Biochemical characterization of the castor bean ent-kaurene synthase(-like) family supports quantum chemical view of diterpene cyclization

Phytochemistry

Volumn 103, Issue , 2014, Pages 13-21

  Jackson, Alana J ^a   Hershey, David M ^a   Chesnut, Taylor ^a   Xu, Meimei ^a   Peters, Reuben J ^a  

^a IOWA STATE UNIVERSITY   (United States)

Author keywords

Diterpenoids; Natural products biosynthesis; Terpene synthases

Indexed keywords

DITERPENE; ENT-KAURENE SYNTHETASE B; TRANSFERASE;

CHEMISTRY; CYCLIZATION; ENZYMOLOGY; METABOLISM; RICINUS COMMUNIS;

ALKYL AND ARYL TRANSFERASES; CASTOR BEAN; CYCLIZATION; DITERPENES;

EID: 84901236690     PISSN: 00319422     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.phytochem.2014.04.005     Document Type: Article

References (38)

1. J. Bohlmann, G. Meyer-Gauen, and R. Croteau Plant terpenoid synthases: molecular biology and phylogenetic analysis Proc. Natl. Acad. Sci. USA 95 1998 4126 4133 (Pubitemid 28207876)
2. A. Caniard, P. Zerbe, S. Legrand, A. Cohade, N. Valot, J.L. Magnard, J. Bohlmann, and L. Legendre Discovery and functional characterization of two diterpene synthases for sclareol biosynthesis in Salvia sclarea (L.) and their relevance for perfume manufacture BMC Plant Biol. 12 2012 119
3. A.P. Chan, J. Crabtree, Q. Zhao, H. Lorenzi, J. Orvis, D. Puiu, A. Melake-Berhan, K.M. Jones, J. Redman, G. Chen, E.B. Cahoon, M. Gedil, M. Stanke, B.J. Haas, J.R. Wortman, C.M. Fraser-Liggett, J. Ravel, and P.D. Rabinowicz Draft genome sequence of the oilseed species Ricinus communis Nat. Biotechnol. 28 2010 951 956
4. F. Chen, D. Tholl, J. Bohlmann, and E. Pichersky The family of terpene synthases in plants: a mid-size family of genes for specialized metabolism that is highly diversified throughout the kingdom Plant J. 66 2011 212 229
5. D.W. Christianson Structural biology and chemistry of the terpenoid cyclases Chem. Rev. 106 2006 3412 3442 (Pubitemid 44376943)
6. A. Cyr, P.R. Wilderman, M. Determan, and R.J. Peters A modular approach for facile biosynthesis of labdane-related diterpenes J. Am. Chem. Soc. 129 2007 6684 6685 (Pubitemid 46847494)
7. W. Gao, M.L. Hillwig, L. Huang, G. Cui, X. Wang, J. Kong, B. Yang, and R.J. Peters A functional genomics approach to tanshinone biosynthesis provides stereochemical insights Org. Lett. 11 2009 5170 5173
8. K. Hayashi, H. Kawaide, M. Notomi, Y. Sakigi, A. Matsuo, and H. Nozaki Identification and functional analysis of bifunctional ent-kaurene synthase from the moss Physcomitrella patens FEBS Lett. 580 2006 6175 6181 (Pubitemid 44666801)
9. D.M. Hershey, X. Lu, J. Zi, and R.J. Peters Functional conservation of the capacity for ent-kaurene biosynthesis and an associated operon in certain rhizobia J. Bact. 196 2014 100 106
10. M.L. Hillwig, M. Xu, T. Toyomasu, M.S. Tiernan, W. Gao, G. Cui, L. Huang, and R.J. Peters Domain loss has independently occurred multiple times in plant terpene synthase evolution Plant J. 68 2011 1051 1060
11. Y.J. Hong, and D.J. Tantillo Formation of beyerene, kaurene, trachylobane, and atiserene diterpenes by rearrangements that avoid secondary carbocations J Am Chem Soc 132 2010 5375 5386
12. H. Kawaide, K. Hayashi, R. Kawanabe, Y. Sakigi, A. Matsuo, M. Natsume, and H. Nozaki Identification of the single amino acid involved in quenching the ent-kauranyl cation by a water molecule in ent-kaurene synthase of Physcomitrella patens FEBS J. 278 2011 123 133
13. H. Kawaide, R. Imai, T. Sassa, and Y. Kamiya Ent-kaurene synthase from the fungus Phaeosphaeria sp. L487. cDNA isolation, characterization, and bacterial expression of a bifunctional diterpene cyclase in fungal gibberellin biosynthesis J. Biol. Chem. 272 1997 21706 21712 (Pubitemid 27382783)
14. J.D. Keasling, A. Mendoza, and P.S. Baran Synthesis: a constructive debate Nature 492 2012 188 189
15. C.I. Keeling, H.K. Dullat, M. Yuen, S.G. Ralph, S. Jancsik, and J. Bohlmann Identification and functional characterization of monofunctional ent-copalyl diphosphate and ent-kaurene synthases in white spruce reveal different patterns for diterpene synthase evolution for primary and secondary metabolism in gymnosperms Plant Physiol. 152 2010 1197 1208
16. M. Köksal, Y. Jin, R.M. Coates, R. Croteau, and D.W. Christianson Taxadiene synthase structure and evolution of modular architecture in terpene biosynthesis Nature 469 2011 116 120
17. D. Morrone, J. Chambers, L. Lowry, G. Kim, A. Anterola, K. Bender, and R.J. Peters Gibberellin biosynthesis in bacteria: separate ent-copalyl diphosphate and ent-kaurene synthases in Bradyrhizobium japonicum FEBS Lett. 583 2009 475 480
18. D. Morrone, L. Lowry, M.K. Determan, D.M. Hershey, M. Xu, and R.J. Peters Increasing diterpene yield with a modular metabolic engineering system in E. coli: comparison of MEV and MEP isoprenoid precursor pathway engineering Appl. Microbiol. Biotechnol. 85 2010 1893 1906
19. D. Morrone, M. Xu, D.B. Fulton, M.K. Determan, and R.J. Peters Increasing complexity of a diterpene synthase reaction with a single residue switch J. Am. Chem. Soc. 130 2008 5400 5401 (Pubitemid 351612929)
20. R.J. Peters Uncovering the complex metabolic network underlying diterpenoid phytoalexin biosynthesis in rice and other cereal crop plants Phytochemistry 67 2006 2307 2317 (Pubitemid 44527936)
21. R.J. Peters Two rings in them all: the labdane-related diterpenoids Nat. Prod. Rep. 27 2010 1521 1530
22. D.R. Robinson, and C.A. West Biosynthesis of cyclic diterpenes in extracts from seedlings of Ricinus communis L. I. Identification of diterpene hydrocarbons formed from mevalonate Biochemistry 9 1970 70 79
23. D.R. Robinson, and C.A. West Biosynthesis of cyclic diterpenes in extracts from seedlings of Ricinus communis L. II. Conversion of geranylgeranyl pyrophosphate into diterpene hydrocarbons and partial purification of the cyclization enzymes Biochemistry 9 1970 80 89
24. A. Roy, F.G. Roberts, P.R. Wilderman, K. Zhou, R.J. Peters, and R.M. Coates 16-Aza-ent-beyerane and 16-aza-ent-trachylobane: potent mechanism based inhibitors of recombinant ent-kaurene synthase from Arabidopsis thaliana J. Am. Chem. Soc. 129 2007 12453 12460 (Pubitemid 47598244)
25. C. Sallaud, C. Giacalone, R. Topfer, S. Goepfert, N. Bakaher, S. Rosti, and A. Tissier Characterization of two genes for the biosynthesis of the labdane diterpene Z-abienol in tobacco (Nicotiana tabacum) glandular trichomes Plant J. 72 2012 1 17
26. M. Schalk, L. Pastore, M.A. Mirata, S. Khim, M. Schouwey, F. Deguerry, V. Pineda, L. Rocci, and L. Daviet Towards a biosynthetic route to sclareol and amber odorants J. Am. Chem. Soc. 134 2012 18900 18903
27. Schmelz, E. A., Huffaker, A., Sims, J., Christensen, S., Lu, X., Okada, K., Peters, R. J., 2014. Biosynthesis, regulation and roles of monocot terpenoid phytoalexins. Plant J. PMID 24467826, in press. http://dx.doi.org/10.1186/1471- 2164-15-73
28. C.M. Spickett, K. Ponnamperuma, and C. Abell The resolution of diterpene cyclase activities from Ricinus communis Phytochemistry 37 1994 971 973 (Pubitemid 2162452)
29. K. Tamura, D. Peterson, N. Peterson, G. Stecher, M. Nei, and S. Kumar MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods Mol. Biol. Evol. 28 2011 2731 2739
30. T. Toyomasu, H. Kawaide, A. Ishizaki, S. Shinoda, M. Otsuka, W. Mitsuhashi, and T. Sassa Cloning of a full-length cDNA encoding ent-kaurene synthase from Gibberella fujikuroi: functional analysis of a bifunctional diterpene cyclase Biosci. Biotechnol. Biochem. 64 2000 660 664
31. P.R. Wilderman, and R.J. Peters A single residue switch converts abietadiene synthase into a pimaradiene specific cyclase J. Am. Chem. Soc. 129 2007 15736 15737
32. M. Xu, P.R. Wilderman, and R.J. Peters Following evolution's lead to a single residue switch for diterpene synthase product outcome Proc. Natl. Acad. Sci. USA 104 2007 7397 7401
33. P. Zerbe, B. Hamberger, M.M. Yuen, A. Chiang, H.K. Sandhu, L.L. Madilao, A. Nguyen, B. Hamberger, S.S. Bach, and J. Bohlmann Gene discovery of modular diterpene metabolism in nonmodel systems Plant Physiol. 162 2013 1073 1091
34. K. Zhou, and R.J. Peters Investigating the conservation pattern of a putative second terpene synthase divalent metal binding motif in plants Phytochemistry 70 2009 366 369
35. K. Zhou, and R.J. Peters Electrostatic effects on (di)terpene synthase product outcome Chem. Commun. 47 2011 4074 4080
36. K. Zhou, M. Xu, M.S. Tiernan, Q. Xie, T. Toyomasu, C. Sugawara, M. Oku, M. Usui, W. Mitsuhashi, M. Chono, P.M. Chandler, and R.J. Peters Functional characterization of wheat ent-kaurene(-like) synthases indicates continuing evolution of labdane-related diterpenoid metabolism in the cereals Phytochemistry 84 2012 47 55
37. Zi, J., Mafu, S., Peters, R. J., 2014. To gibberellins and beyond! Surveying the evolution of diterpenoid metabolism. Annu. Rev. Plant Biol. PMID 24471837, in press.
38. L. Zu, M. Xu, M.W. Lodewyk, D.E. Cane, R.J. Peters, and D.J. Tantillo Effect of isotopically sensitive branching on product distribution for pentalenene synthase: support for a mechanism predicted by quantum chemistry J. Am. Chem. Soc. 134 2012 11369 11371