To gibberellins and beyond! Surveying the evolution of (Di)terpenoid metabolism

Annual Review of Plant Biology

Volumn 65, Issue , 2014, Pages 259-286

  Zi, Jiachen ^a   Mafu, Sibongile ^a   Peters, Reuben J ^a  

^a IOWA STATE UNIVERSITY   (United States)

Author keywords

allelochemicals; biosynthesis; cytochrome P450; phytoalexins; terpene synthases

Indexed keywords

DITERPENE; GERANYLGERANYL PYROPHOSPHATE; GIBBERELLIN; ISOPRENOID PHOSPHATE; TRANSFERASE;

ENZYMOLOGY; EVOLUTION; GENETICS; METABOLISM; MULTIGENE FAMILY; PHYLOGENY; PLANT; REVIEW;

ALKYL AND ARYL TRANSFERASES; BIOLOGICAL EVOLUTION; DITERPENES; GIBBERELLINS; MULTIGENE FAMILY; PHYLOGENY; PLANTS; POLYISOPRENYL PHOSPHATES;

EID: 84899764072     PISSN: 15435008     EISSN: 15452123     Source Type: Book Series    
DOI: 10.1146/annurev-arplant-050213-035705     Document Type: Review

References (131)

1. Akhtar TA, Matsuba Y, Schauvinhold I, Yu G, Lees HA, et al. 2013. The tomato cis-prenyltransferase gene family. Plant J. 73:640-52
2. Anterola A, Shanle E, Mansouri K, Schuette S, Renzaglia K. 2009. Gibberellin precursor is involved in spore germination in the moss Physcomitrella patens. Planta 229:1003-7
3. Banks JA, Nishiyama T, Hasebe M, Bowman JL, Gribskov M, et al. 2011. The Selaginella genome identifies genetic changes associated with the evolution of vascular plants. Science 332:960-63
4. Bensen RJ, Johal GS, Crane VC, Tossberg JT, Schnable PS, et al. 1995. Cloning and characterization of the maize An1 gene. Plant Cell 7:75-84
5. Bomke C, Tudzynski B. 2009. Diversity, regulation, and evolution of the gibberellin biosynthetic pathway in fungi compared to plants and bacteria. Phytochemistry 70:1876-93
6. Caniard A, Zerbe P, Legrand S, Cohade A, Valot N, et al. 2012. Discovery and functional characterization of two diterpene synthases for sclareol biosynthesis in Salvia sclarea (L.) and their relevance for perfume manufacture. BMC Plant Biol. 12:119
7. Cao R, Zhang Y, Mann FM, Huang C, Mukkamala D, et al. 2010. Diterpene cyclases and the nature of the isoprene fold. Proteins 78:2417-32
8. Cartwright DW, Langcake P, Pryce RJ, Leworthy DP, Ride JP. 1977. Chemical activation of host defence mechanisms as a basis for crop protection. Nature 267:511-13
9. Cartwright DW, Langcake P, Pryce RJ, Leworthy DP, Ride JP. 1981. Isolation and characterization of two phytoalexins from rice as momilactones A and B. Phytochemistry 20:535-37
10. Chen F, Tholl D, Bohlmann J, Pichersky E. 2011. 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. 66:212-29
11. Christianson DW. 2006. Structural biology and chemistry of the terpenoid cyclases. Chem. Rev. 106:3412-42
12. Christianson DW. 2008. Unearthing the roots of the terpenome. Curr. Opin. Chem. Biol. 12:141-50
13. Criswell J, Potter K, Shephard F, Beale MB, Peters RJ. 2012. A single residue change leads to a hydroxylated product from the class II diterpene cyclization catalyzed by abietadiene synthase. Org. Lett. 14:5828-31
14. Degenhardt J, Kollner TG, Gershenzon J. 2009. Monoterpene and sesquiterpene synthases and the origin of terpene skeletal diversity in plants. Phytochemistry 70:1621-37
15. Falara V, Pichersky E, Kanellis AK. 2010. A copal-8-ol diphosphate synthase from the angiosperm Cistus creticus subsp. creticus is a putative key enzyme for the formation of pharmacologically active, oxygencontaining labdane-type diterpenes. Plant Physiol. 154:301-10
16. Gao W, Hillwig ML, Huang L, Cui G, Wang X, et al. 2009. A functional genomics approach to tanshinone biosynthesis provides stereochemical insights. Org. Lett. 11:5170-73
17. Gao Y, Honzatko RB, Peters RJ. 2012. Terpenoid synthase structures: a so far incomplete view of complex catalysis. Nat. Prod. Rep. 29:1153-75
18. Guerra-Bubb J, Croteau R, Williams RM. 2012. The early stages of taxol biosynthesis: an interim report on the synthesis and identification of early pathway metabolites. Nat. Prod. Rep. 29:683-96
19. Gunnewich N, Higashi Y, Feng X, Choi KB, Schmidt J, Kutchan TM. 2012. A diterpene synthase from the clary sage Salvia sclarea catalyzes the cyclization of geranylgeranyl diphosphate to (8R)-hydroxycopalyl diphosphate. Phytochemistry 91:93-99
20. Guo J, Zhou YJ, Hillwig ML, Shen Y, Yang L, et al. 2013. CYP76AH1 catalyzes turnover of miltiradiene in tanshinones biosynthesis and enables heterologous production of ferruginol in yeasts. Proc. Natl. Acad. Sci. USA 110:12108-13
21. Hall DE, Zerbe P, Jancsik S, Quesada AL, Dullat H, et al. 2013. Evolution of conifer diterpene synthases: diterpene resin acid biosynthesis in lodgepole pine and jack pine involves monofunctional and bifunctional diterpene synthases. Plant Physiol. 161:600-16
22. Hamberger B, Bak S. 2013. Plant P450s as versatile drivers for evolution of species-specific chemical diversity. Philos. Trans. R. Soc. B 368:20120426
23. Hamberger B, Ohnishi T, Seguin A, Bohlmann J. 2011. Evolution of diterpene metabolism: Sitka spruce CYP720B4 catalyzes multiple oxidations in resin acid biosynthesis of conifer defense against insects. Plant Physiol. 157:1677-95
24. Harris LJ, Saparno A, Johnston A, Prisic S, Xu M, et al. 2005. Themaize An2 gene is induced by Fusarium attack and encodes an ent-copalyl diphosphate synthase. Plant Mol. Biol. 59:881-94
25. Hasegawa M, Mitsuhara I, Seo S, Imai T, Koga J, et al. 2010. Phytoalexin accumulation in the interaction between rice and the blast fungus. Mol. Plant-Microbe Interact. 23:1000-11
26. Hayashi K, Horie K, Hiwatashi Y, Kawaide H, Yamaguchi S, et al. 2010. Endogenous diterpenes derived from ent-kaurene, a common gibberellin precursor, regulate protonema differentiation of the moss Physcomitrella patens. Plant Physiol. 153:1085-97
27. Hayashi K, Kawaide H, Notomi M, Sakigi Y, Matsuo A, Nozaki H. 2006. Identification and functional analysis of bifunctional ent-kaurene synthase from themoss Physcomitrella patens. FEBS Lett. 580:6175-81
28. Hedden P, Thomas SG. 2012. Gibberellin biosynthesis and its regulation. Biochem. J. 444:11-25
29. Helliwell CA, Chandler PM, Poole A, Dennis ES, Peacock WJ. 2001. The CYP88A cytochrome P450, ent-kaurenoic acid oxidase, catalyzes three steps of the gibberellin biosynthesis pathway. Proc. Natl. Acad. Sci. USA 98:2065-70
30. Helliwell CA, Poole A, Peacock WJ, Dennis ES. 1999. Arabidposis ent-kaurene oxidase catalyzes three steps of gibberellin biosynthesis. Plant Physiol. 119:507-10
31. Helliwell CA, Sullivan JA, Mould RM, Gray JC, Peacock WJ, Dennis ES. 2001. A plastid envelope location of Arabidopsis ent-kaurene oxidase links the plastid and endoplasmic reticulum steps of the gibberellin biosynthesis pathway. Plant J. 28:201-8
32. Herde M, Gartner K, Kollner TG, Fode B, Boland W, et al. 2008. Identification and regulation of TPS04/GES, an Arabidopsis geranyllinalool synthase catalyzing the first step in the formation of the insect-induced volatile C16-homoterpene TMTT. Plant Cell 20:1152-68
33. Hillwig ML, Xu M, Toyomasu T, Tiernan MS, Gao W, et al. 2011. Domain loss has independently occurred multiple times in plant terpene synthase evolution. Plant J. 68:1051-60
34. Hirano K, Nakajima M, Asano K, Nishiyama T, Sakakibara H, et al. 2007. The GID1-mediated gibberellin perception mechanism is conserved in the lycophyte Selaginella moellendorffii but not in the bryophyte Physcomitrella patens. Plant Cell 19:3058-79
35. Iijima Y, Gang DR, Fridman E, Lewinsohn E, Pichersky E. 2004. Characterization of geraniol synthase from the peltate glands of sweet basil. Plant Physiol. 134:370-79
36. Itoh H, Tatsumi T, Sakamoto T, Otomo K, Toyomasu T, et al. 2004. A rice semi-dwarf gene, Tan-Ginbozu (D35), encodes the gibberellin biosynthesis enzyme, ent-kaurene oxidase. Plant Mol. Biol. 54:533-47
37. Kanno Y, Otomo K, Kenmoku H, Mitsuhashi W, Yamane H, et al. 2006. Characterization of a rice gene family encoding type-A diterpene cyclases. Biosci. Biotechnol. Biochem. 70:1702-10
38. Kato T, Kabuto C, Sasaki N, Tsunagawa M, Aizawa H, et al. 1973. Momilactones, growth inhibitors from rice, Oryza sativa L. Tetrahedron Lett. 14:3861-64
39. Kato-Noguchi H, Peters RJ. 2013. The role ofmomilactones in rice allelopathy. J. Chem. Ecol. 39:175-85
40. Kawaide H, Hayashi K, Kawanabe R, Sakigi Y, Matsuo A, et al. 2011. 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. 278:123-33
41. Keeling CI, Bohlmann J. 2006. Diterpene resin acids in conifers. Phytochemistry 67:2415-23
42. Keeling CI, Dullat HK, Yuen M, Ralph SG, Jancsik S, Bohlmann J. 2010. 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. 152:1197-208
43. Keeling CI, Weisshaar S, Ralph SG, Jancsik S, Hamberger B, et al. 2011. Transcriptome mining, functional characterization, and phylogeny of a large terpene synthase gene family in spruce (Picea spp.). BMC Plant Biol. 11:43
44. Kirby J, Nishimoto M, Park JG, Withers ST, Nowroozi F, et al. 2010. Cloning of casbene and neocembrene synthases from Euphorbiaceae plants and expression in Saccharomyces cerevisiae. Phytochemistry 71:1466-73
45. Li G, Kollner TG, Yin Y, Jiang Y, Chen H, et al. 2012. Nonseed plant Selaginella moellendorffii has both seed plant and microbial types of terpene synthases. Proc. Natl. Acad. Sci. USA 109:14711-15
46. Lipinski CA, Lombardo F, Dominy BW, Feeney PJ. 1997. Experimental and computational approaches to estimate solubility and permeability in drug discovery and development settings. Adv. Drug Deliv. Rev. 23:3-25
47. Mafu S, Hillwig ML, Peters RJ. 2011. A novel labda-7,13E-dien-15-ol- producing bifunctional diterpene synthase from Selaginella moellendorffii. Chem Bio Chem 12:1984-87
48. Magome H, Nomura T, Hanada A, Takeda-Kamiya N, Ohnishi T, et al. 2013. CYP714B1 and CYP714B2 encode gibberellin 13-oxidases that reduce gibberellin activity in rice. Proc. Natl. Acad. Sci. USA 110:1947-52
49. 2+-dependent inhibition characterizes plant class II diterpene cyclases from primary and secondary metabolism. J. Biol. Chem. 285:20558-63
50. Martin DM, Faldt J, Bohlmann J. 2004. Functional characterization of nine Norway spruce TPS genes and evolution of gymnosperm terpene synthases of the TPS-d subfamily. Plant Physiol. 135:1908-27
51. Mau CJD, West CA. 1994. Cloning of casbene synthase cDNA: evidence for conserved structural features among terpenoid cyclases in plants. Proc. Natl. Acad. Sci. USA 91:8497-501
52. Miyazaki S, Katsumata T, Natsume M, Kawaide H. 2011. The CYP701B1 of Physcomitrella patens is an ent-kaurene oxidase that resists inhibition by uniconazole-P. FEBS Lett. 585:1879-83
53. Morrone D, Chambers J, Lowry L, Kim G, Anterola A, et al. 2009. Gibberellin biosynthesis in bacteria: separate ent-copalyl diphosphate and ent-kaurene synthases in Bradyrhizobium japonicum. FEBS Lett. 583:475-80
54. Morrone D, Chen X, Coates RM, Peters RJ. 2010. Characterization of the kaurene oxidase CYP701A3, a multifunctional cytochrome P450 from gibberellin biosynthesis. Biochem. J. 431:337-44
55. Morrone D, Hillwig ML, Mead ME, Lowry L, Fulton DB, Peters RJ. 2011. Evident and latent plasticity across the rice diterpene synthase family with potential implications for the evolution of diterpenoid metabolism in the cereals. Biochem. J. 435:589-95
56. Morrone D, Jin Y, Xu M, Choi S-Y, Coates RM, Peters RJ. 2006. An unexpected diterpene cyclase from rice: functional identification of a stemodene synthase. Arch. Biochem. Biophys. 448:133-40
57. Morrone D, Xu M, Fulton DB, Determan MK, Peters RJ. 2008. Increasing complexity of a diterpene synthase reaction with a single residue switch. J. Am. Chem. Soc. 130:5400-1
58. Nelson D, Werck-Reichhart D. 2011. A P450-centric view of plant evolution. Plant J. 66:194-211
59. Nualkaew N, De-Eknamkul W, Kutchan TM, Zenk MH. 2006. Membrane-bound geranylgeranyl diphosphate phosphatases: purification and characterization from Croton stellatopilosus leaves. Phytochemistry 67:1613-20
60. Nualkaew N, Guennewich N, Springob K, Klamrak A, De-Eknamkul W, Kutchan TM. 2013. Molecular cloning and catalytic activity of a membrane-bound prenyl diphosphate phosphatase from Croton stellatopilosus Ohba. Phytochemistry 91:140-47
61. Oldfield E, Lin FY. 2012. Terpene biosynthesis: modularity rules. Angew. Chem. Int. Ed. 51:1124-37
62. Ortiz de Montellano PR. 2010. Hydrocarbon hydroxylation by cytochrome P450 enzymes. Chem. Rev. 110:932-48
63. Osbourn A. 2010. Gene clusters for secondary metabolic pathways: an emerging theme in plant biology. Plant Physiol. 154:531-35
64. Peters RJ. 2006. Uncovering the complexmetabolic network underlying diterpenoid phytoalexin biosynthesis in rice and other cereal crop plants. Phytochemistry 67:2307-17
65. Peters RJ. 2010. Two rings in them all: the labdane-related diterpenoids. Nat. Prod. Rep. 27:1521-30
66. Peters RJ. 2013. Gibberellin phytohormone metabolism. In Isoprenoid Synthesis in Plants and Microorganisms: New Concepts and Experimental Approaches, ed. T Bach, M Rohmer, pp. 233-49. New York: Springer
67. Peters RJ, Carter OA, Zhang Y, Matthews BW, Croteau RB. 2003. Bifunctional abietadiene synthase: mutual structural dependence of the active sites for protonation-initiated and ionization-initiated cyclizations. Biochemistry 42:2700-7
68. Peters RJ, Croteau RB. 2002. Abietadiene synthase catalysis: conserved residues involved in protonationinitiated cyclization of geranylgeranyl diphosphate to (+)-copalyl diphosphate. Biochemistry 41:1836-42
69. Peters RJ, Croteau RB. 2002. Abietadiene synthase catalysis: mutational analysis of a prenyl diphosphate ionization-initiated cyclization and rearrangement. Proc. Natl. Acad. Sci. USA 99:580-84
70. Peters RJ, Flory JE, Jetter R, Ravn MM, Lee H-J, et al. 2000. Abietadiene synthase from grand fir (Abies grandis): characterization and mechanism of action of the "pseudomature" recombinant enzyme. Biochemistry 39:15592-602
71. Peters RJ, Ravn MM, Coates RM, Croteau RB. 2001. Bifunctional abietadiene synthase: free diffusive transfer of the (+)-copalyl diphosphate intermediate between two distinct active sites. J. Am. Chem. Soc. 123:8974-78
72. Prisic S, Peters RJ. 2007. Synergistic substrate inhibition of ent-copalyl diphosphate synthase: a potential feed-forward inhibition mechanism limiting gibberellin metabolism. Plant Physiol. 144:445-54
73. Prisic S, Xu J, Coates RM, Peters RJ. 2007. Probing the role of the DXDD motif in class II diterpene cyclases. Chem Bio Chem 8:869-74
74. Prisic S, Xu M, Wilderman PR, Peters RJ. 2004. Rice contains two disparate ent-copalyl diphosphate synthases with distinct metabolic functions. Plant Physiol. 136:4228-36
75. Ravn MM, Coates RM, Flory J, Peters RJ, Croteau R. 2000. Stereochemistry of the cyclization rearrangement of (+)-copalyl diphosphate to (-)-abietadiene catalyzed by recombinant abietadiene synthase from Abies grandis. Org. Lett. 2:573-76
76. Ravn MM, Coates RM, Jetter R, Croteau R. 1998. Stereospecific intramolecular proton transfer in the cyclization of geranylgeranyl diphosphate to (-)-abietadiene catalyzed recombinant cyclase from grand fir (Abies grandis). Chem. Commun. 1998:21-22
77. N2 displacement of diethyl phosphate. Eur. J. Org. Chem. 2000:1401-10
78. Ravn MM, Peters RJ, Coates RM, Croteau RB. 2002. Specificity and mechanism of abietadiene synthase catalysis: stereochemistry and stabilization of the cryptic pimarenyl carbocation intermediate. J. Am. Chem. Soc. 124:6998-7006
79. Rensing SA, Lang D, Zimmer AD, Terry A, Salamov A, et al. 2008. The Physcomitrella genome reveals evolutionary insights into the conquest of land by plants. Science 319:64-69
80. Ro DK, Arimura G, Lau SY, Piers E, Bohlmann J. 2005. Loblolly pine abietadienol/abietadienal oxidase PtAO (CYP720B1) is a multifunctional, multisubstrate cytochrome P450 monooxygenase. Proc. Natl. Acad. Sci. USA 102:8060-65
81. Ro DK, Bohlmann J. 2006. Diterpene resin acid biosynthesis in loblolly pine (Pinus taeda): functional characterization of abietadiene/levopimaradiene synthase (PtTPS-LAS) cDNAand subcellular targeting of PtTPS-LAS and abietadienol/abietadienal oxidase (Pt AO, CYP720B1). Phytochemistry 67:1572-78
82. Roy A, Roberts FG, Wilderman PR, Zhou K, Peters RJ, Coates RM. 2007. 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. 129:12453-60
83. Sakamoto T, Miura K, Itoh H, Tatsumi T, Ueguchi-Tanaka M, et al. 2004. An overview of gibberellin metabolism enzyme genes and their related mutants in rice. Plant Physiol. 134:1642-53
84. Sallaud C, Giacalone C, Töpfer R, Goepfert S, Bakaher N, et al. 2012. Characterization of two genes for the biosynthesis of the labdane diterpene Z-abienol in tobacco (Nicotiana tabacum) glandular trichomes. Plant J. 72:1-17
85. Schalk M, Pastore L, Mirata MA, Khim S, Schouwey M, et al. 2012. Towards a biosynthetic route to sclareol and amber odorants. J. Am. Chem. Soc. 134:18900-3
86. Schepmann HG, Pang J, Matsuda SP. 2001. Cloning and characterization of Ginkgo biloba levopimaradiene synthase, which catalyzes the first committed step in ginkolide biosynthesis. Arch. Biochem. Biophys. 392:263-69
87. Schmelz EA, Kaplan F, Huffaker A, Dafoe NJ, Vaughan MM, et al. 2011. Identity, regulation, and activity of inducible diterpenoid phytoalexins in maize. Proc. Natl. Acad. Sci. USA 108:5455-60
88. Schnable PS, Ware D, Fulton RS, Stein JC, Wei F, et al. 2009. The B73 maize genome: complexity, diversity, and dynamics. Science 326:1112-15
89. Seki H, Ohyama K, Sawai S, Mizutani M, Ohnishi T, et al. 2008. Licorice β-amyrin 11-oxidase, a cytochrome P450 with a key role in the biosynthesis of the triterpene sweetener glycyrrhizin. Proc. Natl. Acad. Sci. USA 105:14204-9
90. Shimura K, Okada A, Okada K, Jikumaru Y, Ko K-W, et al. 2007. Identification of a biosynthetic gene cluster in rice for momilactones. J. Biol. Chem. 282:34013-18
91. Silverstone AL, Chang C-W, Krol E, Sun T-P. 1997. Developmental regulation of the gibberellin biosynthetic gene GA1 in Arabidopsis thaliana. Plant J. 12:9-19
92. Smanski MJ, Peterson RM, Huang SX, Shen B. 2012. Bacterial diterpene synthases: new opportunities for mechanistic enzymology and engineered biosynthesis. Curr. Opin. Chem. Biol. 16:132-41
93. Starks CM, Back K, Chappell J, Noel JP. 1997. Structural basis for cyclic terpene biosynthesis by tobacco 5-epi-aristolochene synthase. Science 277:1815-20
94. Stofer Vogel B, Wildung MR, Vogel G, Croteau R. 1996. Abietadiene synthase from grand fir (Abies grandis). J. Biol. Chem. 271:23262-68
95. 13C labeling and multidimensional NMR analysis of miltiradiene synthesized by bifunctional diterpene cyclase in Selaginella moellendorffii. J. Biol. Chem. 286:42840-47
96. Sun TP. 2011. The molecular mechanism and evolution of the GA-GID1-DELLA signaling module in plants. Curr. Biol. 21:R338-45
97. Sun TP, Kamiya Y. 1994. The Arabidopsis GA1 locus encodes the cyclase ent-kaurene synthetase A of gibberellin biosynthesis. Plant Cell 6:1509-18
98. Swaminathan S, Morrone D, Wang Q, Fulton DB, Peters RJ. 2009. CYP76M7 is an ent-cassadiene C11α-hydroxylase defining a second multifunctional diterpenoid biosynthetic gene cluster in rice. Plant Cell 21:3315-25
99. Takos AM, Rook F. 2012. Why biosynthetic genes for chemical defense compounds cluster. Trends Plant Sci. 17:383-88
100. Toyomasu T. 2008. Recent advances regarding diterpene cyclase genes in higher plants and fungi. Biosci. Biotechnol. Biochem. 72:1168-75
101. Toyomasu T, Usui M, Sugawara C, Otomo K, Hirose Y, et al. 2014. Reverse-genetic approach to verify physiological roles of rice phytoalexins: characterization of a knockdown mutant of OsCPS4 phytoalexin biosynthetic gene in rice. Physiol. Plant. 150:55-62
102. Vandermoten S, Haubruge E, Cusson M. 2009. New insights into short-chain prenyltransferases: structural features, evolutionary history and potential for selective inhibition. Cell. Mol. Life Sci. 66:3685-95
103. Vaughan MM, Wang Q, Webster FX, Kiemle D, Hong YJ, et al. 2013. Formation of the unusual semivolatile diterpene rhizathalene by the Arabidopsis class I terpene synthase TPS08 in the root stele is involved in defense against belowground herbivory. Plant Cell 25:1108-25
104. Vranova E, Coman D, Gruissem W. 2013. Network analysis of the MVA and MEP pathways for isoprenoid synthesis. Annu. Rev. Plant Biol. 64:665-700
105. Walker K, Croteau R. 2001. Taxol biosynthetic genes. Phytochemistry 58:1-7
106. Wang E, Wagner GJ. 2003. Elucidation of the functions of genes central to diterpene metabolism in tobacco trichomes using posttranscriptional gene silencing. Planta 216:686-91
107. Wang E, Wang R, DeParasis J, Loughrin JH, Gan S, Wagner GJ. 2001. Suppression of a P450 hydroxylase gene in plant trichome glands enhances natural-product-based aphid resistance. Nat. Biotechnol. 19:371-74
108. Wang Q, Hillwig ML, Okada K, Yamazaki K, Wu Y, et al. 2012. Characterization of CYP76M5-8 indicates metabolic plasticity within a plant biosynthetic gene cluster. J. Biol. Chem. 287:6159-68
109. Wang Q, Hillwig ML, Peters RJ. 2011. CYP99A3: functional identification of a diterpene oxidase from the momilactone biosynthetic gene cluster in rice. Plant J. 65:87-95
110. Wang Q, Hillwig ML, Wu Y, Peters RJ. 2012. CYP701A8: a rice ent-kaurene oxidase paralog diverted to more specialized diterpenoid metabolism. Plant Physiol. 158:1418-25
111. Wegel E, Koumproglou R, Shaw P, Osbourn A. 2009. Cell type-specific chromatin decondensation of a metabolic gene cluster in oats. Plant Cell 21:3926-36
112. Wilderman PR, Peters RJ. 2007. A single residue switch converts abietadiene synthase into a pimaradiene specific cyclase. J. Am. Chem. Soc. 129:15736-37
113. Wilderman PR, Xu M, Jin Y, Coates RM, Peters RJ. 2004. Identification of syn-pimara-7,15-diene synthase reveals functional clustering of terpene synthases involved in rice phytoalexin/allelochemical biosynthesis. Plant Physiol. 135:2098-105
114. Wildung MR, Croteau RB. 1996. A cDNA clone for taxadiene synthase, the diterpene cyclase that catalyzes the committed step of taxol biosynthesis. J. Biol. Chem. 271:9201-4
115. Wu Y, Hillwig ML, Wang Q, Peters RJ. 2011. Parsing a multifunctional biosynthetic gene cluster from rice: biochemical characterization of CYP71Z6 & 7. FEBS Lett. 585:3446-51
116. Wu Y, Wang Q, Hillwig ML, Peters RJ. 2013. Picking sides: distinct roles for CYP76M6 and-8 in rice oryzalexin biosynthesis. Biochem. J. 454:209-16
117. Wu Y, Zhou K, Toyomasu T, Sugawara C, Oku M, et al. 2012. Functional characterization of wheat copalyl diphosphate synthases elucidates the early evolution of labdane-related diterpenoid metabolism in the cereals. Phytochemistry 84:40-46
118. Xu M, Galhano R, Wiemann P, Bueno E, Tiernan M, et al. 2012. Genetic evidence for natural productmediated plant-plant allelopathy in rice (Oryza sativa). New Phytol. 193:570-75
119. Xu M, Wilderman PR, Morrone D, Xu J, Roy A, et al. 2007. Functional characterization of the rice kaurene synthase-like gene family. Phytochemistry 68:312-26
120. Xu M, Wilderman PR, Peters RJ. 2007. Following evolution's lead to a single residue switch for diterpene synthase product outcome. Proc. Natl. Acad. Sci. USA 104:7397-401
121. Yamaguchi S. 2008. Gibberellin metabolism and its regulation. Annu. Rev. Plant Biol. 59:225-51
122. Yamaguchi S, Saito T, Abe H, Yamane H, Murofushi N, Kamiya Y. 1996. Molecular cloning and characterization of a cDNA encoding the gibberellin biosynthetic enzyme ent-kaurene synthase B from pumpkin (Cucurbita maxima L.). Plant J. 10:101-11
123. Yamane H. 2013. Biosynthesis of phytoalexins and regulatory mechanisms of it in rice. Biosci. Biotechnol. Biochem. 77:1141-48
124. Yasumura Y, Crumpton-Taylor M, Fuentes S, Harberd NP. 2007. Step-by-step acquisition of the gibberellin-DELLA growth-regulatory mechanism during land-plant evolution. Curr. Biol. 17:1225-30
125. Zerbe P, Chiang A, Yuen M, Hamberger B, Draper JA, et al. 2012. Bifunctional cis-abienol synthase from Abies balsamea discovered by transcriptome sequencing and its implications for diterpenoid fragrance production. J. Biol. Chem. 287:12121-31
126. Zhang Y, Zhang B, Yan D, Dong W, Yang W, et al. 2011. Two Arabidopsis cytochrome P450 monooxygenases, CYP714A1 and CYP714A2, function redundantly in plant development through gibberellin deactivation. Plant J. 67:342-53
127. Zhou K, Gao Y, Hoy JA, Mann FM, Honzatko RB, Peters RJ. 2012. Insights into diterpene cyclization from the structure of the bifunctional abietadiene synthase. J. Biol. Chem. 287:6840-50
128. Zhou K, Peters RJ. 2011. Electrostatic effects on (di)terpene synthase product outcome. Chem. Commun. 47:4074-80
129. Zhou K, Xu M, Tiernan MS, Xie Q, Toyomasu T, et al. 2012. Functional characterization of wheat ent-kaurene(-like) synthases indicates continuing evolution of labdane-related diterpenoid metabolism in the cereals. Phytochemistry 84:47-55
130. Zhu Y, Nomura T, Xu Y, Zhang Y, Peng Y, et al. 2006. ELONGATED UPPERMOST INTERNODE encodes a cytochrome P450 monooxygenase that epoxidizes gibberellins in a novel deactivation reaction in rice. Plant Cell 18:442-56
131. Zi J, Peters RJ. 2013. Characterization of CYP76AH4 clarifies phenolic diterpenoid biosynthesis in the Lamiaceae. Org. Biomol. Chem. 11:7650-53