeng 72:379–388CrossRefPubMedGoogle Scholar
  102. Torres AM, Reynoso MM, Rojo FG, Ramirez ML, Chulze SN (2001) Fusarium species (section Liseola) and its mycotoxins in maize harvested in northern Argentina. Food Addit Contam 18:836–843PubMedGoogle Scholar
  103. Tudzynski B, Hölter K (1998) Gibberellin biosynthetic pathway in Gibberella fujikuroi: evidence for a gene cluster. Fungal Genet Biol 25:157–170CrossRefPubMedGoogle Scholar
  104. Tudzynski B (1999) Biosynthesis of gibberellins in Gibberella fujikuroi: biomolecular aspects. Appl Microbiol Biotechnol 52:198–310CrossRefGoogle Scholar
  105. Tudzynski B, Kawaide H, Kamiya Y (1998) Gibberellin biosynthesis in Gibberella fujikuroi: cloning and characterization of the copalyl diphosphate synthase gene. Curr Genet 34:234–240CrossRefPubMedGoogle Scholar
  106. 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 261:106–114CrossRefPubMedGoogle Scholar
  107. Tudzynski B, Hedden P, Carrera E, Gaskin P (2001) The P450-4 gene of Gibberella fujikuroi encodes ent-kaurene oxidase in the gibberellin biosynthesis pathway. Appl Environ Microbiol 67:3514–3522CrossRefPubMedGoogle Scholar
  108. Tudzynski B, Rojas MC, Gaskin P, Hedden P (2002) The Gibberella fujikuroi gibberellin 20-oxidase is a multifunctional monooxygenase. J Biol Chem 277:21264–21253CrossRefGoogle Scholar
  109. Tudzynski B, Mihlan M, Rojas MP, Gaskin P, Hedden P (2003) Characterization of the final two genes of the gibberellin biosynthesis gene cluster of Gibberella fujikuroi. J Biol Chem 278:28635–28643CrossRefPubMedGoogle Scholar
  110. Tudzynski B, Sharon A (2002) Biosynthesis, biological role and application of fungal phytohormones. In: Osiewacz HD (ed) The Mycota, vol 10. Industrial application. Springer, Berlin Heidelberg New YorkGoogle Scholar
  111. Urrutia O, Hedden P, Rojas MC (2001) Monooxygenases involved in GA12 and GA14 synthesis in Gibberella fujikuroi. Phytochemistry 56:505–511CrossRefPubMedGoogle Scholar
  112. Van den Brink JM, van Zeijl CJM, Brons JF, van den Hondel CAMJJ, van Gorcom RFM (1995) Cloning and characterization of the NADPH cytochrome P450 oxidoreductase gene from the filamentous fungus Aspergillus niger. DNA Cell Biol 14:719–729PubMedGoogle Scholar
  113. Voß T, Schulte J, Tudzynski B (2001) A new MFS-transporter gene next to the gibberellin biosynthesis gene cluster of Gibberella fujikuroi is not involved in gibberellin secretion. Curr Genet 39:377–383CrossRefPubMedGoogle Scholar
  114. Wiebe LA, Bjeldanes LF (1981) Fusarin C, a mutagen from Fusarium moniliforme. J Food Sci 46:1424–1426Google Scholar
  115. Woitek S, Unkles SE, Kinghorn JR, Tudzynski B (1997) 3-Hydroxy-3-methylglutaryl-CoA reductase gene of Gibberella fujikuroi: isolation and characterization. Curr Genet 31:38–47CrossRefPubMedGoogle Scholar
  116. Young C, McMillan L, Telfer E, Scott B (2001) Molecular cloning and genetic analysis of an indole-diterpene gene cluster from Penicillium paxilli. Mol Microbiol 39:754–764CrossRefPubMedGoogle Scholar
  117. Yun SH, Arie T, Kaneko I, Yoder OC, Turgeon BG (2000) Molecular organization of mating type loci in heterothallic, homothallic, and asexual Gibberella/Fusarium species. Fungal Genet Biol 31:7–20CrossRefPubMedGoogle Scholar
  118. Zeller KA, Summerell BA, Bullock S, Leslie JF (2003) Gibberella konza (Fusarium konzum) sp. Nov. From prairie grasses, a new species in the Gibberella fujikuroi species complex. Mycologia 95:943–954Google Scholar

Copyright information

© Springer-Verlag 2004

Authors and Affiliations

  1. 1.Institut für Botanik der Westfälischen Wilhelms-Universität MünsterMünsterGermany

Personalised recommendations