1jfg Citations

Structure of trichodiene synthase from Fusarium sporotrichioides provides mechanistic inferences on the terpene cyclization cascade.

Proc. Natl. Acad. Sci. U.S.A. 98 13543-8 (2001)
Cited: 95 times
EuropePMC logo PMID: 11698643

Abstract

The x-ray crystal structure of recombinant trichodiene synthase from Fusarium sporotrichioides has been determined to 2.5-A resolution, both unliganded and complexed with inorganic pyrophosphate. This reaction product coordinates to three Mg(2+) ions near the mouth of the active site cleft. A comparison of the liganded and unliganded structures reveals a ligand-induced conformational change that closes the mouth of the active site cleft. Binding of the substrate farnesyl diphosphate similarly may trigger this conformational change, which would facilitate catalysis by protecting reactive carbocationic intermediates in the cyclization cascade. Trichodiene synthase also shares significant structural similarity with other sesquiterpene synthases despite a lack of significant sequence identity. This similarity indicates divergence from a common ancestor early in the evolution of terpene biosynthesis.

Articles - 1jfg mentioned but not cited (1)

  1. Computational design and selections for an engineered, thermostable terpene synthase. Diaz JE, Lin CS, Kunishiro K, Feld BK, Avrantinis SK, Bronson J, Greaves J, Saven JG, Weiss GA. Protein Sci. 20 1597-1606 (2011)


Reviews citing this publication (19)

  1. Importance of Inherent Substrate Reactivity in Enzyme-Promoted Carbocation Cyclization/Rearrangements. Tantillo DJ. Angew. Chem. Int. Ed. Engl. 56 10040-10045 (2017)
  2. Structural and Chemical Biology of Terpenoid Cyclases. Christianson DW. Chem. Rev. 117 11570-11648 (2017)
  3. Bacterial terpene cyclases. Dickschat JS. Nat Prod Rep 33 87-110 (2016)
  4. Terpenoid biosynthesis off the beaten track: unconventional cyclases and their impact on biomimetic synthesis. Baunach M, Franke J, Hertweck C. Angew. Chem. Int. Ed. Engl. 54 2604-2626 (2015)
  5. Cellular compartmentalization of secondary metabolism. Kistler HC, Broz K. Front Microbiol 6 68 (2015)
  6. Traversing the fungal terpenome. Quin MB, Flynn CM, Schmidt-Dannert C. Nat Prod Rep 31 1449-1473 (2014)
  7. Sesquiterpene synthases: passive catalysts or active players? Miller DJ, Allemann RK. Nat Prod Rep 29 60-71 (2012)
  8. Terpenoid synthase structures: a so far incomplete view of complex catalysis. Gao Y, Honzatko RB, Peters RJ. Nat Prod Rep 29 1153-1175 (2012)
  9. Electrophilic and nucleophilic enzymatic cascade reactions in biosynthesis. Ueberbacher BT, Hall M, Faber K. Nat Prod Rep 29 337-350 (2012)
  10. Biosynthesis via carbocations: theoretical studies on terpene formation. Tantillo DJ. Nat Prod Rep 28 1035-1053 (2011)
  11. Monoterpene and sesquiterpene synthases and the origin of terpene skeletal diversity in plants. Degenhardt J, Köllner TG, Gershenzon J. Phytochemistry 70 1621-1637 (2009)
  12. Unearthing the roots of the terpenome. Christianson DW. Curr Opin Chem Biol 12 141-150 (2008)
  13. Brushes with sage. Cane DE. Arch. Biochem. Biophys. 448 117-122 (2006)
  14. Elucidation of the biosynthetic origin of the anti-inflammatory pseudopterosins. Kerr RG, Kohl AC, Ferns TA. J. Ind. Microbiol. Biotechnol. 33 532-538 (2006)
  15. Biogenesis, molecular regulation and function of plant isoprenoids. Bouvier F, Rahier A, Camara B. Prog. Lipid Res. 44 357-429 (2005)
  16. Fungal secondary metabolism - from biochemistry to genomics. Keller NP, Turner G, Bennett JW. Nat. Rev. Microbiol. 3 937-947 (2005)
  17. Attracting friends to feast on foes: engineering terpene emission to make crop plants more attractive to herbivore enemies. Degenhardt J, Gershenzon J, Baldwin IT, Kessler A. Curr. Opin. Biotechnol. 14 169-176 (2003)
  18. Structure, mechanism and function of prenyltransferases. Liang PH, Ko TP, Wang AH. Eur. J. Biochem. 269 3339-3354 (2002)
  19. Molecular scaffolds for chemical wizardry: learning nature's rules for terpene cyclases. Greenhagen B, Chappell J. Proc. Natl. Acad. Sci. U.S.A. 98 13479-13481 (2001)

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  1. Designed divergent evolution of enzyme function. Yoshikuni Y, Ferrin TE, Keasling JD. Nature 440 1078-1082 (2006)
  2. Bornyl diphosphate synthase: structure and strategy for carbocation manipulation by a terpenoid cyclase. Whittington DA, Wise ML, Urbansky M, Coates RM, Croteau RB, Christianson DW. Proc. Natl. Acad. Sci. U.S.A. 99 15375-15380 (2002)
  3. Identifying and manipulating structural determinates linking catalytic specificities in terpene synthases. Greenhagen BT, O'Maille PE, Noel JP, Chappell J. Proc. Natl. Acad. Sci. U.S.A. 103 9826-9831 (2006)
  4. Identification and functional analysis of genes controlling biosynthesis of 2-methylisoborneol. Komatsu M, Tsuda M, Omura S, Oikawa H, Ikeda H. Proc. Natl. Acad. Sci. U.S.A. 105 7422-7427 (2008)
  5. X-ray crystal structure of aristolochene synthase from Aspergillus terreus and evolution of templates for the cyclization of farnesyl diphosphate. Shishova EY, Di Costanzo L, Cane DE, Christianson DW. Biochemistry 46 1941-1951 (2007)
  6. Taxadiene synthase structure and evolution of modular architecture in terpene biosynthesis. Köksal M, Jin Y, Coates RM, Croteau R, Christianson DW. Nature 469 116-120 (2011)
  7. Expression and mechanistic analysis of a germacradienol synthase from Streptomyces coelicolor implicated in geosmin biosynthesis. Cane DE, Watt RM. Proc. Natl. Acad. Sci. U.S.A. 100 1547-1551 (2003)
  8. Identification of sesquiterpene synthases from Nostoc punctiforme PCC 73102 and Nostoc sp. strain PCC 7120. Agger SA, Lopez-Gallego F, Hoye TR, Schmidt-Dannert C. J. Bacteriol. 190 6084-6096 (2008)
  9. Conversion of squalene to the pentacarbocyclic hopene. Reinert DJ, Balliano G, Schulz GE. Chem. Biol. 11 121-126 (2004)
  10. Novel genes of Fusarium graminearum that negatively regulate deoxynivalenol production and virulence. Gardiner DM, Kazan K, Manners JM. Mol. Plant Microbe Interact. 22 1588-1600 (2009)
  11. Structure of epi-isozizaene synthase from Streptomyces coelicolor A3(2), a platform for new terpenoid cyclization templates. Aaron JA, Lin X, Cane DE, Christianson DW. Biochemistry 49 1787-1797 (2010)
  12. Crystal structure of (+)-delta-cadinene synthase from Gossypium arboreum and evolutionary divergence of metal binding motifs for catalysis. Gennadios HA, Gonzalez V, Di Costanzo L, Li A, Yu F, Miller DJ, Allemann RK, Christianson DW. Biochemistry 48 6175-6183 (2009)
  13. Monoterpene biosynthesis in lemon (Citrus limon). cDNA isolation and functional analysis of four monoterpene synthases. Lücker J, El Tamer MK, Schwab W, Verstappen FW, van der Plas LH, Bouwmeester HJ, Verhoeven HA. Eur. J. Biochem. 269 3160-3171 (2002)
  14. Diversity of sesquiterpene synthases in the basidiomycete Coprinus cinereus. Agger S, Lopez-Gallego F, Schmidt-Dannert C. Mol. Microbiol. 72 1181-1195 (2009)
  15. Expression, purification, and characterization of recombinant amorpha-4,11-diene synthase from Artemisia annua L. Picaud S, Olofsson L, Brodelius M, Brodelius PE. Arch. Biochem. Biophys. 436 215-226 (2005)
  16. Crystal structure of albaflavenone monooxygenase containing a moonlighting terpene synthase active site. Zhao B, Lei L, Vassylyev DG, Lin X, Cane DE, Kelly SL, Yuan H, Lamb DC, Waterman MR. J. Biol. Chem. 284 36711-36719 (2009)
  17. Trinuclear Metal Clusters in Catalysis by Terpenoid Synthases. Aaron JA, Christianson DW. Pure Appl. Chem. 82 1585-1597 (2010)
  18. Engineering cotton (+)-delta-cadinene synthase to an altered function: germacrene D-4-ol synthase. Yoshikuni Y, Martin VJ, Ferrin TE, Keasling JD. Chem. Biol. 13 91-98 (2006)
  19. X-ray crystallographic studies of substrate binding to aristolochene synthase suggest a metal ion binding sequence for catalysis. Shishova EY, Yu F, Miller DJ, Faraldos JA, Zhao Y, Coates RM, Allemann RK, Cane DE, Christianson DW. J. Biol. Chem. 283 15431-15439 (2008)
  20. Enantiospecific (+)- and (-)-germacrene D synthases, cloned from goldenrod, reveal a functionally active variant of the universal isoprenoid-biosynthesis aspartate-rich motif. Prosser I, Altug IG, Phillips AL, König WA, Bouwmeester HJ, Beale MH. Arch. Biochem. Biophys. 432 136-144 (2004)
  21. Characterization of delta-guaiene synthases from cultured cells of Aquilaria, responsible for the formation of the sesquiterpenes in agarwood. Kumeta Y, Ito M. Plant Physiol. 154 1998-2007 (2010)
  22. Structural and mechanistic analysis of trichodiene synthase using site-directed mutagenesis: probing the catalytic function of tyrosine-295 and the asparagine-225/serine-229/glutamate-233-Mg2+B motif. Vedula LS, Jiang J, Zakharian T, Cane DE, Christianson DW. Arch. Biochem. Biophys. 469 184-194 (2008)
  23. Insights into diterpene cyclization from structure of bifunctional abietadiene synthase from Abies grandis. Zhou K, Gao Y, Hoy JA, Mann FM, Honzatko RB, Peters RJ. J. Biol. Chem. 287 6840-6850 (2012)
  24. Sesquiterpene synthases Cop4 and Cop6 from Coprinus cinereus: catalytic promiscuity and cyclization of farnesyl pyrophosphate geometric isomers. Lopez-Gallego F, Agger SA, Abate-Pella D, Distefano MD, Schmidt-Dannert C. Chembiochem 11 1093-1106 (2010)
  25. Induced-fit mechanism in class I terpene cyclases. Baer P, Rabe P, Fischer K, Citron CA, Klapschinski TA, Groll M, Dickschat JS. Angew. Chem. Int. Ed. Engl. 53 7652-7656 (2014)
  26. Exploring biosynthetic diversity with trichodiene synthase. Vedula LS, Zhao Y, Coates RM, Koyama T, Cane DE, Christianson DW. Arch. Biochem. Biophys. 466 260-266 (2007)
  27. Structure of a three-domain sesquiterpene synthase: a prospective target for advanced biofuels production. McAndrew RP, Peralta-Yahya PP, DeGiovanni A, Pereira JH, Hadi MZ, Keasling JD, Adams PD. Structure 19 1876-1884 (2011)
  28. Role of arginine-304 in the diphosphate-triggered active site closure mechanism of trichodiene synthase. Vedula LS, Cane DE, Christianson DW. Biochemistry 44 12719-12727 (2005)
  29. Mutational analysis of a monoterpene synthase reaction: altered catalysis through directed mutagenesis of (-)-pinene synthase from Abies grandis. Hyatt DC, Croteau R. Arch. Biochem. Biophys. 439 222-233 (2005)
  30. Nonseed plant Selaginella moellendorffi [corrected] has both seed plant and microbial types of terpene synthases. Li G, Köllner TG, Yin Y, Jiang Y, Chen H, Xu Y, Gershenzon J, Pichersky E, Chen F. Proc. Natl. Acad. Sci. U.S.A. 109 14711-14715 (2012)
  31. Altering product outcome in Abies grandis (-)-limonene synthase and (-)-limonene/(-)-alpha-pinene synthase by domain swapping and directed mutagenesis. Katoh S, Hyatt D, Croteau R. Arch. Biochem. Biophys. 425 65-76 (2004)
  32. Mechanistic insights from the binding of substrate and carbocation intermediate analogues to aristolochene synthase. Chen M, Al-lami N, Janvier M, D'Antonio EL, Faraldos JA, Cane DE, Allemann RK, Christianson DW. Biochemistry 52 5441-5453 (2013)
  33. Overexpression of the trichodiene synthase gene tri5 increases trichodermin production and antimicrobial activity in Trichoderma brevicompactum. Tijerino A, Cardoza RE, Moraga J, Malmierca MG, Vicente F, Aleu J, Collado IG, Gutiérrez S, Monte E, Hermosa R. Fungal Genet. Biol. 48 285-296 (2011)
  34. Alternative termination chemistries utilized by monoterpene cyclases: chimeric analysis of bornyl diphosphate, 1,8-cineole, and sabinene synthases. Peters RJ, Croteau RB. Arch. Biochem. Biophys. 417 203-211 (2003)
  35. Investigating the conservation pattern of a putative second terpene synthase divalent metal binding motif in plants. Zhou K, Peters RJ. Phytochemistry 70 366-369 (2009)
  36. Defining the potassium binding region in an apple terpene synthase. Green S, Squire CJ, Nieuwenhuizen NJ, Baker EN, Laing W. J. Biol. Chem. 284 8661-8669 (2009)
  37. Hedycaryol synthase in complex with nerolidol reveals terpene cyclase mechanism. Baer P, Rabe P, Citron CA, de Oliveira Mann CC, Kaufmann N, Groll M, Dickschat JS. Chembiochem 15 213-216 (2014)
  38. Conformational Analysis, Thermal Rearrangement, and EI-MS Fragmentation Mechanism of (1(10)E,4E,6S,7R)-Germacradien-6-ol by (13)C-Labeling Experiments. Rabe P, Barra L, Rinkel J, Riclea R, Citron CA, Klapschinski TA, Janusko A, Dickschat JS. Angew. Chem. Int. Ed. Engl. 54 13448-13451 (2015)
  39. A method for investigating the stereochemical course of terpene cyclisations. Rabe P, Rinkel J, Klapschinski TA, Barra L, Dickschat JS. Org. Biomol. Chem. 14 158-164 (2016)
  40. Domain swapping of Citrus limon monoterpene synthases: impact on enzymatic activity and product specificity. El Tamer MK, Lücker J, Bosch D, Verhoeven HA, Verstappen FW, Schwab W, van Tunen AJ, Voragen AG, de Maagd RA, Bouwmeester HJ. Arch. Biochem. Biophys. 411 196-203 (2003)
  41. Cloning and characterization of an Armillaria gallica cDNA encoding protoilludene synthase, which catalyzes the first committed step in the synthesis of antimicrobial melleolides. Engels B, Heinig U, Grothe T, Stadler M, Jennewein S. J. Biol. Chem. 286 6871-6878 (2011)
  42. Selectivity of fungal sesquiterpene synthases: role of the active site's H-1 alpha loop in catalysis. López-Gallego F, Wawrzyn GT, Schmidt-Dannert C. Appl. Environ. Microbiol. 76 7723-7733 (2010)
  43. Stabilisation of transition states prior to and following eudesmane cation in aristolochene synthase. Forcat S, Allemann RK. Org. Biomol. Chem. 4 2563-2567 (2006)
  44. Genetic dissection of sesquiterpene biosynthesis by Fusarium fujikuroi. Brock NL, Huss K, Tudzynski B, Dickschat JS. Chembiochem 14 311-315 (2013)
  45. Biosynthetic potential of sesquiterpene synthases: alternative products of tobacco 5-epi-aristolochene synthase. O'Maille PE, Chappell J, Noel JP. Arch. Biochem. Biophys. 448 73-82 (2006)
  46. Structures and Biosynthesis of Corvol Ethers--Sesquiterpenes from the Actinomycete Kitasatospora setae. Rabe P, Pahirulzaman KA, Dickschat JS. Angew. Chem. Int. Ed. Engl. 54 6041-6045 (2015)
  47. Electrostatic effects on (di)terpene synthase product outcome. Zhou K, Peters RJ. Chem. Commun. (Camb.) 47 4074-4080 (2011)
  48. Improved conditions for production of recombinant plant sesquiterpene synthases in Escherichia coli. Picaud S, Olsson ME, Brodelius PE. Protein Expr. Purif. 51 71-79 (2007)
  49. Structural basis for antibody catalysis of a cationic cyclization reaction. Zhu X, Heine A, Monnat F, Houk KN, Janda KD, Wilson IA. J. Mol. Biol. 329 69-83 (2003)
  50. The first structure of a bacterial diterpene cyclase: CotB2. Janke R, Görner C, Hirte M, Brück T, Loll B. Acta Crystallogr. D Biol. Crystallogr. 70 1528-1537 (2014)
  51. Modes of inactivation of trichodiene synthase by a cyclopropane-containing farnesyldiphosphate analog. Hong YJ, Tantillo DJ. Org. Biomol. Chem. 7 4101-4109 (2009)
  52. Experimental and Theoretical Studies on Corvol Ether Biosynthesis. Rabe P, Janusko A, Goldfuss B, Dickschat JS. Chembiochem 17 146-149 (2016)
  53. Structural Studies of Geosmin Synthase, a Bifunctional Sesquiterpene Synthase with αα Domain Architecture That Catalyzes a Unique Cyclization-Fragmentation Reaction Sequence. Harris GG, Lombardi PM, Pemberton TA, Matsui T, Weiss TM, Cole KE, Köksal M, Murphy FV, Vedula LS, Chou WK, Cane DE, Christianson DW. Biochemistry 54 7142-7155 (2015)
  54. Mushroom hunting by using bioinformatics: application of a predictive framework facilitates the selective identification of sesquiterpene synthases in basidiomycota. Quin MB, Flynn CM, Wawrzyn GT, Choudhary S, Schmidt-Dannert C. Chembiochem 14 2480-2491 (2013)
  55. Structural Revision and Elucidation of the Biosynthesis of Hypodoratoxide by (13) C,(13) C COSY NMR Spectroscopy. Barra L, Ibrom K, Dickschat JS. Angew. Chem. Int. Ed. Engl. 54 6637-6640 (2015)
  56. A single amino acid determines the site of deprotonation in the active center of sesquiterpene synthases SbTPS1 and SbTPS2 from Sorghum bicolor. Garms S, Chen F, Boland W, Gershenzon J, Köllner TG. Phytochemistry 75 6-13 (2012)
  57. Mechanism of Germacradien-4-ol Synthase-Controlled Water Capture. Grundy DJ, Chen M, González V, Leoni S, Miller DJ, Christianson DW, Allemann RK. Biochemistry 55 2112-2121 (2016)
  58. The role of aristolochene synthase in diphosphate activation. Faraldos JA, Gonzalez V, Allemann RK. Chem. Commun. (Camb.) 48 3230-3232 (2012)
  59. Genome-wide analysis of terpene synthases in soybean: functional characterization of GmTPS3. Liu J, Huang F, Wang X, Zhang M, Zheng R, Wang J, Yu D. Gene 544 83-92 (2014)
  60. Position-Specific Mass Shift Analysis: A Systematic Method for Investigating the EI-MS Fragmentation Mechanism of epi-Isozizaene. Rabe P, Klapschinski TA, Dickschat JS. Chembiochem 17 1333-1337 (2016)
  61. Structural and mechanistic analysis of engineered trichodiene synthase enzymes from Trichoderma harzianum: towards higher catalytic activities empowering sustainable agriculture. Kumari I, Chaudhary N, Sandhu P, Ahmed M, Akhter Y. J. Biomol. Struct. Dyn. 34 1176-1189 (2016)
  62. Functional Characterization of Novel Sesquiterpene Synthases from Indian Sandalwood, Santalum album. Srivastava PL, Daramwar PP, Krithika R, Pandreka A, Shankar SS, Thulasiram HV. Sci Rep 5 10095 (2015)
  63. Biosynthesis of mercapturic acid derivative of the labdane-type diterpene, cyslabdan that potentiates imipenem activity against methicillin-resistant Staphylococcus aureus: cyslabdan is generated by mycothiol-mediated xenobiotic detoxification. Ikeda H, Shin-Ya K, Nagamitsu T, Tomoda H. J. Ind. Microbiol. Biotechnol. 43 325-342 (2016)
  64. Small genome of the fungus Escovopsis weberi, a specialized disease agent of ant agriculture. de Man TJ, Stajich JE, Kubicek CP, Teiling C, Chenthamara K, Atanasova L, Druzhinina IS, Levenkova N, Birnbaum SS, Barribeau SM, Bozick BA, Suen G, Currie CR, Gerardo NM. Proc. Natl. Acad. Sci. U.S.A. 113 3567-3572 (2016)
  65. Probing the reaction mechanism of aristolochene synthase with 12,13-difluorofarnesyl diphosphate. Yu F, Miller DJ, Allemann RK. Chem. Commun. (Camb.) 4155-4157 (2007)
  66. Pogostol biosynthesis by the endophytic fungus Geniculosporium. Barra L, Schulz B, Dickschat JS. Chembiochem 15 2379-2383 (2014)
  67. Functional characterization and transient expression manipulation of a new sesquiterpene synthase involved in β-caryophyllene accumulation in Ocimum. Jayaramaiah RH, Anand A, Beedkar SD, Dholakia BB, Punekar SA, Kalunke RM, Gade WN, Thulasiram HV, Giri AP. Biochem. Biophys. Res. Commun. 473 265-271 (2016)
  68. Natural Phenolic Inhibitors of Trichothecene Biosynthesis by the Wheat Fungal Pathogen Fusarium culmorum: A Computational Insight into the Structure-Activity Relationship. Pani G, Dessì A, Dallocchio R, Scherm B, Azara E, Delogu G, Migheli Q. PLoS ONE 11 e0157316 (2016)
  69. Floral sesquiterpenes and their synthesis in dioecious kiwifruit. Nieuwenhuizen NJ, Green S, Atkinson RG. Plant Signal Behav 5 61-63 (2010)
  70. Structure-based virtual screening of hypothetical inhibitors of the enzyme longiborneol synthase-a potential target to reduce Fusarium head blight disease. Bresso E, Leroux V, Urban M, Hammond-Kosack KE, Maigret B, Martins NF. J Mol Model 22 163 (2016)
  71. Identification of a novel sesquiterpene biosynthetic machinery involved in astellolide biosynthesis. Shinohara Y, Takahashi S, Osada H, Koyama Y. Sci Rep 6 32865 (2016)
  72. Carbocation-π interaction: evaluation of the stabilization by phenylalanine of a biochemical carbocation intermediate. Ditchfield R, Spencer TA. Org. Biomol. Chem. 14 9543-9548 (2016)
  73. Isolation and functional characterization of a methyl jasmonate-responsive 3-carene synthase from Lavandula x intermedia. Adal AM, Sarker LS, Lemke AD, Mahmoud SS. Plant Mol. Biol. 93 641-657 (2017)
  74. Characterization of the first naturally thermostable terpene synthases and development of strategies to improve thermostability in this family of enzymes. Styles MQ, Nesbitt EA, Marr S, Hutchby M, Leak DJ. FEBS J. 284 1700-1711 (2017)
  75. Identification of a trichothecene production inhibitor by chemical array and library screening using trichodiene synthase as a target protein. Maeda K, Nakajima Y, Motoyama T, Kondoh Y, Kawamura T, Kanamaru K, Ohsato S, Nishiuchi T, Yoshida M, Osada H, Kobayashi T, Kimura M. Pestic Biochem Physiol 138 1-7 (2017)