The ergot alkaloid gene cluster: Functional analyses and evolutionary aspects

Phytochemistry

Volumn 70, Issue 15-16, 2009, Pages 1822-1832

  Lorenz, Nicole ^a   Haarmann, Thomas ^a   Pažoutová, Sylvie ^b   Jung, Manfred ^c   Tudzynski, Paul ^a  

^a UNIVERSITY OF MÜNSTER   (Germany)

^b INSTITUTE OF MICROBIOLOGY   (Czech Republic)

^c UNIVERSITY OF FREIBURG   (Germany)

Author keywords

Claviceps purpurea; Ergopeptines; Ergot alkaloid gene cluster; Ergot fungus

Indexed keywords

ERGOT ALKALOID;

AMINO ACID SEQUENCE; CHEMICAL STRUCTURE; CHEMISTRY; CLAVICEPS; FUNGAL GENE; GENETICS; METABOLISM; MOLECULAR EVOLUTION; REVIEW;

AMINO ACID SEQUENCE; CLAVICEPS; ERGOT ALKALOIDS; EVOLUTION, MOLECULAR; GENES, FUNGAL; MOLECULAR STRUCTURE;

CLAVICEPS; CLAVICEPS PURPUREA; FUNGI;

EID: 70350742023     PISSN: 00319422     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.phytochem.2009.05.023     Document Type: Review

References (81)

1. Alderman S.C. Diversity and speciation in Claviceps. In: White J.F., Bacon C.W., and Hywel-Jones N.L. (Eds). Clavicipitalean Fungi: Evolutionary Biology, Chemistry, Biocontrol and Cultural Impacts (2003), Marcel Dekker, New York, Basel 195-245
2. Alderman S.C., Coats D.D., Crowe F.J., and Butler M.D. Occurrence and distribution of ergot and estimates of seed loss in Kentuckey bluegrass grown for seed in central Oregon. Plant Dis. 82 (1998) 89-93
3. Alex L.A., Borkovich K.A., and Simon M.I. Hyphal development in Neurospora crassa: involvement of a two-component histidine kinase. Proc. Natl. Acad. Sci. USA 93 (1996) 3416-3421
4. Andrianopoulos A., Kourambas S., Sharp J.A., Davis M.A., and Hynes M.J. Characterization of the Aspergillus nidulans nmrA gene involved in nitrogen metabolite repression. J. Bacteriol. 180 (1998) 1973-1977
5. Arcamone F., Bonino C., Chain E.B., Ferretti A., Pennella P., Tonolo A., and Vero L. Production of lysergic acid derivatives by a strain of Claviceps paspali Stevens and Hall in submerged culture. Nature 187 (1960) 238-239
6. Bakana P., Claeys M., Totté J., Pieters L.A., Van Hoof L., Vemba T., Van den Berghe D.A., and Vlietinck A.J. Structure and chemotherapeutical activity of a polyisoprenylated benzophenone from the stem bark of Garcinia huillensis. J. Ethnopharmacol. 21 (1987) 75-84
7. Ball O.J.P., Miles C.O., and Prestidge R.A. Ergopeptine alkaloids and Neotyphodium lolii-mediated resistance in perennial ryegrass against adult Heteronychus arator (Coleoptera, Scarabaeidae). J. Econ. Entomol. 90 (1997) 1382-1391
8. Berde B., and Stürmer E. Introduction to the pharmacology of ergot alkaloids and related compounds. In: Berde B., and Schild H.O. (Eds). Ergot Alkaloids and Related Compounds (1978), Springer, Berlin, Heidelberg, New York 1-28
9. Bok J.W., and Keller N.P. LaeA, a regulator of secondary metabolism in Aspergillus spp. Eukaryotic Cell 3 (2004) 527-535
10. Bové F.J. The Story of Ergot (1970), S. Karger, Basel
11. Bush L.P., Wilkinson H.H., and Schardl C.L. Bioprotective alkaloids of grass-fungal endophyte symbioses. Plant Physiol. 114 (1997) 1-7
12. Catlett N.L., Yoder O.C., and Turgeon B.G. Whole-genome analysis of two-component signal transduction genes in fungal pathogens. Eukaryotic Cell 2 (2003) 1151-1161
13. Cheng L.J., Robbers J.E., and Floss H.G. End-product regulation of ergot alkaloid formation in intact cells and protoplasts of Claviceps species, strain SD58. J. Nat. Prod. 43 (1980) 329-339
14. Clay K., and Cheplick G.P. Effect of ergot alkaloids from fungal endophyte-infected grasses on fall armyworm (Spodoptera frugiperda). J. Chem. Ecol. 15 (1989) 169-182
15. Correia T., Grammel N., Ortel I., Tudzynski P., and Keller U. Molecular cloning and analysis of the ergopeptine assembly system in the ergot fungus Claviceps purpurea. Chem. Biol. 10 (2003) 1281-1292
16. Davie J.R. Covalent modifications of histones: expression from chromatin templates. Genes Dev. 8 (1998) 173-178
17. Ehmann A. The van Urk-Salkowski reagent - a sensitive and specific chromogenic reagent for silica gel thin-layer chromatographic detection and identification of indole derivatives. J. Chromatogr. 132 (1977) 267-276
18. Eich E., and Pertz H. Antimicrobial and antitumor effects of ergot alkaloids and their derivatives. In: Kren V., and Cvak L. (Eds). Ergot: The Genus Claviceps (1999), Harwood Academic Publishers, Amsterdam 441-449
19. Eich E., Eichberg D., and Müller W.E. Clavines - new antibiotics with cytostatic activity. Biochem. Pharmacol. 33 (1984) 523-526
20. Eliseeva E.D., Valkov V., Jung M., and Jung M.O. Characterization of novel inhibitors of histone acetyltransferases. Mol. Cancer Ther. 6 (2007) 2391-2398
21. Felsenstein J. Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39 (1985) 783-791
22. Fleetwood D.J., Scott B., Lane G.A., Tanaka A., and Johnson R.D. A complex ergovaline gene cluster in epichloe endophytes of grasses. Appl. Environ. Microbiol. 73 (2007) 2571-2579
23. Frederickson D.E., Mantle P.G., and de Milliano W.A.J. Claviceps africana sp. Nov.; the distinctive ergot pathogen of sorghum in Africa. Mycol. Res. 95 (1991) 1101-1107
24. Fuentes S.F., de la Isla M.-L., Ullstrup A.J., and Rodriguez A.E. Claviceps gigantea, pathogen of maize in Mexico. Phytopathology 54 (1964) 379-381
25. Galagan J.E., Calvo S.E., Cuomo C., Ma L.J., Wortman J.R., Batzoglou S., Lee S.I., Basturkmen M., Spevak C.C., Clutterbuck J., Kapitonov V., Jurka J., Scazzocchio C., Farman M., Butler J., Purcell S., Harris S., Braus G.H., Draht O., Busch S., D'Enfert C., Bouchier C., Goldman G.H., Bell-Pedersen D., Griffiths-Jones S., Doonan J.H., Yu J., Vienken K., Pain A., Freitag M., Selker E.U., Archer D.B., Penalva M.A., Oakley B.R., Momany M., Tanaka T., Kumagai T., Asai K., Machida M., Nierman W.C., Denning D.W., Caddick M., Hynes M., Paoletti M., Fischer R., Miller B., Dyer P., Sachs M.S., Osmani S.A., and Birren B.W. Sequencing of Aspergillus nidulans and comparative analysis with A. Fumigatus and A. oryzae. Nature 438 (2005) 1105-1115
26. Gebler J.C., and Poulter D. Purification and characterization of dimethylallyl tryptophan synthase from Claviceps purpurea. Arch. Biochem. Biophys. 296 (1992) 308-313
27. Grunstein M. Histone acetylation in chromatin structure and transcription. Nature 389 (1997) 349-352
28. Haarmann T., Machado C., Lübbe Y., Correia T., Schardl C.L., Panaccione D.G., and Tudzynski P. The ergot alkaloid gene cluster in Claviceps purpurea: extension of the cluster sequence and intra species evolution. Phytochemistry 66 (2005) 1312-1320
29. Haarmann T., Ortel I., Tudzynski P., and Keller U. Identification of the cytochrome P450 monooxygenase that bridges the clavine and ergoline alkaloid pathways. ChemBioChem 7 (2006) 645-652
30. Haarmann T., Lorenz N., and Tudzynski P. Use of a nonhomologous end joining deficient strain (Δku70) of the ergot fungus Claviceps purpurea for identification of the nonribosomal peptide synthetase gene involved in ergotamine biosynthesis. Fungal Genet. Biol. 45 (2008) 35-44
31. Kantorová M., Kolínská R., Pažoutová S., Honzátko A., Havlicek V., and Flieger M. Ergot alkaloids produced by submerged cultures of Claviceps zizaniae. J. Nat. Prod. 65 (2002) 1039-1040
32. Kawai M., Rich D.H., and Walton J.D. The structure and conformation of HC-toxin. Biochem. Biophys. Res. Commun. 111 (1983) 398-403
33. Keller U., and Tudzynski P. Ergot alkaloids. In: Osiewacz H.D. (Ed). The Mycota, Vol. X. "Industrial Applications" (2002), Springer, Berlin 157-181
34. Kim D.H., Kim M., and Kwon H.J. Histone deacetylase in carcinogenesis and its inhibitors as anti-cancer agents. J. Biochem. Mol. Biol. 36 (2003) 110-119
35. Korinek V., Barker N., Morin P.J., van Wichen D., de Weger R., Kinzler K.W., Vogelstein B., and Clevers H. Constitutive transcriptional activation by a beta-catenin-Tcf complex in APC-/- colon carcinoma. Science 275 (1997) 1784-1787
36. Kornberg R.D., and Lorch Y. Twenty-five years of the Nucleosome, fundamental particle of the eukaryote chromosome. Cell 98 (1999) 285-294
37. Liu Y.G., and Whittier R.F. Thermal asymmetric interlaced PCR: automatable amplification and sequencing of insert end fragments from P1 and YAC clones for chromosome walking. Genomics 25 (1995) 674-681
38. Lorenz N., Wilson E.V., Machado C., Schardl C., and Tudzynski P. Comparison of ergot alkaloid biosynthesis gene clusters in Claviceps species indicate loss of late pathway steps in evolution of C. fusiformis. Appl. Environ. Microbiol. 73 (2007) 7185-7191
39. Maeda T., Wurgler-Murphy S.M., and Saito H. A two-component system that regulates an osmosensing MAP kinase cascade in yeast. Nature 369 (1994) 242-245
40. Merrick C.J., and Duraisingh M.T. Heterochromatin-mediated control of virulence gene expression. Mol. Microbiol. 62 (2006) 612-620
41. Mihlan M., Homann V., Liu T.W., and Tudzynski B. AREA directly mediates nitrogen regulation of gibberellin biosynthesis in Gibberella fujikuroi, but its activity is not affected by NMR. Mol. Microbiol. 47 (2003) 975-991
42. Millar C.B., and Grunstein M. Genome-wide patterns of histone modifications in yeast. Nat. Rev. Mol. Cell Biol. 7 (2006) 657-666
43. Motoyama T., Kadokura K., Ohira T., Ichiishi A., Fujimura M., Yamaguchi I., and Kudo T. A two-component histidine kinase of the rice blast fungus is involved in osmotic stress response and fungicide action. Fungal Genet. Biol. 42 (2005) 200-212
44. Nierman W.C., Pain A., Anderson M.J., Wortman J.R., Kim H.S., Arroyo J., Berriman M., Abe K., Archer D.B., Bermejo C., Bennett J., Bowyer P., Chen D., Collins M., Coulsen R., Davies R., Dyer P.S., Farman M., Fedorova N., Fedorova N., Feldblyum T.V., Fischer R., Fosker N., Fraser A., Garcia J.L., Garcia M.J., Goble A., Goldman G.H., Gomi K., Griffith-Jones S., Gwilliam R., Haas B., Haas H., Harris D., Horiuchi H., Huang J., Humphray S., Jimenez J., Keller N., Khouri H., Kitamoto K., Kobayashi T., Konzack S., Kulkarni R., Kumagai T., Lafon A., Latge J.P., Li W., Lord A., Lu C., Majoros W.H., May G.S., Miller B.L., Mohamoud Y., Molina M., Monod M., Mouyna I., Mulligan S., Murphy L., O'Neil S., Paulsen I., Penalva M.A., Pertea M., Price C., Pritchard B.L., Quail M.A., Rabbinowitsch E., Rawlins N., Rajandream M.A., Reichard U., Renauld H., Robson G.D., Rodriguez de Cordoba S., Rodriguez-Pena J.M., Ronning C.M., Rutter S., Salzberg S.L., Sanchez M., Sanchez-Ferrero J.C., Saunders D., Seeger K., Squares R., Squares S., Takeuchi M., Tekaia F., Turner G., Vazquez de Aldana C.R., Weidman J., White O., Woodward J., Yu J.H., Fraser C., Galagan J.E., Asai K., Machida M., Hall N., Barrell B., and Denning D.W. Genomic sequence of the pathogenic and allergenic filamentous fungus Aspergillus fumigatus. Nature 438 (2005) 1151-1156
45. Ochiai N., Tokai T., Nishiuchi T., Takahashi-Ando N., Fujimura M., and Kimura M. Involvement of the osmosensor histidine kinase and osmotic stress-activated protein kinases in the regulation of secondary metabolism in Fusarium graminearum. Biochem. Biophys. Res. Commun. 363 (2007) 639-644
46. O'Donnell K., and Cigelnik E. Two divergent intragenomic rDNA ITS2 types within a monophyletic lineage of the fungus Fusarium are nonorthologous. Mol. Phylogenet. Evol. 7 (1997) 103-116
47. Ortel I., and Keller U. Combinatorial assembly of simple and complex d-lysergic acid alkaloid peptide classes in the ergot fungus Claviceps purpurea. J. Biol. Chem. 284 (2009) 6650-6660
48. Panaccione D.G., Cipoletti J.R., Sedlock A.B., Blemings K.P., Schardl C.L., Machado C., and Seidel G.E. Effects of ergot alkaloids on food preference and satiety in rabbits, as assessed with gene-knock out endophytes in perennial ryegrass (Lolium perenne). J. Agric. Food Chem. 54 (2006) 4582-4587
49. Parkinson J.S., and Kofoid E.C. Communication modules in bacterial signaling proteins. Annu. Rev. Genet. 26 (1992) 71-112
50. Pažoutová S., Kolařík M., Odvody G.N., Frederickson D.E., Olšovská J., and Man P. A species complex including Claviceps fusiformis and Claviceps hirtella. Fungal Diversity 31 (2008) 95-110
51. Pažoutová S., Olšovská J., S ̌ulc M., Chudíc ̌ková M., and Flieger M. Claviceps nigricans and Claviceps grohii: their alkaloids and phylogenetic placement. J. Nat. Prod. 71 (2008) 1085-1188
52. Perrin R.M., Fedorova N.D., Bok J.W., Cramer R.A., Wortman J.R., Kim H.S., Nierman W.C., and Keller N.P. Transcriptional regulation of chemical diversity in Aspergillus fumigatus by LaeA. PLoS Pathog. 3 (2007) 50
53. Razin S.V., Iarovaia O.V., Sjakste N., Sjakste T., Bagdoniene L., Rynditch A.V., Eivazova E.R., Lipinski M., and Vassetzky Y.S. Chromatin domains and regulation of transcription. J. Mol. Biol. 369 (2007) 597-607
54. Rehmeyer C., Li W., Kusaba M., Kim Y.S., Brown D., Staben C., Dean R., and Farman M. Organization of chromosome ends in the rice blast fungus, Magnoporthe oryzae. Nucl. Acids Res. 34 (2006) 4685-4701
55. Riederer B., Han M., and Keller U. d-Lysergyl peptide synthetase from the ergot fungus Claviceps purpurea. J. Biol. Chem. 271 (1996) 27524-27530
56. Rigbers O., and Li S.M. Ergot alkaloid biosynthesis in Aspergillus fumigatus. Overproduction and biochemical characterization of a 4-dimethylallyltryptophan N-methyltransferase. J. Biol. Chem. 283 (2008) 26859-26868
57. Saitou N., and Nei M. The neighbor-joining method: a method for reconstructing phylogenetic trees. Mol. Biol. Evol. 4 (1987) 406-425
58. Schäfer S., Saunders L., Eliseeva E.D., Velena A., Jung M., Schwienhorst A., Strasser A., Dickmanns A., Ficner R., Schlimme S., Sippl W., Verdin E., and Jung M. Phenylalanine-containing hydroxamic acids as selective inhibitors of class IIb histone deacetylases (HDACs). Bioorg. Med. Chem. 16 (2008) 2011-2033
59. Schardl C.L., Panaccione D.G., and Tudzynski P. Ergot alkaloids - biology and molecular biology. Alkaloids Chem. Biol. 63 (2006) 45-86
60. Schardl C.L., Scott B., Florea S., and Zhang D. Epichloë endophytes: Clavicipitaceous symbionts of grasses. In: Deising H. (Ed). The Mykota V: Plant Relationships. second ed. (2009), Springer Verlag, Berlin, Heidelberg 275-306
61. Schönig B., Brown D.W., Oeser B., and Tudzynski B. Cross-species hybridization with Fusarium verticillioides microarrays reveals insights in Fusarium fujikuroi nitrogen regulation and the role of AreA and NMR. Eukaryotic Cell 7 (2008) 1831-1846
62. Schwarz G., and Eich E. Influence of ergot alkaloids on growth of Streptomyces purpurascens and production of its secondary metabolites. Planta Med. 47 (1983) 212-214
63. Segmüller N., Ellendorf U., Tudzynski B., and Tudzynski P. Bcsak1, a stress-activated MAP kinase is involved in vegetative differentiation and pathogenicity in Botrytis cinerea. Eukary. Cell 6 (2007) 211-221
64. Stadler P.A., and Giger R. Ergot alkaloids and their derivatives in medical chemistry and therapy. In: Krosgard-Larson P., Christensen C.H., and Kofod H. (Eds). Natural Products and Drug Development (1984), Munksgaard, Copenhagen 463-485
65. Stock A.M., Wylie D.C., Mottonen J.M., Lupas A.N., Ninfa E.G., Ninfa A.J., Schutt C.E., and Stock J.B. Phosphoproteins involved in bacterial signal transduction. Cold Spring Harb. Symp. Quant. Biol. 53 (1988) 49-57
66. Stock A.M., Robinson V.L., and Goudreau P.N. Two-component signal transduction. Annu. Rev. Biochem. 69 (2000) 183-215
67. Tamura K., Nei M., and Kumar S. Prospects for inferring very large phylogenies by using the neighbor-joining method. Proc. Natl. Acad. Sci. USA 101 (2004) 11030-11035
68. Tamura, K., Dudley, J., Nei, M., Kumar, S., 2007. MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol. Biol. Evol. doi:10.1093/molbev/msm092.
69. Terauchi R., and Kahl G. Rapid isolation of promoter sequences by TAIL-PCR: the 5′-flanking regions of Pal and Pgi genes from yams (Dioscorea). Mol. Gen. Genet. 263 (2000) 554-560
70. Tomsett A.B., Dunn-Coleman N.S., and Garrett R.H. The regulation of nitrate assimilation in Neurospora crassa: the isolation and genetic analysis of nmr-1 mutants. Mol. Gen. Genet. 182 (1981) 229-233
71. Tsai H.F., Wang H., Gebler J.C., Poulter C.D., and Schardl C.L. The Claviceps purpurea gene encoding dimethylallyltryptophan synthase, the committed step for ergot alkaloid biosynthesis. Biochem. Biophys. Res. Commun. 216 (1995) 119-125
72. Tudzynski P., Hölter K., Correia T., Arntz C., Grammel N., and Keller U. Evidence for an ergot alkaloid gene cluster in Claviceps purpurea. Mol. Gen. Genet. 261 (1999) 133-141
73. Valkov, V., 2007. Synthese von Histon-Acetyltransferase-Hemmstoffen und Entwicklung von neuen Testmethoden. Ph.D. Thesis. University of Freiburg.
74. Vendrell M., Angulo E., Casadó V., Lluis C., Franco R., Albericio F., and Royo M. Novel ergopeptides as dual ligands for adenosine and dopamine receptors. J. Med. Chem. 50 (2007) 3062-3069
75. Viaud M., Fillinger S., Liu W., Polepalli J.S., Le Pêcheur P., Kunduru A.R., Leroux P., and Legendre L. A class III histidine kinase acts as a novel virulence factor in Botrytis cinerea. Mol. Plant-Microbe Interact. 19 (2006) 1042-1050
76. Walton J.D. HC-toxin. Phytochemistry 67 (2006) 1406-1413
77. Waltzer L., and Bienz M. Drosophila CBP represses the transcription factor TCF to antagonize Wingless signalling. Nature 395 (1998) 521-525
78. Wiemann P., Willmann A., Straeten M., Kleigrewe K., Beyer M., Humpf H.-U., and Tudzynski B. Biosynthesis of the red pigment bikaverin in Fusarium fujikuroi: genes, their function and regulation. Mol. Microbiol. 72 (2009) 931-946
79. Wynne Aherne G., Rowlands M.G., Stimson L., and Workman P. Assays for the identification and evaluation of histone acetyltransferase inhibitors. Methods 26 (2002) 245-253
80. Yamaguchi F., Ariga T., Yoshimura Y., and Nakazawa H. Antioxidative and anti-glycation activity of garcinol from Garcinia indica fruit rind. J. Agric. Food Chem. 48 (2000) 180-185
81. Yoshida M., Horinouchi S., and Beppu T. Trichostatin A and trapoxin: novel chemical probes for the role of histone acetylation in chromatin structure and function. BioEssays 17 (1995) 423-430