1n20 Citations

Bornyl diphosphate synthase: structure and strategy for carbocation manipulation by a terpenoid cyclase.

Proc Natl Acad Sci U S A 99 15375-80 (2002)
Related entries: 1n1b, 1n1z, 1n21, 1n22, 1n23, 1n24

Cited: 160 times
EuropePMC logo PMID: 12432096

Abstract

The x-ray crystal structure of dimeric (+)-bornyl diphosphate synthase, a metal-requiring monoterpene cyclase from Salvia officinalis, is reported at 2.0-A resolution. Each monomer contains two alpha-helical domains: the C-terminal domain catalyzes the cyclization of geranyl diphosphate, orienting and stabilizing multiple reactive carbocation intermediates; the N-terminal domain has no clearly defined function, although its N terminus caps the active site in the C-terminal domain during catalysis. Structures of complexes with aza analogues of substrate and carbocation intermediates, as well as complexes with pyrophosphate and bornyl diphosphate, provide "snapshots" of the terpene cyclization cascade.

Reviews - 1n20 mentioned but not cited (1)

  1. Terpenoid synthase structures: a so far incomplete view of complex catalysis. Gao Y, Honzatko RB, Peters RJ. Nat Prod Rep 29 1153-1175 (2012)

Articles - 1n20 mentioned but not cited (14)

  1. 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)
  2. Structure of isoprene synthase illuminates the chemical mechanism of teragram atmospheric carbon emission. Köksal M, Zimmer I, Schnitzler JP, Christianson DW. J Mol Biol 402 363-373 (2010)
  3. Identification of amino acid networks governing catalysis in the closed complex of class I terpene synthases. Schrepfer P, Buettner A, Goerner C, Hertel M, van Rijn J, Wallrapp F, Eisenreich W, Sieber V, Kourist R, Brück T. Proc Natl Acad Sci U S A 113 E958-67 (2016)
  4. Biochemical characterization and homology modeling of methylbutenol synthase and implications for understanding hemiterpene synthase evolution in plants. Gray DW, Breneman SR, Topper LA, Sharkey TD. J Biol Chem 286 20582-20590 (2011)
  5. Structure of 2-methylisoborneol synthase from Streptomyces coelicolor and implications for the cyclization of a noncanonical C-methylated monoterpenoid substrate. Köksal M, Chou WK, Cane DE, Christianson DW. Biochemistry 51 3011-3020 (2012)
  6. An (E,E)-α-farnesene synthase gene of soybean has a role in defence against nematodes and is involved in synthesizing insect-induced volatiles. Lin J, Wang D, Chen X, Köllner TG, Mazarei M, Guo H, Pantalone VR, Arelli P, Stewart CN, Wang N, Chen F. Plant Biotechnol J 15 510-519 (2017)
  7. 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)
  8. Predicting Productive Binding Modes for Substrates and Carbocation Intermediates in Terpene Synthases-Bornyl Diphosphate Synthase as a Representative Case. O'Brien TE, Bertolani SJ, Zhang Y, Siegel JB, Tantillo DJ. ACS Catal 8 3322-3330 (2018)
  9. Molecular cloning and biochemical characterization of isoprene synthases from the tropical trees Ficus virgata, Ficus septica, and Casuarina equisetifolia. Oku H, Inafuku M, Ishikawa T, Takamine T, Ishmael M, Fukuta M. J Plant Res 128 849-861 (2015)
  10. Structural Characterization of Early Michaelis Complexes in the Reaction Catalyzed by (+)-Limonene Synthase from Citrus sinensis Using Fluorinated Substrate Analogues. Kumar RP, Morehouse BR, Matos JO, Malik K, Lin H, Krauss IJ, Oprian DD. Biochemistry 56 1716-1725 (2017)
  11. Predicting binding sites from unbound versus bound protein structures. Clark JJ, Orban ZJ, Carlson HA. Sci Rep 10 15856 (2020)
  12. Combinatorial biosynthesis and the basis for substrate promiscuity in class I diterpene synthases. Jia M, Mishra SK, Tufts S, Jernigan RL, Peters RJ. Metab Eng 55 44-58 (2019)
  13. Purification and biochemical characterization of recombinant Persicaria minor β-sesquiphellandrene synthase. Ker DS, Pang SL, Othman NF, Kumaran S, Tan EF, Krishnan T, Chan KG, Othman R, Hassan M, Ng CL. PeerJ 5 e2961 (2017)
  14. Cyclization mechanism of monoterpenes catalyzed by monoterpene synthases in dipterocarpaceae. Lu X, Bai J, Tian Z, Li C, Ahmed N, Liu X, Cheng J, Lu L, Cai J, Jiang H, Wang W. Synth Syst Biotechnol 9 11-18 (2024)


Reviews citing this publication (26)

  1. The family of terpene synthases in plants: a mid-size family of genes for specialized metabolism that is highly diversified throughout the kingdom. Chen F, Tholl D, Bohlmann J, Pichersky E. Plant J 66 212-229 (2011)
  2. Lessons from natural molecules. Clardy J, Walsh C. Nature 432 829-837 (2004)
  3. Monoterpene and sesquiterpene synthases and the origin of terpene skeletal diversity in plants. Degenhardt J, Köllner TG, Gershenzon J. Phytochemistry 70 1621-1637 (2009)
  4. Biochemistry of plant volatiles. Dudareva N, Pichersky E, Gershenzon J. Plant Physiol 135 1893-1902 (2004)
  5. Terpene synthases and the regulation, diversity and biological roles of terpene metabolism. Tholl D. Curr Opin Plant Biol 9 297-304 (2006)
  6. Genes, enzymes and chemicals of terpenoid diversity in the constitutive and induced defence of conifers against insects and pathogens. Keeling CI, Bohlmann J. New Phytol 170 657-675 (2006)
  7. Structural and Chemical Biology of Terpenoid Cyclases. Christianson DW. Chem Rev 117 11570-11648 (2017)
  8. Unearthing the roots of the terpenome. Christianson DW. Curr Opin Chem Biol 12 141-150 (2008)
  9. Biosynthesis via carbocations: theoretical studies on terpene formation. Tantillo DJ. Nat Prod Rep 28 1035-1053 (2011)
  10. Terpene biosynthesis: modularity rules. Oldfield E, Lin FY. Angew Chem Int Ed Engl 51 1124-1137 (2012)
  11. Bacterial terpene cyclases. Dickschat JS. Nat Prod Rep 33 87-110 (2016)
  12. 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)
  13. Terpene Synthases as Metabolic Gatekeepers in the Evolution of Plant Terpenoid Chemical Diversity. Karunanithi PS, Zerbe P. Front Plant Sci 10 1166 (2019)
  14. Diversity, regulation, and genetic manipulation of plant mono- and sesquiterpenoid biosynthesis. Yu F, Utsumi R. Cell Mol Life Sci 66 3043-3052 (2009)
  15. Molecular and structural basis of metabolic diversity mediated by prenyldiphosphate converting enzymes. Brandt W, Bräuer L, Günnewich N, Kufka J, Rausch F, Schulze D, Schulze E, Weber R, Zakharova S, Wessjohann L. Phytochemistry 70 1758-1775 (2009)
  16. Multi-domain terpenoid cyclase architecture and prospects for proximity in bifunctional catalysis. Chen M, Harris GG, Pemberton TA, Christianson DW. Curr Opin Struct Biol 41 27-37 (2016)
  17. On the Evolution and Functional Diversity of Terpene Synthases in the Pinus Species: A Review. Alicandri E, Paolacci AR, Osadolor S, Sorgonà A, Badiani M, Ciaffi M. J Mol Evol 88 253-283 (2020)
  18. Enhanced structural diversity in terpenoid biosynthesis: enzymes, substrates and cofactors. Vattekkatte A, Garms S, Brandt W, Boland W. Org Biomol Chem 16 348-362 (2018)
  19. Chimeric Terpene Synthases Possessing both Terpene Cyclization and Prenyltransfer Activities. Mitsuhashi T, Abe I. Chembiochem (2018)
  20. Protein engineering towards natural product synthesis and diversification. Zabala AO, Cacho RA, Tang Y. J Ind Microbiol Biotechnol 39 227-241 (2012)
  21. Current understanding and biotechnological application of the bacterial diterpene synthase CotB2. Driller R, Garbe D, Mehlmer N, Fuchs M, Raz K, Major DT, Brück T, Loll B. Beilstein J Org Chem 15 2355-2368 (2019)
  22. Evolution of Terpene Synthases in Orchidaceae. Huang LM, Huang H, Chuang YC, Chen WH, Wang CN, Chen HH. Int J Mol Sci 22 6947 (2021)
  23. Plasticity engineering of plant monoterpene synthases and application for microbial production of monoterpenoids. Lei D, Qiu Z, Qiao J, Zhao GR. Biotechnol Biofuels 14 147 (2021)
  24. Predictive Engineering of Class I Terpene Synthases Using Experimental and Computational Approaches. Leferink NGH, Scrutton NS. Chembiochem 23 e202100484 (2022)
  25. Brushes with sage. Cane DE. Arch Biochem Biophys 448 117-122 (2006)
  26. Decoding Catalysis by Terpene Synthases. Whitehead JN, Leferink NGH, Johannissen LO, Hay S, Scrutton NS. ACS Catal 13 12774-12802 (2023)

Articles citing this publication (119)

  1. Terpene synthases are widely distributed in bacteria. Yamada Y, Kuzuyama T, Komatsu M, Shin-Ya K, Omura S, Cane DE, Ikeda H. Proc Natl Acad Sci U S A 112 857-862 (2015)
  2. Functional characterization of nine Norway Spruce TPS genes and evolution of gymnosperm terpene synthases of the TPS-d subfamily. Martin DM, Fäldt J, Bohlmann J. Plant Physiol 135 1908-1927 (2004)
  3. The variability of sesquiterpenes emitted from two Zea mays cultivars is controlled by allelic variation of two terpene synthase genes encoding stereoselective multiple product enzymes. Köllner TG, Schnee C, Gershenzon J, Degenhardt J. Plant Cell 16 1115-1131 (2004)
  4. Rational conversion of substrate and product specificity in a Salvia monoterpene synthase: structural insights into the evolution of terpene synthase function. Kampranis SC, Ioannidis D, Purvis A, Mahrez W, Ninga E, Katerelos NA, Anssour S, Dunwell JM, Degenhardt J, Makris AM, Goodenough PW, Johnson CB. Plant Cell 19 1994-2005 (2007)
  5. Identification of syn-pimara-7,15-diene synthase reveals functional clustering of terpene synthases involved in rice phytoalexin/allelochemical biosynthesis. Wilderman PR, Xu M, Jin Y, Coates RM, Peters RJ. Plant Physiol 135 2098-2105 (2004)
  6. Structure of limonene synthase, a simple model for terpenoid cyclase catalysis. Hyatt DC, Youn B, Zhao Y, Santhamma B, Coates RM, Croteau RB, Kang C. Proc Natl Acad Sci U S A 104 5360-5365 (2007)
  7. Tomato linalool synthase is induced in trichomes by jasmonic acid. van Schie CC, Haring MA, Schuurink RC. Plant Mol Biol 64 251-263 (2007)
  8. Evolution of the isoprene biosynthetic pathway in kudzu. Sharkey TD, Yeh S, Wiberley AE, Falbel TG, Gong D, Fernandez DE. Plant Physiol 137 700-712 (2005)
  9. Terpene Specialized Metabolism in Arabidopsis thaliana. Tholl D, Lee S. Arabidopsis Book 9 e0143 (2011)
  10. Following evolution's lead to a single residue switch for diterpene synthase product outcome. Xu M, Wilderman PR, Peters RJ. Proc Natl Acad Sci U S A 104 7397-7401 (2007)
  11. Functional identification of rice syn-copalyl diphosphate synthase and its role in initiating biosynthesis of diterpenoid phytoalexin/allelopathic natural products. Xu M, Hillwig ML, Prisic S, Coates RM, Peters RJ. Plant J 39 309-318 (2004)
  12. Vitis vinifera terpenoid cyclases: functional identification of two sesquiterpene synthase cDNAs encoding (+)-valencene synthase and (-)-germacrene D synthase and expression of mono- and sesquiterpene synthases in grapevine flowers and berries. Lücker J, Bowen P, Bohlmann J. Phytochemistry 65 2649-2659 (2004)
  13. 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)
  14. 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)
  15. Functional characterization of the rice kaurene synthase-like gene family. Xu M, Wilderman PR, Morrone D, Xu J, Roy A, Margis-Pinheiro M, Upadhyaya NM, Coates RM, Peters RJ. Phytochemistry 68 312-326 (2007)
  16. Cloning and functional characterization of three terpene synthases from lavender (Lavandula angustifolia). Landmann C, Fink B, Festner M, Dregus M, Engel KH, Schwab W. Arch Biochem Biophys 465 417-429 (2007)
  17. Trinuclear Metal Clusters in Catalysis by Terpenoid Synthases. Aaron JA, Christianson DW. Pure Appl Chem 82 1585-1597 (2010)
  18. cDNA isolation, functional expression, and characterization of (+)-alpha-pinene synthase and (-)-alpha-pinene synthase from loblolly pine (Pinus taeda): stereocontrol in pinene biosynthesis. Phillips MA, Wildung MR, Williams DC, Hyatt DC, Croteau R. Arch Biochem Biophys 411 267-276 (2003)
  19. The diverse sesquiterpene profile of patchouli, Pogostemon cablin, is correlated with a limited number of sesquiterpene synthases. Deguerry F, Pastore L, Wu S, Clark A, Chappell J, Schalk M. Arch Biochem Biophys 454 123-136 (2006)
  20. Diterpene cyclases and the nature of the isoprene fold. Cao R, Zhang Y, Mann FM, Huang C, Mukkamala D, Hudock MP, Mead ME, Prisic S, Wang K, Lin FY, Chang TK, Peters RJ, Oldfield E. Proteins 78 2417-2432 (2010)
  21. 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)
  22. Conversion of squalene to the pentacarbocyclic hopene. Reinert DJ, Balliano G, Schulz GE. Chem Biol 11 121-126 (2004)
  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. A Comprehensive Survey on the Terpene Synthase Gene Family Provides New Insight into Its Evolutionary Patterns. Jiang SY, Jin J, Sarojam R, Ramachandran S. Genome Biol Evol 11 2078-2098 (2019)
  25. 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)
  26. 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)
  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. Structural elucidation of cisoid and transoid cyclization pathways of a sesquiterpene synthase using 2-fluorofarnesyl diphosphates. Noel JP, Dellas N, Faraldos JA, Zhao M, Hess BA, Smentek L, Coates RM, O'Maille PE. ACS Chem Biol 5 377-392 (2010)
  29. 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)
  30. Reprogramming the chemodiversity of terpenoid cyclization by remolding the active site contour of epi-isozizaene synthase. Li R, Chou WK, Himmelberger JA, Litwin KM, Harris GG, Cane DE, Christianson DW. Biochemistry 53 1155-1168 (2014)
  31. Transcriptome analysis and identification of genes related to terpenoid biosynthesis in Cinnamomum camphora. Chen C, Zheng Y, Zhong Y, Wu Y, Li Z, Xu LA, Xu M. BMC Genomics 19 550 (2018)
  32. A detailed view of 2-methylisoborneol biosynthesis. Brock NL, Ravella SR, Schulz S, Dickschat JS. Angew Chem Int Ed Engl 52 2100-2104 (2013)
  33. Unusual features of a recombinant apple alpha-farnesene synthase. Green S, Friel EN, Matich A, Beuning LL, Cooney JM, Rowan DD, MacRae E. Phytochemistry 68 176-188 (2007)
  34. Functional analysis of (4S)-limonene synthase mutants reveals determinants of catalytic outcome in a model monoterpene synthase. Srividya N, Davis EM, Croteau RB, Lange BM. Proc Natl Acad Sci U S A 112 3332-3337 (2015)
  35. 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)
  36. Plasticity and evolution of (+)-3-carene synthase and (-)-sabinene synthase functions of a sitka spruce monoterpene synthase gene family associated with weevil resistance. Roach CR, Hall DE, Zerbe P, Bohlmann J. J Biol Chem 289 23859-23869 (2014)
  37. 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)
  38. 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)
  39. Quantum chemical dissection of the classic terpinyl/pinyl/bornyl/camphyl cation conundrum-the role of pyrophosphate in manipulating pathways to monoterpenes. Hong YJ, Tantillo DJ. Org Biomol Chem 8 4589-4600 (2010)
  40. 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)
  41. Two pockets in the active site of maize sesquiterpene synthase TPS4 carry out sequential parts of the reaction scheme resulting in multiple products. Köllner TG, O'Maille PE, Gatto N, Boland W, Gershenzon J, Degenhardt J. Arch Biochem Biophys 448 83-92 (2006)
  42. Analysis of Terpene Synthase Family Genes in Camellia sinensis with an Emphasis on Abiotic Stress Conditions. Zhou HC, Shamala LF, Yi XK, Yan Z, Wei S. Sci Rep 10 933 (2020)
  43. Structure of the ent-Copalyl Diphosphate Synthase PtmT2 from Streptomyces platensis CB00739, a Bacterial Type II Diterpene Synthase. Rudolf JD, Dong LB, Cao H, Hatzos-Skintges C, Osipiuk J, Endres M, Chang CY, Ma M, Babnigg G, Joachimiak A, Phillips GN, Shen B. J Am Chem Soc 138 10905-10915 (2016)
  44. 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)
  45. 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)
  46. An unexpected diterpene cyclase from rice: functional identification of a stemodene synthase. Morrone D, Jin Y, Xu M, Choi SY, Coates RM, Peters RJ. Arch Biochem Biophys 448 133-140 (2006)
  47. Emission and Accumulation of Monoterpene and the Key Terpene Synthase (TPS) Associated with Monoterpene Biosynthesis in Osmanthus fragrans Lour. Zeng X, Liu C, Zheng R, Cai X, Luo J, Zou J, Wang C. Front Plant Sci 6 1232 (2015)
  48. Exploring the Influence of Domain Architecture on the Catalytic Function of Diterpene Synthases. Pemberton TA, Chen M, Harris GG, Chou WK, Duan L, Köksal M, Genshaft AS, Cane DE, Christianson DW. Biochemistry 56 2010-2023 (2017)
  49. 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)
  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. 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)
  52. Structural Basis of Catalysis in the Bacterial Monoterpene Synthases Linalool Synthase and 1,8-Cineole Synthase. Karuppiah V, Ranaghan KE, Leferink NGH, Johannissen LO, Shanmugam M, Ní Cheallaigh A, Bennett NJ, Kearsey LJ, Takano E, Gardiner JM, van der Kamp MW, Hay S, Mulholland AJ, Leys D, Scrutton NS. ACS Catal 7 6268-6282 (2017)
  53. Towards a comprehensive understanding of the structural dynamics of a bacterial diterpene synthase during catalysis. Driller R, Janke S, Fuchs M, Warner E, Mhashal AR, Major DT, Christmann M, Brück T, Loll B. Nat Commun 9 3971 (2018)
  54. 16-Aza-ent-beyerane and 16-Aza-ent-trachylobane: potent mechanism-based inhibitors of recombinant ent-kaurene synthase from Arabidopsis thaliana. Roy A, Roberts FG, Wilderman PR, Zhou K, Peters RJ, Coates RM. J Am Chem Soc 129 12453-12460 (2007)
  55. Bornyl-diphosphate synthase from Lavandula angustifolia: A major monoterpene synthase involved in essential oil quality. Despinasse Y, Fiorucci S, Antonczak S, Moja S, Bony A, Nicolè F, Baudino S, Magnard JL, Jullien F. Phytochemistry 137 24-33 (2017)
  56. To what extent do structural changes in catalytic metal sites affect enzyme function? Valasatava Y, Rosato A, Furnham N, Thornton JM, Andreini C. J Inorg Biochem 179 40-53 (2018)
  57. Electrostatic effects on (di)terpene synthase product outcome. Zhou K, Peters RJ. Chem Commun (Camb) 47 4074-4080 (2011)
  58. Buffer interference with protein dynamics: a case study on human liver fatty acid binding protein. Long D, Yang D. Biophys J 96 1482-1488 (2009)
  59. Functional and Structural Characterization of a (+)-Limonene Synthase from Citrus sinensis. Morehouse BR, Kumar RP, Matos JO, Olsen SN, Entova S, Oprian DD. Biochemistry 56 1706-1715 (2017)
  60. 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)
  61. A detailed view on 1,8-cineol biosynthesis by Streptomyces clavuligerus. Rinkel J, Rabe P, Zur Horst L, Dickschat JS. Beilstein J Org Chem 12 2317-2324 (2016)
  62. Experiment and Simulation Reveal How Mutations in Functional Plasticity Regions Guide Plant Monoterpene Synthase Product Outcome. Leferink NGH, Ranaghan KE, Karuppiah V, Currin A, van der Kamp MW, Mulholland AJ, Scrutton NS. ACS Catal 8 3780-3791 (2019)
  63. RNA-Seq in the discovery of a sparsely expressed scent-determining monoterpene synthase in lavender (Lavandula). Adal AM, Sarker LS, Malli RPN, Liang P, Mahmoud SS. Planta 249 271-290 (2019)
  64. Crystal Structure and Potential Head-to-Middle Condensation Function of a Z,Z-Farnesyl Diphosphate Synthase. Chan YT, Ko TP, Yao SH, Chen YW, Lee CC, Wang AH. ACS Omega 2 930-936 (2017)
  65. Enantioselective Tail-to-Head Cyclizations Catalyzed by Dual-Hydrogen-Bond Donors. Kutateladze DA, Strassfeld DA, Jacobsen EN. J Am Chem Soc 142 6951-6956 (2020)
  66. Genome-Wide Analysis of Terpene Synthase Gene Family in Mentha longifolia and Catalytic Activity Analysis of a Single Terpene Synthase. Chen Z, Vining KJ, Qi X, Yu X, Zheng Y, Liu Z, Fang H, Li L, Bai Y, Liang C, Li W, Lange BM. Genes (Basel) 12 518 (2021)
  67. In Planta Recapitulation of Isoprene Synthase Evolution from Ocimene Synthases. Li M, Xu J, Algarra Alarcon A, Carlin S, Barbaro E, Cappellin L, Velikova V, Vrhovsek U, Loreto F, Varotto C. Mol Biol Evol 34 2583-2599 (2017)
  68. Inhibition of monoterpene cyclases by inert analogues of geranyl diphosphate and linalyl diphosphate. Karp F, Zhao Y, Santhamma B, Assink B, Coates RM, Croteau RB. Arch Biochem Biophys 468 140-146 (2007)
  69. 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)
  70. Proposed mechanism for diterpene synthases in the formation of phomactatriene and taxadiene. Tokiwano T, Endo T, Tsukagoshi T, Goto H, Fukushi E, Oikawa H. Org Biomol Chem 3 2713-2722 (2005)
  71. Substitution of Aromatic Residues with Polar Residues in the Active Site Pocket of epi-Isozizaene Synthase Leads to the Generation of New Cyclic Sesquiterpenes. Blank PN, Barrow GH, Chou WKW, Duan L, Cane DE, Christianson DW. Biochemistry 56 5798-5811 (2017)
  72. Functional identification of a Lippia dulcis bornyl diphosphate synthase that contains a duplicated, inhibitory arginine-rich motif. Hurd MC, Kwon M, Ro DK. Biochem Biophys Res Commun 490 963-968 (2017)
  73. Predicting the functions and specificity of triterpenoid synthases: a mechanism-based multi-intermediate docking approach. Tian BX, Wallrapp FH, Holiday GL, Chow JY, Babbitt PC, Poulter CD, Jacobson MP. PLoS Comput Biol 10 e1003874 (2014)
  74. Characterization of α-humulene synthases responsible for the production of sesquiterpenes induced by methyl jasmonate in Aquilaria cell culture. Kumeta Y, Ito M. J Nat Med 70 452-459 (2016)
  75. Probing the Role of Active Site Water in the Sesquiterpene Cyclization Reaction Catalyzed by Aristolochene Synthase. Chen M, Chou WK, Al-Lami N, Faraldos JA, Allemann RK, Cane DE, Christianson DW. Biochemistry 55 2864-2874 (2016)
  76. 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)
  77. Bioinformatics-aided identification, characterization and applications of mushroom linalool synthases. Zhang C, Chen X, Lee RTC, T R, Maurer-Stroh S, Rühl M. Commun Biol 4 223 (2021)
  78. Enantioselective inhibition of squalene synthase by aziridine analogues of presqualene diphosphate. Koohang A, Bailey JL, Coates RM, Erickson HK, Owen D, Poulter CD. J Org Chem 75 4769-4777 (2010)
  79. Functional characterization of a new terpene synthase from Plectranthus amboinicus. Ashaari NS, Ab Rahim MH, Sabri S, Lai KS, Song AA, Abdul Rahim R, Wan Abdullah WMAN, Ong Abdullah J. PLoS One 15 e0235416 (2020)
  80. Functional characterization of three Coffea arabica L. monoterpene synthases: insights into the enzymatic machinery of coffee aroma. Del Terra L, Lonzarich V, Asquini E, Navarini L, Graziosi G, Suggi Liverani F, Pallavicini A. Phytochemistry 89 6-14 (2013)
  81. Four terpene synthases contribute to the generation of chemotypes in tea tree (Melaleuca alternifolia). Padovan A, Keszei A, Hassan Y, Krause ST, Köllner TG, Degenhardt J, Gershenzon J, Külheim C, Foley WJ. BMC Plant Biol 17 160 (2017)
  82. 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)
  83. Molecular dynamics study of taxadiene synthase catalysis. Escorcia AM, van Rijn JPM, Cheng GJ, Schrepfer P, Brück TB, Thiel W. J Comput Chem 39 1215-1225 (2018)
  84. Diversification of the monoterpene synthase gene family (TPSb) in Protium, a highly diverse genus of tropical trees. Zapata F, Fine PV. Mol Phylogenet Evol 68 432-442 (2013)
  85. Overexpression of Terpenoid Biosynthesis Genes From Garden Sage (Salvia officinalis) Modulates Rhizobia Interaction and Nodulation in Soybean. Ali M, Miao L, Hou Q, Darwish DB, Alrdahe SS, Ali A, Benedito VA, Tadege M, Wang X, Zhao J. Front Plant Sci 12 783269 (2021)
  86. Redesigning the Molecular Choreography to Prevent Hydroxylation in Germacradien-11-ol Synthase Catalysis. Srivastava PL, Escorcia AM, Huynh F, Miller DJ, Allemann RK, van der Kamp MW. ACS Catal 11 1033-1041 (2021)
  87. The amino-terminal segment in the β-domain of δ-cadinene synthase is essential for catalysis. González V, Grundy DJ, Faraldos JA, Allemann RK. Org Biomol Chem 14 7451-7454 (2016)
  88. Unexpected reactivity of 2-fluorolinalyl diphosphate in the active site of crystalline 2-methylisoborneol synthase. Köksal M, Chou WK, Cane DE, Christianson DW. Biochemistry 52 5247-5255 (2013)
  89. An automated pipeline for the screening of diverse monoterpene synthase libraries. Leferink NGH, Dunstan MS, Hollywood KA, Swainston N, Currin A, Jervis AJ, Takano E, Scrutton NS. Sci Rep 9 11936 (2019)
  90. Molecular cloning and characterization of a linalool synthase from lemon myrtle. Sugiura M, Ito S, Saito Y, Niwa Y, Koltunow AM, Sugimoto O, Sakai H. Biosci Biotechnol Biochem 75 1245-1248 (2011)
  91. A Structural View on the Stereospecificity of Plant Borneol-Type Dehydrogenases. Chánique AM, Dimos N, Drienovská I, Calderini E, Pantín MP, Helmer CPO, Hofer M, Sieber V, Parra LP, Loll B, Kourist R. ChemCatChem 13 2262-2277 (2021)
  92. Alternative synthesis of the Colorado potato beetle pheromone. Faraldos JA, Coates RM, Giner JL. J Org Chem 78 10548-10554 (2013)
  93. Purification and kinetic properties of elisabethatriene synthase from the coral Pseudopterogorgia elisabethae. Brück TB, Kerr RG. Comp Biochem Physiol B Biochem Mol Biol 143 269-278 (2006)
  94. The role of aristolochene synthase in diphosphate activation. Faraldos JA, Gonzalez V, Allemann RK. Chem Commun (Camb) 48 3230-3232 (2012)
  95. A non-synonymous nucleotide substitution can account for one evolutionary route to sesquiterpene synthase activity in the TPS-b subgroup. Green S, Baker EN, Laing W. FEBS Lett 585 1841-1846 (2011)
  96. Molecular Determinants of Carbocation Cyclisation in Bacterial Monoterpene Synthases. Leferink NGH, Escorcia AM, Ouwersloot BR, Johanissen LO, Hay S, van der Kamp MW, Scrutton NS. Chembiochem 23 e202100688 (2022)
  97. A Comparison of Two Monoterpenoid Synthases Reveals Molecular Mechanisms Associated With the Difference of Bioactive Monoterpenoids Between Amomum villosum and Amomum longiligulare. Zhao H, Li M, Zhao Y, Lin X, Liang H, Wei J, Wei W, Ma D, Zhou Z, Yang J. Front Plant Sci 12 695551 (2021)
  98. Direct Evidence of an Enzyme-Generated LPP Intermediate in (+)-Limonene Synthase Using a Fluorinated GPP Substrate Analog. Morehouse BR, Kumar RP, Matos JO, Yu Q, Bannister A, Malik K, Temme JS, Krauss IJ, Oprian DD. ACS Chem Biol 14 2035-2043 (2019)
  99. Discovery, Structure, and Mechanism of a Class II Sesquiterpene Cyclase. Pan X, Du W, Zhang X, Lin X, Li FR, Yang Q, Wang H, Rudolf JD, Zhang B, Dong LB. J Am Chem Soc 144 22067-22074 (2022)
  100. Incubation of 2-methylisoborneol synthase with the intermediate analog 2-methylneryl diphosphate. Chou WK, Gould CA, Cane DE. J Antibiot (Tokyo) 70 625-631 (2017)
  101. Kinetic studies and homology modeling of a dual-substrate linalool/nerolidol synthase from Plectranthus amboinicus. Ashaari NS, Ab Rahim MH, Sabri S, Lai KS, Song AA, Abdul Rahim R, Ong Abdullah J. Sci Rep 11 17094 (2021)
  102. Identification of a Novel (-)-5-Epieremophilene Synthase from Salvia miltiorrhiza via Transcriptome Mining. Fang X, Li CY, Yang Y, Cui MY, Chen XY, Yang L. Front Plant Sci 8 627 (2017)
  103. Molecular characterization of a Novel NAD+-dependent farnesol dehydrogenase SoFLDH gene involved in sesquiterpenoid synthases from Salvia officinalis. Ali M, Nishawy E, Ramadan WA, Ewas M, Rizk MS, Sief-Eldein AGM, El-Zayat MAS, Hassan AHM, Guo M, Hu GW, Wang S, Ahmed FA, Amar MH, Wang QF. PLoS One 17 e0269045 (2022)
  104. Overexpression of Panax ginseng sesquiterpene synthase gene confers tolerance against Pseudomonas syringae pv. tomato in Arabidopsis thaliana. Yoon SJ, Sukweenadhi J, Khorolragchaa A, Mathiyalagan R, Subramaniyam S, Kim YJ, Kim HB, Kim MJ, Kim YJ, Yang DC. Physiol Mol Biol Plants 22 485-495 (2016)
  105. Tweezing the cofactor preference of gymnosperm pinene synthase. Tashiro M, Ono K, Kimura Y, Kawai-Noma S, Saito K, Umeno D. Biosci Biotechnol Biochem 82 1058-1061 (2018)
  106. Understanding the role of active site residues in CotB2 catalysis using a cluster model. Raz K, Driller R, Brück T, Loll B, Major DT. Beilstein J Org Chem 16 50-59 (2020)
  107. Artemisia annua L. plants lacking Bornyl diPhosphate Synthase reallocate carbon from monoterpenes to sesquiterpenes except artemisinin. Czechowski T, Branigan C, Rae A, Rathbone D, Larson TR, Harvey D, Catania TM, Zhang D, Li Y, Salmon M, Bowles DJ, O Maille P, Graham IA. Front Plant Sci 13 1000819 (2022)
  108. Cloning, functional characterization and evaluating potential in metabolic engineering for lavender ( +)-bornyl diphosphate synthase. Adal AM, Najafianashrafi E, Sarker LS, Mahmoud SS. Plant Mol Biol 111 117-130 (2023)
  109. Exploring the catalytic cascade of cembranoid biosynthesis by combination of genetic engineering and molecular simulations. Schrepfer P, Ugur I, Klumpe S, Loll B, Kaila VRI, Brück T. Comput Struct Biotechnol J 18 1819-1829 (2020)
  110. Genome-wide identification, expression profile and evolutionary relationships of TPS genes in the neotropical fruit tree species Psidium cattleyanum. Canal D, Escudero FLG, Mendes LA, da Silva Ferreira MF, Turchetto-Zolet AC. Sci Rep 13 3930 (2023)
  111. Highly selective acid-catalyzed olefin isomerization of limonene to terpinolene by kinetic suppression of overreactions in a confined space of porous metal-macrocycle frameworks. He W, Tashiro S, Shionoya M. Chem Sci 13 8752-8758 (2022)
  112. Multiple variation patterns of terpene synthases in 26 maize genomes. Sun Y, Xiao W, Wang QN, Wang J, Kong XD, Ma WH, Liu SX, Ren P, Xu LN, Zhang YJ. BMC Genomics 24 46 (2023)
  113. Historical Article Nature as organic chemist. Cane DE. J Antibiot (Tokyo) 69 473-485 (2016)
  114. Structure of Sesquisabinene Synthase 1, a Terpenoid Cyclase That Generates a Strained [3.1.0] Bridged-Bicyclic Product. Blank PN, Shinsky SA, Christianson DW. ACS Chem Biol 14 1011-1019 (2019)
  115. Thirteen Dipterocarpoideae genomes provide insights into their evolution and borneol biosynthesis. Tian Z, Zeng P, Lu X, Zhou T, Han Y, Peng Y, Xiao Y, Zhou B, Liu X, Zhang Y, Yu Y, Li Q, Zong H, Zhang F, Jiang H, He J, Cai J. Plant Commun 3 100464 (2022)
  116. Unusual (2R,6R)-bicyclo[3.1.1]heptane ring construction in fungal α-trans-bergamotene biosynthesis. Wen YH, Chen TJ, Jiang LY, Li L, Guo M, Peng Y, Chen JJ, Pei F, Yang JL, Wang RS, Gong T, Zhu P. iScience 25 104030 (2022)
  117. In Silico Genome-Wide Mining and Analysis of Terpene Synthase Gene Family in Hevea Brasiliensis. Liang J, Wang, Li X, Huang W, Xie C, Fu M, Zhang H, Meng Q. Biochem Genet 61 1185-1209 (2023)
  118. Monoterpene Synthase Genes and Monoterpene Profiles in Pinus nigra subsp. laricio. Alicandri E, Covino S, Sebastiani B, Paolacci AR, Badiani M, Sorgonà A, Ciaffi M. Plants (Basel) 11 449 (2022)
  119. Tryptophan Stabilization of a Biochemical Carbocation Evaluated by Analysis of π Complexes of 3-Ethylindole with the t-Butyl Cation. Spencer TA, Ditchfield R. ACS Omega 8 26497-26507 (2023)