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Structural and functional characterization of TRI3 trichothecene 15-O-acetyltransferase from Fusarium sporotrichioides

  1. Graeme S. Garvey1,
  2. Susan P. McCormick2,
  3. Nancy J. Alexander2,
  4. Ivan Rayment1,*

Article first published online: 16 MAR 2009

DOI: 10.1002/pro.80

Issue

Protein Science

Protein Science

Volume 18, Issue 4, pages 747–761, April 2009

Additional Information

How to Cite

Garvey, G. S., McCormick, S. P., Alexander, N. J. and Rayment, I. (2009), Structural and functional characterization of TRI3 trichothecene 15-O-acetyltransferase from Fusarium sporotrichioides. Protein Science, 18: 747–761. doi: 10.1002/pro.80

Author Information

  1. 1

    Department of Biochemistry, University of Wisconsin, Madison, Wisconsin 53706

  2. 2

    Mycotoxin Research Unit, USDA/ARS, National Center for Agricultural Utilization Research, Peoria, Illinois 61604

*Department of Biochemistry, 433 Babcock Dr., Madison, WI 53706

Publication History

  1. Issue published online: 25 MAR 2009
  2. Article first published online: 16 MAR 2009
  3. Accepted manuscript online: 16 MAR 2009 12:00AM EST
  4. Manuscript Accepted: 15 JAN 2009
  5. Manuscript Revised: 6 JAN 2009
  6. Manuscript Received: 15 OCT 2008

Funded by

  • NIH. Grant Number: AR35186
  • U.S. Department of Agriculture. Grant Number: 59-0790-6-066
  • U.S. Department of Agriculture NP 108 Food Safety
  • U.S. Department of Energy, Office of Energy Research. Grant Number: W-31-109-ENG-38

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References

  • 1
    Stack RW ( 1999) Return of an old problem: Fusarium head blight of small grains. Available at: http://www.apsnetorg/online/feature/FHB/Top.html (accessed on February 2, 2008).
  • 2
    Nganje WE, Bangsund DA, Leistritz FL, Wilson WW, Tiapo NM ( 2004) Regional economic impacts of Fusarium head blight in wheat and barley. Rev Agric Econ 26: 332–347.
    Direct Link:
  • 3
    Windels CE ( 2000) Economic and social impacts of Fusarium head blight: changing farms and rural communities in the Northern Great Plains. Phytopathology 90: 17–21.
  • 4
    Bennett JW, Klich M ( 2003) Mycotoxins. Clin Microbiol Rev 16: 497–516.
  • 5
    Anderson DW, Black RM, Lee CG, Pottage C, Rickard RL, Sandford MS, Webber TD, Williams NE ( 1989) Structure-activity studies of trichothecenes: cytotoxicity of analogues and reaction products derived from T-2 toxin and neosolaniol. J Med Chem 32: 555–562.
  • 6
    Alexander NJ, McCormick SP, Ziegenhorn SL ( 1999) Phytotoxicity of selected trichothecenes using Chlamydomonas reinhardtii as a model system. Natural Toxins 7: 265–269.
    Direct Link:
  • 7
    Desjardins AE, McCormick SP, Appell M ( 2007) Structure-activity relationships of trichothecene toxins in an Arabidopsis thaliana leaf assay. J Agric Food Chem 55: 6487–6492.
  • 8
    Zamir LO, Devor KA, Sauriol F ( 1991) Biosynthesis of the trichothecene 3-acetyldeoxynivalenol. Identification of the oxygenation steps after isotrichodermin. J Biol Chem 266: 14992–15000.
  • 9
    McCormick SP, Hohn TM, Desjardins AE ( 1996) Isolation and characterization of Tri3, a gene encoding 15-O-acetyltransferase from Fusarium sporotrichioides. Appl Environ Microbiol 62: 353–359.
  • 10
    Kimura M, Tokai T, Takahashi-Ando N, Ohsato S, Fujimura M ( 2007) Molecular and genetic studies of fusarium trichothecene biosynthesis: pathways, genes, and evolution. Biosci Biotechnol Biochem 71: 2105–2123.
  • 11
    Tokai T, Koshino H, Takahashi-Ando N, Sato M, Fujimura M, Kimura M ( 2007) Fusarium Tri4 encodes a key multifunctional cytochrome P450 monooxygenase for four consecutive oxygenation steps in trichothecene biosynthesis. Biochem Biophys Res Commun 353: 412–417.
  • 12
    Hohn TM, Beremand PD ( 1989) Isolation and nucleotide sequence of a sesquiterpene cyclase gene from the trichothecene-producing fungus Fusarium sporotrichioides. Gene 79: 131–138.
  • 13
    McCormick SP, Alexander NJ, Proctor RH ( 2006) Fusarium Tri4 encodes a multifunctional oxygenase required for trichothecene biosynthesis. Can J Microbiol 52: 636–642.
  • 14
    Kimura M, Kaneko I, Komiyama M, Takatsuki A, Koshino H, Yoneyama K, Yamaguchi I ( 1998) Trichothecene 3-O-acetyltransferase protects both the producing organism and transformed yeast from related mycotoxins. Cloning and characterization of Tri101. J Biol Chem 273: 1654–1661.
  • 15
    Alexander NJ, Hohn TM, McCormick SP ( 1998) The TRI11 gene of Fusarium sporotrichioides encodes a cytochrome P-450 monooxygenase required for C-15 hydroxylation in trichothecene biosynthesis. Appl Environ Microbiol 64: 221–225.
  • 16
    Brown DW, McCormick SP, Alexander NJ, Proctor RH, Desjardins AE ( 2001) A genetic and biochemical approach to study trichothecene diversity in Fusarium sporotrichioides and Fusarium graminearum. Fungal Genet Biol 32: 121–133.
  • 17
    Brown DW, McCormick SP, Alexander NJ, Proctor RH, Desjardins AE ( 2002) Inactivation of a cytochrome P-450 is a determinant of trichothecene diversity in Fusarium species. Fungal Genet Biol 36: 224–233.
  • 18
    Lee T, Han YK, Kim KH, Yun SH, Lee YW ( 2002) Tri13 and Tri7 determine deoxynivalenol- and nivalenol-producing chemotypes of Gibberella zeae. Appl Environ Microbiol 68: 2148–2154.
  • 19
    Brown DW, Proctor RH, Dyer RB, Plattner RD ( 2003) Characterization of a fusarium 2-gene cluster involved in trichothecene C-8 modification. J Agric Food Chem 51: 7936–7944.
  • 20
    Meek IB, Peplow AW, Ake C,Jr,Phillips TD, Beremand MN ( 2003) Tri1 encodes the cytochrome P450 monooxygenase for C-8 hydroxylation during trichothecene biosynthesis in Fusarium sporotrichioides and resides upstream of another new Tri gene. Appl Environ Microbiol 69: 1607–1613.
  • 21
    McCormick SP, Harris LJ, Alexander NJ, Ouellet T, Saparno A, Allard S, Desjardins AE ( 2004) Tri1 in Fusarium graminearum encodes a P450 oxygenase. Appl Environ Microbiol 70: 2044–2051.
  • 22
    Peplow AW, Meek IB, Wiles MC, Phillips TD, Beremand MN ( 2003) Tri16 is required for esterification of position C-8 during trichothecene mycotoxin production by Fusarium sporotrichioides. Appl Environ Microbiol 69: 5935–5940.
  • 23
    McCormick SP, Alexander NJ ( 2002) Fusarium Tri8 encodes a trichothecene C-3 esterase. Appl Environ Microbiol 68: 2959–2964.
  • 24
    Ueno Y, Sawano M, Ishii K ( 1975) Production of trichothecene mycotoxins by Fusarium species in shake culture. Appl Microbiol 30: 4–9.
  • 25
    Miller JD, Greenhalgh R, Wang Y, Lu M ( 1991) Trichothecene chemotypes of three Fusarium species. Mycologia 83: 121–130.
  • 26
    O'Donnell K, Kistler HC, Tacke BK, Casper HH ( 2000) Gene genealogies reveal global phylogeographic structure and reproductive isolation among lineages of Fusarium graminearum, the fungus causing wheat scab. Proc Natl Acad Sci USA 97: 7905–7910.
  • 27
    Ward TJ, Bielawski JP, Kistler HC, Sullivan E, O'Donnell K ( 2002) Ancestral polymorphism and adaptive evolution in the trichothecene mycotoxin gene cluster of phytopathogenic Fusarium. Proc Natl Acad Sci USA 99: 9278–9283.
  • 28
    Goswami RS, Kistler HC ( 2005) Pathogenicity and in planta mycotoxin accumulation among members of the Fusarium graminearum species complex on wheat and rice. Phytopathology 95: 1397–1404.
  • 29
    Starkey DE, Ward TJ, Aoki T, Gale LR, Kistler HC, Geiser DM, Suga H, Toth B, Varga J, O'Donnell K ( 2007) Global molecular surveillance reveals novel Fusarium head blight species and trichothecene toxin diversity. Fungal Genet Biol 44: 1191–1204.
  • 30
    Ward TJ, Clear RM, Rooney AP, O'Donnell K, Gaba D, Patrick S, Starkey DE, Gilbert J, Geiser DM, Nowicki TW ( 2008) An adaptive evolutionary shift in Fusarium head blight pathogen populations is driving the rapid spread of more toxigenic Fusarium graminearum in North America. Fungal Genet Biol 45: 473–484.
  • 31
    Desjardins AE ( 2008) Natural product chemistry meets genetics: when is a genotype a chemotype? J Agric Food Chem 56: 7587–7592.
  • 32
    Kimura M, Tokai T, O'Donnell K, Ward TJ, Fujimura M, Hamamoto H, Shibata T, Yamaguchi I ( 2003) The trichothecene biosynthesis gene cluster of Fusarium graminearum F15 contains a limited number of essential pathway genes and expressed non-essential genes. FEBS Lett 539: 105–110.
  • 33
    Garvey GS, McCormick SP, Rayment I ( 2008) Structural and functional characterization of the TRI101 trichothecene 3-O-acetyltransferase from Fusarium sporotrichioides and Fusarium graminearum: kinetic insights to combating Fusarium head blight. J Biol Chem 283: 1660–1669.
  • 34
    Krissinel E, Henrick K ( 2004) Secondary-structure matching (SSM), a new tool for fast protein structure alignment in three dimensions. Acta Crystallogr Sect D 60(12, Part 1): 2256–2268.
    Direct Link:
  • 35
    Buglino J, Onwueme KC, Ferreras JA, Quadri LE, Lima CD ( 2004) Crystal structure of PapA5, a phthiocerol dimycocerosyl transferase from Mycobacterium tuberculosis. J Biol Chem 279: 30634–30642.
  • 36
    Onwueme KC, Ferreras JA, Buglino J, Lima CD, Quadri LE ( 2004) Mycobacterial polyketide-associated proteins are acyltransferases: proof of principle with Mycobacterium tuberculosis PapA5. Proc Natl Acad Sci USA 101: 4608–4613.
  • 37
    Ma X, Koepke J, Panjikar S, Fritzsch G, Stockigt J ( 2005) Crystal structure of vinorine synthase, the first representative of the BAHD superfamily. J Biol Chem 280: 13576–13583.
  • 38
    D'Auria JC ( 2006) Acyltransferases in plants: a good time to be BAHD. Curr Opin Plant Biol 9: 331–340.
  • 39
    Bayer A, Ma X, Stockigt J ( 2004) Acetyltransfer in natural product biosynthesis—functional cloning and molecular analysis of vinorine synthase. Bioorg Med Chem 12: 2787–2795.
  • 40
    Poirot O, O'Toole E, Notredame C ( 2003) Tcoffee@igs: a web server for computing, evaluating and combining multiple sequence alignments. Nucleic Acids Res 31: 3503–3506.
  • 41
    Ho SN, Hunt HD, Horton RM, Pullen JK, Pease LR ( 1989) Site-directed mutagenesis by overlap extension using the polymerase chain reaction. Gene 77: 51–59.
  • 42
    Rocco CJ, Dennison KL, Klenchin VA, Rayment I, Escalante-Semerena JC ( 2008) Construction and use of new cloning vectors for the rapid isolation of recombinant proteins from Escherichia coli. Plasmid 59: 231–237.
  • 43
    Laemmli UK ( 1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227: 680–685.
  • 44
    Shih YP, Wu HC, Hu SM, Wang TF, Wang AH ( 2005) Self-cleavage of fusion protein in vivo using TEV protease to yield native protein. Protein Sci 14: 936–941.
    Direct Link:
  • 45
    Otwinowski Z, Minor W ( 1997) Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol 276: 307–326.
  • 46
    Terwilliger TC, Berendzen J ( 1999) Automated MAD and MIR structure solution. Acta Crystallogr D 55 (Part 4): 849–861.
    Direct Link:
  • 47
    Terwilliger TC ( 2000) Maximum-likelihood density modification. Acta Crystallogr D Biol Crystallogr 56 (Part 8): 965–972.
    Direct Link:
  • 48
    Perrakis A, Harkiolaki M, Wilson KS, Lamzin VS ( 2001) ARP/wARP and molecular replacement. Acta Crystallogr D Biol Crystallogr 57 (Part 10): 1445–1450.
    Direct Link:
  • 49
    Emsley P, Cowtan K ( 2004) Coot: model-building tools for molecular graphics. Acta Crystallogr D Biol Crystallogr 60(12, Part 1): 2126–2132a.
    Direct Link:
  • 50
    Murshudov GN, Vagin AA, Dodson EJ ( 1997) Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr D Biol Crystallogr 53 (Part 3): 240–255.
    Direct Link:
  • 51
    Laskowski RA, MacArthur MW, Moss DS, Thornton JM ( 1993) PROCHECK: a program to check the stereochemical quality of protein structures. J Appl Crystallogr 26: 283–291.
    Direct Link:
  • 52
    Vagin A, Teplyakov A ( 1997) MOLREP: an automated program for molecular replacement. J Appl Crystallogr 30: 1022–1025.
    Direct Link:
  • 53
    Ellman GL ( 1959) Tissue sulphydryl groups. Arch Biochem Biophys 82: 70.
  • 54
    Proctor RH, Hohn TM, McCormick SP ( 1995) Reduced virulence of Gibberella zeae caused by disruption of a trichothecene toxin biosynthetic gene. Mol Plant Microbe Interact 8: 593–601.
  • 55
    Sambrook J, Fritsch EF, Maniatis T ( 1989) Molecular cloning: a laboratory manual. New York: Cold Spring Harbor Laboratory, Cold Spring Harbor.
  • 56
    Miller JD, Blackwell BA ( 1986) Biosynthesis of 3-Acetyldeoxynivalenol and other metabolites by Fusarium-culmorum Hlx 1503 in a stirred jar fermenter. Can J Bot Rev Can Bot 64: 1–5.
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