Identification of extracellular siderophores and a related peptide from the endophytic fungus Epichloë festucae in culture and endophyte-infected Lolium perenne

Phytochemistry

Volumn 75, Issue , 2012, Pages 128-139

  Koulman, Albert ^a   Lee, T Verne ^b   Fraser, Karl ^c   Johnson, Linda ^c   Arcus, Vickery ^d   Lott, J Shaun ^b   Rasmussen, Susanne ^c   Lane, Geoffrey ^c  

^a Elsie Widdowson Laboratory   (United Kingdom)

^b UNIVERSITY OF AUCKLAND   (New Zealand)

^c AGRESEARCH GRASSLANDS   (New Zealand)

^d UNIVERSITY OF WAIKATO   (New Zealand)

Author keywords

Clavicipitaceae; Cyclic peptide; Epichlo festucae; High resolution MS n (HRMS n); LC MS n; Lolium perenne; NMR; Poaceae; Siderophore

Indexed keywords

PEPTIDE; SIDEROPHORE;

ARTICLE; CHEMICAL STRUCTURE; CHEMISTRY; EPICHLOE; ISOLATION AND PURIFICATION; LOLIUM; MICROBIOLOGY;

EPICHLOE; LOLIUM; MOLECULAR STRUCTURE; PEPTIDES; SIDEROPHORES;

CLAVICIPITACEAE; EPICHLOE; EPICHLOE FESTUCAE; FUNGI; LOLIUM; LOLIUM PERENNE; POACEAE;

EID: 84856208783     PISSN: 00319422     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.phytochem.2011.11.020     Document Type: Article

References (44)

1. 2O (II) Acta Crystallogr. C 41 1985 341 347
2. Budzikiewicz, H., 2010. Microbial siderophores. Fortschr. Chem. Org. Naturst., vol. 92. Springer-Verlag, Vienna, pp. 1-75.
3. L.P. Bush, F.F. Fannin, M.R. Siegel, D.L. Dahlman, and H.R. Burton Chemistry, occurrence and biological effects of saturated pyrrolizidine alkaloids associated with endophyte-grass interactions Agric. Ecosyst. Environ. 44 1993 81 102
4. L.P. Bush, H.H. Wilkinson, and C.L. Schardl Bioprotective alkaloids of grass-fungal endophyte symbioses Plant Physiol. 114 1997 1 7 (Pubitemid 28110888)
5. K.E. Bushley, D.R. Ripoll, and B.G. Turgeon Module evolution and substrate specificity of fungal nonribosomal peptide synthetases involved in siderophore biosynthesis BMC Evol. Biol. 8 2008 328
6. M. Cao, A. Koulman, L.J. Johnson, and G.A. Lane Advanced data-mining strategies for the analysis of direct-infusion ion trap mass spectrometry data from the association of Lolium perenne with its endophytic fungus Neotyphodium lolii Plant Physiol. 146 2008 1501 1514 (Pubitemid 352844048)
7. K. Clay, and C. Schardl Evolutionary origins and ecological consequences of endophyte symbiosis with grasses Am. Nat. 160 Suppl. 4 2002 S99 S127
8. A. Dellagi, D. Segond, M. Rigault, M. Fagard, C. Simon, P. Saindrenan, and D. Expert Microbial siderophores exert a subtle role in Arabidopsis during infection by manipulating the immune response and the iron status Plant Physiol. 150 2009 1687 1696
9. H. Diekmann, and H. Zahner Constitution and catabolism of fusigen to delta-2-anhydromevalonic acid lactone Eur. J. Biochem. 3 1967 213 218
10. M. Eisendle, H. Oberegger, I. Zadra, and H. Haas The siderophore system is essential for viability of Aspergillus nidulans: functional analysis of two genes encoding l-ornithine N 5-monooxygenase (sidA) and a non-ribosomal peptide synthetase (sidC) Mol. Microbiol. 49 2003 359 375 (Pubitemid 36851193)
11. S.A. Essén, D. Bylund, S.J.M. Holmström, M. Moberg, and U.S. Lundström Quantification of hydroxamate siderophores in soil solutions of podzolic soil profiles in Sweden BioMetals 19 2006 269 282 (Pubitemid 43946167)
12. D.J. Fleetwood, B. Scott, G.A. Lane, A. Tanaka, and R.D. Johnson A complex ergovaline gene gluster in Epichloë endophytes of grasses Appl. Environ. Microbiol. 73 2007 2571 2579 (Pubitemid 46668750)
13. R.T. Gallagher, A.D. Hawkes, P.S. Steyn, and R. Vleggaar Tremorgenic neurotoxins from perennial ryegrass causing ryegrass staggers disorder of livestock: structure elucidation of lolitrem B J. Chem. Soc. Chem. Commun. 1984 614 616
14. M.A.F. Jalal, and D. van der Helm Isolation and spectroscopic identification of fungal siderophores G. Winkelmann, CRC Handbook of Microbial Iron Chelates 1991 CRC Press Boca Raton 235 269
15. L. Johnson Iron and siderophores in fungal-host interactions Mycol. Res. 112 2008 170 183
16. L. Johnson, M. Steringa, A. Koulman, M. Christensen, R.D. Johnson, C.R. Voisey, G. Bryan, I. Lamont, and S. Rasmussen Biosynthesis of an extracellular siderophore is essential for maintenance of mutualistic endophyte-grass symbioses A.J. Popay, E.R. Thom, 6th International Symposium on Fungal Endophytes of Grasses 2007 New Zealand Grasslands Association Dunedin, New Zealand 177 179
17. R. Johnson, C. Voisey, L. Johnson, J. Pratt, D. Fleetwood, A. Khan, and G. Bryan Distribution of NRPS gene families within the Neotyphodium/ Epichloë complex Fungal Genet. Biol. 44 2007 1180 1190 (Pubitemid 47532772)
18. A. Koulman, G.A. Lane, M.J. Christensen, K. Fraser, and B.A. Tapper Peramine and other fungal alkaloids are exuded in the guttation fluid of endophyte-infected grasses Phytochemistry 68 2007 355 360 (Pubitemid 46127568)
19. A. Koulman, B.A. Tapper, K. Fraser, M. Cao, G.A. Lane, and S. Rasmussen High throughput direct infusion ion trap mass spectrometry: a new method for metabolomics Rapid Commun. Mass Spectrom. 21 2007 421 428 (Pubitemid 46212555)
20. T.V. Lee, L.J. Johnson, R.D. Johnson, A. Koulman, G.A. Lane, J.S. Lott, and V.L. Arcus Structure of a eukaryotic nonribosomal peptide synthetase adenylation domain that activates a large hydroxamate amino acid in siderophore biosynthesis J. Biol. Chem. 285 2010 2415 2427
21. P.C. Lyons, R.D. Plattner, and C.W. Bacon Occurrence of peptide and clavine ergot alkaloids in tall fescue grass Science 232 1986 487 489 (Pubitemid 16052358)
22. P.G. Mantle, and L.J. Nisbet Differentiation of Claviceps purpurea in axenic culture J. Gen. Microbiol. 93 1976 321 334
23. E. Mawji, M. Gledhill, P.J. Worsfold, and E.P. Achterberg Collision-induced dissociation of three groups of hydroxamate siderophores: ferrioxamines, ferrichromes and coprogens/fusigens Rapid Commun. Mass Spectrom. 22 2008 2195 2202 (Pubitemid 351998626)
24. P. McCormack, P.J. Worsfold, and M. Gledhill Separation and detection of siderophores produced by marine bacterioplankton using high-performance liquid chromatography with electrospray ionization mass spectrometry Anal. Chem. (Washington, DC, US) 75 2003 2647 2652 (Pubitemid 36667109)
25. D.G. Panaccione, R.D. Johnson, J.H. Wang, C.A. Young, P. Damrongkool, B. Scott, and C.L. Schardl Elimination of ergovaline from a grass-Neotyphodium endophyte symbiosis by genetic modification of the endophyte Proc. Natl. Acad. Sci. USA 98 2001 12820 12825 (Pubitemid 33020028)
26. A.J. Popay, and S.A. Bonos Biotic responses in endophytic grasses C.A. Roberts, C.P. West, D.E. Spiers, Neotyphodium in Cool Season Grasses 2005 Blackwell Publishing Ames, IA 163 185
27. S. Rasmussen, A. Parsons, K. Fraser, H. Xue, and J. Newman Metabolic profiles of Lolium perenne are differentially affected by nitrogen supply, carbohydrate content, and fungal endophyte infection Plant Physiol. 146 2008 1440 1453 (Pubitemid 352844150)
28. R. Rellan-Alvarez, J. Giner-Martinez-Sierra, J. Orduna, I. Orera, J.A. Rodriguez-Castrillon, J.I. Garcia-Alonso, J. Abadia, and A. Alvarez-Fernandez Identification of a tri-iron(III), tri-citrate complex in the xylem sap of iron-deficient tomato resupplied with iron: new insights into plant iron long-distance transport Plant Cell Physiol. 51 2010 91 102
29. J. Renshaw, G. Robson, A. Trinci, M. Wiebe, F. Livens, D. Collison, and R. Taylor Fungal siderophores: structures, functions and applications Mycol. Res. 106 2002 1123 1142 (Pubitemid 36016730)
30. D.D. Rowan, and D.L. Gaynor Isolation of feeding deterrents against Argentine stem weevil from ryegrass infected with the endophyte Acremonium loliae J. Chem. Ecol. 12 1986 647 658
31. C.L. Schardl, R.B. Grossman, P. Nagabhyru, J.R. Faulkner, and U.P. Mallik Loline alkaloids: currencies of mutualism Phytochemistry 68 2007 980 996 (Pubitemid 46415759)
32. T. Schwecke, K. Göttling, P. Durek, I. Dueñas, N.F. Käufer, S. Zock-Emmenthal, E. Staub, T. Neuhof, R. Dieckmann, and H. Von Döhren Nonribosomal peptide synthesis in Schizosoccharomyces pombe and the architectures of ferrichrome-type siderophore synthetases in fungi ChemBioChem 7 2006 612 622
33. G.J. Sharman, D.H. Williams, D.F. Ewing, and C. Ratledge Isolation, purification and structure of exochelin MS, the extracellular siderophore from Mycobacterium smegmatis Biochem. J. 305 1995 187 196
34. M.R. Siegel, and L.P. Bush Defensive chemicals in grass fungal endophyte associations J.T. Romeo, J.A. Saunders, P. Barbosa, Phytochemical Diversity and Redundancy in Ecological Interactions 1996 Plenum New York 81 119
35. M.R. Siegel, G.C.M. Latch, L.P. Bush, F.F. Fannin, D.D. Rowan, B.A. Tapper, C.W. Bacon, and M.C. Johnson Fungal endophyte-infected grasses: alkaloid accumulation and aphid response J. Chem. Ecol. 16 1990 3301 3315
36. A.V. Simionato, G.D. de Souza, E. Rodrigues-Filho, J. Glick, P. Vouros, and E. Carrilho Tandem mass spectrometry of coprogen and deferoxamine hydroxamic siderophores Rapid Commun. Mass Spectrom. 20 2006 193 199 (Pubitemid 43121620)
37. M.J. Spiering, C.D. Moon, H.H. Wilkinson, and C.L. Schardl Gene clusters for insecticidal loline alkaloids in the grass-endophytic fungus Neotyphodium uncinatum Genetics 169 2005 1403 1414 (Pubitemid 40547452)
38. M.J. Spiering, J.R. Faulkner, D.X. Zhang, C. Machado, R.B. Grossman, and C.L. Schardl Role of the LolP cytochrome P450 monooxygenase in loline alkaloid biosynthesis Fungal Genet. Biol. 45 2008 1307 1314
39. A. Tanaka, B.A. Tapper, A. Popay, E.J. Parker, and B. Scott A symbiosis expressed non-ribosomal peptide synthetase from a mutualistic fungal endophyte of perennial ryegrass confers protection to the symbiotum from insect herbivory Mol. Microbiol. 57 2005 1036 1050 (Pubitemid 41139864)
40. D. van der Helm, and G. Winkelmann Hydroxamates and polycarboxylates as iron transport agents (siderophores) in fungi G.W.D. Winge, Metal Ions in Fungi 1994 Marcel Dekker New York 39 98
41. D. van der Helm, M.A.F. Jalal, and M.B. Hossain The crystal structures, conformations and configurations of siderophores G. Winkelmann, D. van der Helm, J.B. Neilands, Iron Transport in Microbes, Plants, and Animals 1987 VCH Weinheim, Federal Republic of Germany New York, NY
42. C.A. Young, M.K. Bryant, M.J. Christensen, B.A. Tapper, G.T. Bryan, and B. Scott Molecular cloning and genetic analysis of a symbiosis-expressed gene cluster for lolitrem biosynthesis from a mutualistic endophyte of perennial ryegrass Mol. Genet. Genomics 274 2005 13 29 (Pubitemid 41396980)
43. C.A. Young, S. Felitti, K. Shields, G. Spangenberg, R.D. Johnson, G.T. Bryan, S. Saikia, and B. Scott A complex gene cluster for indolediterpene biosynthesis in the grass endophyte Neotyphodium lolii Fungal Genet. Biol. 43 2006 679 693 (Pubitemid 44292548)
44. W.M. Yuan, G.D. Gentil, A.D. Budde, and S.A. Leong Characterization of the Ustilago maydis sid2 gene, encoding a multidomain peptide synthetase in the ferrichrome biosynthetic gene cluster J. Bacteriol. 183 2001 4040 4051 (Pubitemid 32565485)