The hexanoyl-CoA precursor for cannabinoid biosynthesis is formed by an acyl-activating enzyme in Cannabis sativa trichomes

Plant Journal

Volumn 71, Issue 3, 2012, Pages 353-365

  Stout, Jake M ^a,b   Boubakir, Zakia ^a,b   Ambrose, Stephen J ^a   Purves, Randy W ^a   Page, Jonathan E ^a,b  

^a NATIONAL RESEARCH COUNCIL CANADA   (Canada)

^b UNIVERSITY OF SASKATCHEWAN   (Canada)

Author keywords

acyl activating enzyme; acyl CoA; cannabinoid; Cannabis sativa; hexanoate; marijuana

Indexed keywords

ACYL-COA; CANNABINOID; CANNABIS SATIVA; HEXANOATE; MARIJUANA;

BIOCHEMISTRY; CELLS; CYTOLOGY; ENCODING (SYMBOLS); HEMP; OXYGENATION; UNSATURATED FATTY ACIDS;

ENZYMES;

ACYL COENZYME A; CANNABINOID; CANNABIS; HEXANOIC ACID; HEXANOIC ACID DERIVATIVE; HEXANOYL COENZYME A; HEXANOYL-COENZYME A; LONG CHAIN FATTY ACID COENZYME A LIGASE; TRANSCRIPTOME; VEGETABLE PROTEIN;

AMINO ACID SEQUENCE; ANTIBODY SPECIFICITY; ARTICLE; BIOSYNTHESIS; CHEMISTRY; CYTOPLASM; ENZYMOLOGY; FLOWER; GENE LIBRARY; GENETICS; KINETICS; METABOLISM; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PEROXISOME; PHYLOGENY; PLANT LEAF; PLANT ROOT; PLANT STEM; SEQUENCE ALIGNMENT;

ACYL COENZYME A; AMINO ACID SEQUENCE; BASE SEQUENCE; CANNABINOIDS; CANNABIS; CAPROATES; COENZYME A LIGASES; CYTOPLASM; FLOWERS; GENE LIBRARY; KINETICS; MOLECULAR SEQUENCE DATA; ORGAN SPECIFICITY; PEROXISOMES; PHYLOGENY; PLANT LEAVES; PLANT PROTEINS; PLANT ROOTS; PLANT STEMS; SEQUENCE ALIGNMENT; TRANSCRIPTOME;

CANNABIS; CANNABIS SATIVA;

EID: 84864419262     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/j.1365-313X.2012.04949.x     Document Type: Article

References (55)

1. Austin, M.B., Saito, T., Bowman, M.E., Haydock, S., Kato, A., Moore, B.S., Kay, R.R., and, Noel, J.P., (2006) Biosynthesis of Dictyostelium discoideum differentiation-inducing factor by a hybrid type I fatty acid-type III polyketide synthase. Nature Chem. Biol. 2, 494-502.
2. van Bakel, H., Stout, J.M., Cote, A.G., Tallon, C., Sharpe, A.G., Hughes, T.R., and, Page, J.E., (2011) The draft genome and transcriptome of Cannabis sativa. Genome Biol. 12, R102. oi:.
3. Chen, H., Kim, H.U., Weng, H., and, Browse, J., (2011) Malonyl-CoA synthetase, encoded by ACYL ACTIVATING ENZYME13, is essential for growth and development of Arabidopsis. Plant Cell, 23, 2247-2262.
4. Cook, D., Rimando, A.M., Clemente, T.E., et al. (2010) Alkylresorcinol synthases expressed in Sorghum bicolor root hairs play an essential role in the biosynthesis of the allelopathic benzoquinone sorgoleone. Plant Cell, 22, 867-887.
5. Dai, X., Wang, G., Yang, D.S., Tang, Y., Broun, P., Marks, M.D., Sumner, L.W., Dixon, R.A., and, Zhao, P.X., (2010) TrichOME: a comparative omics database for plant trichomes. Plant Physiol. 152, 44-54.
6. Dayanandan, P., and, Kaufman, P.B., (1976) Trichomes of Cannabis sativa L. (Cannabaceae). Am. J. Bot. 63, 578-591.
7. Dehesh, K., Edwards, P., Hayes, T., Cranmer, A.M., and, Fillatti, J., (1996) Two novel thioesterases are key determinants of the bimodal distribution of acyl chain length of Cuphea palustris seed oil. Plant Physiol. 110, 203-210.
8. Dewick, P.M., (2009) Medicinal Natural Products: A Biosynthetic Approach, 3rd edn. Chichester: John Wiley & Sons.
9. Earley, K.W., Haag, J.R., Pontes, O., Opper, K., Juehne, T., Song, K., and, Pikaard, C.S., (2006) Gateway-compatible vectors for plant functional genomics and proteomics. Plant J. 45, 616-629.
10. Elsohly, M.A., and, Slade, D., (2005) Chemical constituents of marijuana: the complex mixture of natural cannabinoids. Life Sci. 78, 539-548.
11. Fellermeier, M., and, Zenk, M.H., (1998) Prenylation of olivetolate by a hemp transferase yields cannabigerolic acid, the precursor of tetrahydrocannabinol. FEBS Lett. 427, 283-285.
12. Fellermeier, M., Eisenreich, W., Bacher, A., and, Zenk, M.H., (2001) Biosynthesis of cannabinoids. Incorporation experiments with 13C-labeled glucoses. Eur. J. Biochem. 268, 1596-1604.
13. Gaoni, Y., and, Mechoulam, R., (1964) Isolation, structure, and partial synthesis of an active constituent of hashish. J. Am. Chem. Soc. 86, 1646-1647.
14. Gershenzon, J., McCaskill, D., Rajaonarivony, J.I., Mihaliak, C., Karp, F., and, Croteau, R., (1992) Isolation of secretory cells from plant glandular trichomes and their use in biosynthetic studies of monoterpenes and other gland products. Anal. Biochem. 200, 130-138.
15. Ghosh, R., Chhabra, A., Phatale, P.A., Samrat, S.K., Sharma, J., Gosain, A., Mohanty, D., Saran, S., and, Gokhale, R.S., (2008) Dissecting the functional role of polyketide synthases in Dictyostelium discoideum: biosynthesis of the differentiation regulating factor 4-methyl-5-pentylbenzene-1,3-diol. J. Biol. Chem. 283, 11348-11354.
16. Gray, D., and, Prestage, S., (1999) Fresh tomato specific fluctuations in the composition of lipoxygenase-generated C6 aldehydes. Food Chem. 64, 149-155.
17. Horper, W., (1996) Biosynthesis of primin and miconidin and its derivatives. Phytochemistry 41, 451-456.
18. Hu, Y., Gai, Y., Yin, L., Wang, X., Feng, C., Feng, L., Li, D., Jiang, X.-N., and, Wang, D.-C., (2010) Crystal structures of a Populus tomentosa 4-coumarate:CoA ligase shed light on its enzymatic mechanisms. Plant Cell, 22, 3093-3104.
19. Izzo, A.A., Borrelli, F., Capasso, R., Di Marzo, V., and, Mechoulam, R., (2009) Non-psychotropic plant cannabinoids: new therapeutic opportunities from an ancient herb. Trends Pharmacol. Sci. 30, 515-527.
20. Kienow, L., Schneider, K., Bartsch, M., Stuible, H.-P., Weng, H., Miersch, O., Wasternack, C., and, Kombrink, E., (2008) Jasmonates meet fatty acids: functional analysis of a new acyl-coenzyme A synthetase family from Arabidopsis thaliana. J. Exp. Bot. 59, 403-19.
21. Koo, A.J.K., Chung, H.S., Kobayashi, Y., and, Howe, G.A., (2006) Identification of a peroxisomal acyl-activating enzyme involved in the biosynthesis of jasmonic acid in Arabidopsis. J. Biol. Chem. 281, 33511-33520.
22. Kroumova, A.B., and, Wagner, G.J., (2003) Different elongation pathways in the biosynthesis of acyl groups of trichome exudate sugar esters from various solanaceous plants. Planta, 216, 1013-1021.
23. Kroumova, A.B., Xie, Z., and, Wagner, G.J., (1994) A pathway for the biosynthesis of straight and branched, odd- and even-length, medium-chain fatty acids in plants. Proc. Natl. Acad. Sci. USA, 91, 11437-11441.
24. Lange, B.M., Wildung, M.R., Stauber, E.J., Sanchez, C., Pouchnik, D., and, Croteau, R., (2000) Probing essential oil biosynthesis and secretion by functional evaluation of expressed sequence tags from mint glandular trichomes. Proc. Natl. Acad. Sci. USA, 97, 2934-2939.
25. Lanyon, V.S., Turner, J.C., and, Mahlberg, P.G., (1981) Quantitative analysis of cannabinoids in the secretory product from capitate-stalked glands of Cannabis sativa L. (Cannabaceae). Bot. Gaz. 142, 316-319.
26. Lingner, T., Kataya, A.R., Antonicelli, G.E., Benichou, A., Nilssen, K., Chen, X.-Y., Siemsen, T., Morgenstern, B., Meinicke, P., and, Reumann, S., (2011) Identification of novel plant peroxisomal targeting signals by a combination of machine learning methods and in vivo subcellular targeting analyses. Plant Cell, 23, 1556-72.
27. 9-tetrahydrocannabinol biosynthesis in Cannabis sativa. J. Exp. Bot. 60, 3715-3726.
28. Matoba, T., Hidaka, H., Narita, H., Kitamura, K., Kaizuma, N., and, Kito, M., (1985) Lipoxygenase-2 isozyme is responsible for generation of n-hexanal in soybean homogenate. J. Agric. Food Chem. 33, 852-855.
29. Mechoulam, R., (2005) Plant cannabinoids: a neglected pharmacological treasure trove. Br. J. Pharmacol. 146, 913-915.
30. Mechoulam, R., Parker, L.A., and, Gallily, R., (2002) Cannabidiol: an overview of some pharmacological aspects. J. Clin. Pharmacol. 42, 11S-19S.
31. Meisel, L., Fonseca, B., Gonzaelz, S., Baeza-Yates, R., Cambiazo, V., Campos, R., Gonzalez, M., Orellana, A., Retamales, J., and, Silva, H., (2005) A rapid and efficient method for purifying high quality total RNA from peaches (Prunus persica) for functional genomics analyses. Biol. Res. 38, 83-88.
32. Nagel, J., Culley, L., Lu, Y., Liu, E., Matthews, P.D., Stevens, J.F., and, Page, J.E., (2008) EST analysis of hop glandular trichomes identifies an O-methyltransferase that catalyzes the biosynthesis of xanthohumol. Plant Cell, 20, 186-200.
33. Nelson, B.K., Cai, X., and, Nebenführ, A., (2007) A multicolored set of in vivo organelle markers for co-localization studies in Arabidopsis and other plants. Plant J. 51, 1126-1136.
34. Perera, M.A., Choi, S.-Y., Wurtele, E.S., and, Nikolau, B.J., (2009) Quantitative analysis of short-chain acyl-coenzymeAs in plant tissues by LC-MS-MS electrospray ionization method. J. Chromatogr. 877, 482-488.
35. Phillips, M.A., Leõn, P., Boronat, A., and, Rodríguez- Concepciõn, M., (2008) The plastidial MEP pathway: unified nomenclature and resources. Trends Plant Sci. 13, 619-623.
36. Pichersky, E., and, Gang, D.R., (2000) Genetics and biochemistry of secondary metabolites in plants: an evolutionary perspective. Trends Plant Sci. 5, 439-445.
37. Raharjo, T.J., Chang, W.T., Verberne, M.C., Peltenburg-Looman, A.M., Linthorst, H.J., and, Verpoorte, R., (2004) Cloning and over-expression of a cDNA encoding a polyketide synthase from Cannabis sativa. Plant Physiol. Biochem. 42, 291-297.
38. Reumann, S., (2004) Specification of the peroxisome targeting signals type 1 and type 2 of plant peroxisomes by bioinformatics analyses. Plant Physiol. 135, 783-800.
39. Rowan, D.D., Allen, J.M., Fielder, S., and, Hunt, M.B., (1999) Biosynthesis of straight-chain ester volatiles in red delicious and granny smith apples using deuterium-labeled precursors. J. Agric. Food Chem. 47, 2553-2562.
40. Schmelz, S., and, Naismith, J.H., (2009) Adenylate-forming enzymes. Curr. Opin. Struct. Biol. 19, 666-671.
41. Schneider, K., Kienow, L., Schmelzer, E., Colby, T., Bartsch, M., Miersch, O., Wasternack, C., Kombrink, E., and, Stuible, H.-P., (2005) A new type of peroxisomal acyl-coenzyme A synthetase from Arabidopsis thaliana has the catalytic capacity to activate biosynthetic precursors of jasmonic acid. J. Biol. Chem. 280, 13962-13972.
42. Shockey, J., and, Browse, J., (2011) Genome-level and biochemical diversity of the acyl-activating enzyme superfamily in plants. Plant J. 66, 143-160.
43. Shockey, J.M., Fulda, M.S., and, Browse, J.A., (2002) Arabidopsis contains nine long-chain acyl-coenzyme a synthetase genes that participate in fatty acid and glycerolipid metabolism. Plant Physiol. 129, 1710-1722.
44. Shockey, J.M., Fulda, M.S., and, Browse, J., (2003) Arabidopsis contains a large superfamily of acyl-activating enzymes. Phylogenetic and biochemical analysis reveals a new class of acyl-coenzyme A synthetases Plant Physiol. 132, 1065-1076.
45. 1-tetrahydrocannabinolic acid synthase from Cannabis sativa L. J. Biol. Chem. 279, 39767-39774.
46. Souza, C. de A., Barbazuk, B., Ralph, S.G., Bohlmann, J., Hamberger, B., and, Douglas, C.J., (2008) Genome-wide analysis of a land plant-specific acyl:coenzyme A synthetase (ACS) gene family in Arabidopsis, poplar, rice and Physcomitrella. New Phytol. 179, 987-1003.
47. Sparkes, I.A., Runions, J., Kearns, A., and, Hawes, C., (2006) Rapid, transient expression of fluorescent fusion proteins in tobacco plants and generation of stably transformed plants. Nat. Protocol. 1, 2019-2025.
48. Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M., and, Kumar, S., (2011) MEGA5: Molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol. Biol. Evol. 28, 2731-2739.
49. Taura, F., Sirikantaramas, S., Shoyama, Y., Yoshikai, K., Shoyama, Y., and, Morimoto, S., (2007) Cannabidiolic-acid synthase, the chemotype-determining enzyme in the fiber-type Cannabis sativa. FEBS Lett. 581, 2929-2934.
50. Taura, F., Tanaka, S., Taguchi, C., Fukamizu, T., Tanaka, H., Shoyama, Y., and, Morimoto, S., (2009) Characterization of olivetol synthase, a polyketide synthase putatively involved in cannabinoid biosynthetic pathway. FEBS Lett. 583, 2061-2066.
51. Townsend, C.A., Christensen, S.B., and, Trautwein, K., (1984) Hexanoate as a starter unit in polyketide biosynthesis. J. Am. Chem. Soc. 106, 3868-3869.
52. Wang, G., Tian, L., Aziz, N., Broun, P., Dai, X., He, J., King, A., Zhao, P.X., and, Dixon, R.A., (2008) Terpene biosynthesis in glandular trichomes of hop (Humulus lupulus L.). Plant Physiol. 148, 1254-1266.
53. Xiao, S., and, Chye, M.-L., (2011) New roles for acyl-CoA-binding proteins (ACBPs) in plant development, stress responses and lipid metabolism. Prog. Lipid Res. 50, 141-151.
54. Xu, Z., Metsä-Ketelä, M., and, Hertweck, C., (2009) Ketosynthase III as a gateway to engineering the biosynthesis of antitumoral benastatin derivatives. J. Biotechnol. 140, 107-113.
55. Yabe, K., and, Nakajima, H., (2004) Enzyme reactions and genes in aflatoxin biosynthesis. Appl. Microbiol. Biotechnol. 64, 745-755.