The gymnosperm cytochrome P450 CYP750B1 catalyzes stereospecific monoterpene hydroxylation of (+)-sabinene in thujone biosynthesis in western redcedar

Plant Physiology

Volumn 168, Issue 1, 2015, Pages 94-106

  Gesell, Andreas ^a   Blaukopf, Markus ^b   Madilao, Lina ^a   Yuen, Macaire M S ^a   Withers, Stephen G ^b   Mattsson, Jim ^c   Russell, John H ^d   Bohlmann, Jörg ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^b UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^c SIMON FRASER UNIVERSITY   (Canada)

^d RESEARCH BRANCH   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

GYMNOSPERMAE; THUJA PLICATA; UNGULATA;

BETA-THUJONE; CARBANILAMIDE DERIVATIVE; CYTOCHROME P450; ISOPROTURON; MESSENGER RNA; NICOTINAMIDE ADENINE DINUCLEOTIDE; SABINENE; SABINOL; TERPENE; TISSUE EXTRACT;

BARK; BIOCATALYSIS; BIOSYNTHESIS; CHEMISTRY; ENZYME SPECIFICITY; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENETIC ASSOCIATION STUDY; GENETICS; HYDROXYLATION; METABOLISM; MOLECULAR GENETICS; PHYLOGENY; PLANT GENE; PLANT LEAF; STEREOISOMERISM; THUJA;

BIOCATALYSIS; BIOSYNTHETIC PATHWAYS; CYTOCHROME P-450 ENZYME SYSTEM; GENE EXPRESSION REGULATION, PLANT; GENES, PLANT; GENETIC ASSOCIATION STUDIES; HYDROXYLATION; MOLECULAR SEQUENCE DATA; MONOTERPENES; NAD; PHENYLUREA COMPOUNDS; PHYLOGENY; PLANT BARK; PLANT LEAVES; RNA, MESSENGER; STEREOISOMERISM; SUBSTRATE SPECIFICITY; TERPENES; THUJA; TISSUE EXTRACTS;

EID: 84929493482     PISSN: 00320889     EISSN: 15322548     Source Type: Journal    
DOI: 10.1104/pp.15.00315     Document Type: Article

References (54)

1. Aharoni A, Giri AP, Verstappen FWA, Bertea CM, Sevenier R, Sun Z, Jongsma MA, Schwab W, Bouwmeester HJ (2004) Gain and loss of fruit flavor compounds produced by wild and cultivated strawberry species. Plant Cell 16: 3110–3131
2. Anderson AB, Gripenberg J (1948) Antibiotic substances from the heart wood of Thuja plicata D. Don; the constitution of b-thujaplicin. Acta Chem Scand 2: 644–650
3. Birol I, Raymond A, Jackman SD, Pleasance S, Coope R, Taylor GA, Yuen MMS, Keeling CI, Brand D, Vandervalk BP, et al (2013) Assembling the 20 Gb white spruce (Picea glauca) genome from whole-genome shotgun sequencing data. Bioinformatics 29: 1492–1497
4. Burney OT, Jacobs DF (2011) Ungulate herbivory of regenerating conifers in relation to foliar nutrition and terpenoid production. For Ecol Manage 262: 1834–1845
5. Cankar K, van Houwelingen A, Goedbloed M, Renirie R, de Jong RM, Bouwmeester H, Bosch D, Sonke T, Beekwilder J (2014) Valencene oxidase CYP706M1 from Alaska cedar (Callitropsis nootkatensis). FEBS Lett 588: 1001–1007
6. 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: 212–229
7. Collu G, Unver N, Peltenburg-Looman AMG, van der Heijden R, Verpoorte R, Memelink J (2001) Geraniol 10-hydroxylase, a cytochrome P450 enzyme involved in terpenoid indole alkaloid biosynthesis. FEBS Lett 508: 215–220
8. Croteau R, Ketchum REB, Long RM, Kaspera R, Wildung MR (2006) Taxol biosynthesis and molecular genetics. Phytochem Rev 5: 75–97
9. De La Torre AR, Birol I, Bousquet J, Ingvarsson PK, Jansson S, Jones SJN, Keeling CI, MacKay J, Nilsson O, Ritland K, et al (2014) Insights into conifer giga-genomes. Plant Physiol 166: 1724–1732
10. Dehal SS, Croteau R (1987) Metabolism of monoterpenes: specificity of the dehydrogenases responsible for the biosynthesis of camphor, 3-thujone, and 3-isothujone. Arch Biochem Biophys 258: 287–291
11. Dess DB, Martin JC (1983) Readily accessible 12-I-5 oxidant for the conversion of primary and secondary alcohols to aldehydes and ketones. J Org Chem 48: 4155–4156
12. Foster AJ, Hall DE, Mortimer L, Abercromby S, Gries R, Gries G, Bohlmann J, Russell J, Mattsson J (2013) Identification of genes in Thuja plicata foliar terpenoid defenses. Plant Physiol 161: 1993–2004
13. Gardner JAF, Barton GM, MacLean H (1959) The polyoxyphenols of western red cedar (thuja plicata donn.). Can J Chem 37: 1703–1709
14. Garside P, Halsall TG, Hornby GM (1969) Action of peracetic acid on (+)-sabinol. J Chem Soc C 5: 716–721
15. Grabherr MG, Haas BJ, Yassour M, Levin JZ, Thompson DA, Amit I, Adiconis X, Fan L, Raychowdhury R, Zeng Q, et al (2011) Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat Biotechnol 29: 644–652
16. Hall DE, Robert JA, Keeling CI, Domanski D, Quesada AL, Jancsik S, Kuzyk MA, Hamberger B, Borchers CH, Bohlmann J (2011) An integrated genomic, proteomic and biochemical analysis of (+)-3-carene biosynthesis in Sitka spruce (Picea sitchensis) genotypes that are resistant or susceptible to white pine weevil. Plant J 65: 936–948
17. Hamann T, Møller BL (2007) Improved cloning and expression of cytochrome P450s and cytochrome P450 reductase in yeast. Protein Expr Purif 56: 121–127
18. Hamberger B, Bak S (2013) Plant P450s as versatile drivers for evolution of species-specific chemical diversity. Philos Trans R Soc Lond B Biol Sci 368: 20120426
19. Hamberger B, Ohnishi T, Hamberger B, Séguin 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: 1677–1695
20. Hebda RJ, Mathewes RW (1984) Holocene history of cedar and native Indian cultures of the north american pacific coast. Science 225: 711–713
21. Karp F, Croteau R (1982) Evidence that sabinene is an essential precursor of C(3)-oxygenated thujane monoterpenes. Arch Biochem Biophys 216: 616–624
22. Keeling CI, Bohlmann J (2006) Genes, enzymes and chemicals of terpenoid diversity in the constitutive and induced defence of conifers against insects and pathogens. New Phytol 170: 657–675
23. Kimball BA, Russell JH, Griffin DL, Johnston JJ (2005) Response factor considerations for the quantitative analysis of western redcedar (Thuja plicata) foliar monoterpenes. J Chromatogr Sci 43: 253–258
24. Kimball BA, Russell JH, Ott P (2012) Phytochemical variation within a single plant species influences foraging behavior of deer. Oikos 5: 743–751
25. Lohse M, Bolger AM, Nagel A, Fernie AR, Lunn JE, Stitt M, Usadel B (2012) RobiNA: a user-friendly, integrated software solution for RNASeq-based transcriptomics. Nucleic Acids Res 40: W622–W627
26. Lupien S, Karp F, Wildung M, Croteau R (1999) Regiospecific cytochrome P450 limonene hydroxylases from mint (Mentha) species: cDNA isolation, characterization, and functional expression of (-)-4S-limonene3-hydroxylase and (-)-4S-limonene-6-hydroxylase. Arch Biochem Biophys 368: 181–192
27. MacLean H, Murakami K (1966) Lignans of western red cedar (Thuja plicata Donn). V. Hydroxythujaplicatin methyl ether. Can J Chem 44: 1827–1830
28. Mamane V, Gress T, Krause H, Fürstner A (2004) Platinum- and goldcatalyzed cycloisomerization reactions of hydroxylated enynes. J Am Chem Soc. 126: 8654–8655
29. Morris PI, Stirling R (2012) Western red cedar extractives associated with durability in ground contact. Wood Sci Technol 46: 991–1002
30. Neale DB, Wegrzyn JL, Stevens KA, Zimin AV, Puiu D, Crepeau MW, Cardeno C, Koriabine M, Holtz-Morris AE, Liechty JD, et al (2014) Decoding the massive genome of loblolly pine using haploid DNA and novel assembly strategies. Genome Biol 15: R59
31. Nei M, Kumar S (2000) Molecular Evolution and Phylogenetics, Ed 1. Oxford University Press, New York, pp 1–333
32. Nelson DR (2006) Cytochrome P450 nomenclature, 2004. Methods Mol Biol 320: 1–10
33. Nystedt B, Street NR, Wetterbom A, Zuccolo A, Lin YC, Scofield DG, Vezzi F, Delhomme N, Giacomello S, Alexeyenko A, et al (2013) The Norway spruce genome sequence and conifer genome evolution. Nature 497: 579–584
34. Ohloff G, Uhde G, Thomas AF, Kováts Esz (1966) The absolute configuration of thujane. Tetrahedron 22: 309–320
35. Omura T, Sato R (1964) The carbon monoxide-binding pigment of liver microsomes. I. Evidence for its hemoprotein nature. J Biol Chem 239: 2370–2378
36. Pompon D, Louerat B, Bronine A, Urban P (1996) Yeast expression of animal and plant P450s in optimized redox environments. Methods Enzymol 272: 51–64
37. Ro DK, Arimura G, Lau SYW, 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: 8060–8065
38. Ro DK, Paradise EM, Ouellet M, Fisher KJ, Newman KL, Ndungu JM, Ho KA, Eachus RA, Ham TS, Kirby J, et al (2006) Production of the antimalarial drug precursor artemisinic acid in engineered yeast. Nature 440: 940–943
39. Roach CR, Hall DE, Zerbe P, Bohlmann J (2014) Plasticity and evolution of (+)-3-carene synthase and (-)-sabinene synthase functions of a sitka spruce monoterpene synthase gene family associated with weevil resistance. J Biol Chem 289: 23859–23869
40. Robineau T, Batard Y, Nedelkina S, Cabello-Hurtado F, LeRet M, Sorokine O, Didierjean L, Werck-Reichhart D (1998) The chemically inducible plant cytochrome P450 CYP76B1 actively metabolizes phenylureas and other xenobiotics. Plant Physiol 118: 1049–1056
41. Rontein D, Onillon S, Herbette G, Lesot A, Werck-Reichhart D, Sallaud C, Tissier A (2008) CYP725A4 from yew catalyzes complex structural rearrangement of taxa-4(5),11(12)-diene into the cyclic ether 5(12)-oxa-3 (11)-cyclotaxane. J Biol Chem 283: 6067–6075
42. Ruijter JM, Ramakers C, Hoogaars WMH, Karlen Y, Bakker O, van den Hoff MJB, Moorman AF (2009) Amplification efficiency: linking baseline and bias in the analysis of quantitative PCR data. Nucleic Acids Res 37: e45
43. Russell JH, Ferguson CF (2008) Preliminary results from five generations of a western redcedar (Thuja plicata) selection study with self mating. Tree Genet Genomes 4: 509–518
44. Russell JH, Yanchuk AD (2012) Breeding for growth improvement and resistance to multiple pests in Thuja plicata. Gen Tech Rep 240: 40–44
45. Sirisoma NS, Höld KM, Casida JE (2001) alpha- and beta-Thujones (herbal medicines and food additives): synthesis and analysis of hydroxy and dehydro metabolites. J Agric Food Chem 49: 1915–1921
46. Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol Biol Evol 24: 1596–1599
47. Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22: 4673–4680
48. Tisserand R, Young R (2014) Essential Oil Safety, Ed 2. Churchill Livingstone, London, pp 1–784
49. Tsiri D, Graikou K, Pobłocka-Olech L, Krauze-Baranowska M, Spyropoulos C, Chinou I (2009) Chemosystematic value of the essential oil composition of Thuja species cultivated in Poland-antimicrobial activity. Molecules 14: 4707–4715
50. Umbreit MA, Sharpless KB (1977) Allylic oxidation of olefins by catalytic and stoichiometric Selenium dioxide with tert-Butyl hydroperoxide. J Am Chem Soc 99: 5526–5528
51. Von Rudloff E, Lapp MS, Yeh FC (1988) Chemosystematic study of Thuja plicata: multivariate analysis of leaf oil terpene composition. Biochem Syst Ecol 16: 119–125
52. Vourc’h G, Russell J, Martin JL (2002) Linking deer browsing and terpene production among genetic identities in Chamaecyparis nootkatensis and Thuja plicata (Cupressaceae). J Hered 93: 370–376
53. Vourc’h G, Martin JL, Duncan P, Escarré J, Clausen TP (2001) Defensive adaptations of Thuja plicata to ungulate browsing: a comparative study between mainland and island populations. Oecologia 126: 84–93
54. Zifkin M, Jin A, Ozga JA, Zaharia LI, Schernthaner JP, Gesell A, Abrams SR, Kennedy JA, Constabel CP (2012) Gene expression and metabolite profiling of developing highbush blueberry fruit indicates transcriptional regulation of flavonoid metabolism and activation of abscisic acid metabolism. Plant Physiol 158: 200–224