Recent progress in the metabolic engineering of alkaloids in plant systems

Current Opinion in Biotechnology

Volumn 24, Issue 2, 2013, Pages 354-365

  Glenn, Weslee S ^a,b   Runguphan, Weerawat ^b,d   O'Connor, Sarah E ^a,c  

^a JOHN INNES CENTRE   (United Kingdom)

^b MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^c UNIVERSITY OF EAST ANGLIA   (United Kingdom)

^d JOINT BIOENERGY INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BENZYLISOQUINOLINE ALKALOIDS; CHEMICAL ECOLOGY; ENZYMATIC PATHWAYS; MONOTERPENE INDOLE ALKALOIDS; PLANT ALKALOIDS; PLANT SYSTEMS; PRODUCTION OF; RECENT PROGRESS;

ALKALOIDS; BIOCHEMISTRY; METABOLIC ENGINEERING; NITROGEN COMPOUNDS; SCAFFOLDS;

METABOLITES;

ALKALOID DERIVATIVE; BISBENZYLISOQUINOLINE ALKALOID; CYTOCHROME P450; GLUCOSINOLATE; MONOTERPENE INDOLE ALKALOID; UNCLASSIFIED DRUG;

CARBON METABOLISM; ENZYME ACTIVITY; ENZYME SPECIFICITY; ENZYME SYNTHESIS; GENE CLUSTER; GENE OVEREXPRESSION; METABOLIC ENGINEERING; NITROGEN METABOLISM; NONHUMAN; PLANT DEFENSE; PLANT GENOME; PLANT LEAF; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVIEW; RNA INTERFERENCE;

ALKALOIDS; BENZYLISOQUINOLINES; BIOLOGICAL AGENTS; CYTOCHROME P-450 ENZYME SYSTEM; GLUCOSINOLATES; INDOLE ALKALOIDS; METABOLIC ENGINEERING; MONOTERPENES; PLANTS;

EID: 84874992963     PISSN: 09581669     EISSN: 18790429     Source Type: Journal    
DOI: 10.1016/j.copbio.2012.08.003     Document Type: Review

References (59)

1. Shibamoto T., Bjeldanes L.F. Introduction to Food Toxicology 2009, Academic Press (Elsevier).
2. Lipinski C., Hopkins A. Navigating chemical space for biology and medicine. Nature 2004, 432:855-861.
3. Rosén J., Gottfries J., Muresan S., Backlund A., Oprea L.A. Novel chemical space exploration via natural products. J Med Chem 2009, 52:1953-1962.
4. Leonard E., Runguphan W., O'Connor S.E., Prather K.J. Opportunities in metabolic engineering to facilitate scalable alkaloid production. Nat Chem Biol 2009, 5:292-300.
5. Martin D.B.C., Nguyen L.Q., Vanderwal C.D. Syntheses of strychnine, norfluorocurarine, dehydrodesacetylretuline, and valparicine enabled by intramolecular cycloadditions of Zincke aldehydes. J Org Chem 2012, 77:17-46.
6. Murata J., Roepke J., Gordon H., De Luca V. The leaf epidermome of Catharanthus roseus reveals its biochemical specialization. Plant Cell 2008, 20:524-542.
7. Liscombe D.K., O'Connor S.E. A virus-induced gene silencing approach to understanding alkaloid metabolism in Catharanthus roseus. Phytochemistry 2011, 72:1969-1977.
8. Seigler D.S. Plant Secondary Metabolism 1998, Kluwer Academic Publishers.
9. O'Connor S.E., Maresh J.J. Chemistry and biology of monoterpene indole alkaloid biosynthesis. Nat Prod Rep 2006, 23:532-547.
10. Guirimand G., Courdavault V., Lanoue A., Mahroug S., Guihur A., Blanc N., Giglioli-Guivarc'h N., St-Pierre B., Burlaut V. Strictosidine activation in Apocynaceae: towards a " nuclear time bomb" ?. BMC Plant Biol 2010, 10.
11. Dewick P.M. Medicinal Natural Products A Biosynthetic Approach 2001, John Wiley & Sons. edn 2.
12. Giddings L.-A., Liscombe D.K., Hamilton J.P., Childs K.L., DellaPenna D., Buell C.R., O'Connor S.E. A stereoselective hydroxylation step of alkaloid biosynthesis by a unique cytochrome P450 in Catharanthus roseus. J Biol Chem 2011, 286:16751-16757.
13. Mizutani M., Sato F. Unusual P450 reactions in plant secondary metabolism. Arch Biochem Biophys 2011, 507:194-203.
14. Mizutani M., Ohta D. Diversification of P450 genes during land plant evolution. Annu Rev Plant Biol 2010, 61:291-315.
15. Sawayama A.M., Chen M.M.Y., Kulanthaivel P., Kuo M.-S., Hemmerle H., Arnold F.H. A panel of cytochrome P450 BM3 variants to produce drug metabolites and diversify lead compounds. Chem Eur J 2009, 15:11723-11729.
16. Leonard E., Koffas M.A.G. Engineering of artificial plant cytochrome P450 enzymes for synthesis of isoflavones by Escherichia coli. Appl Environ Microbiol 2007, 73:7246-7251.
17. Denisov I., Sligar S.G. Cytochromes P450 in nanodiscs. Biochem Biophys 2011, 1814:223-229.
18. Neumann C.S., Fujimori D.G., Walsh C.T. Halogenation strategies in natural product biosynthesis. Chem Biol 2008, 15:99-109.
19. Herrera-Rodriguez L.N., Khan F., Robins K.T., Meyer H.-P. Perspective on biotechnological halogenation. Part I: halogenated products and enzymatic halogenation. Chem Today 2011, 29:31-33.
20. Blasiak L.C., Drennan C.L. Structural perspective on enzymatic halogenation. Acc Chem Res 2009, 42:147-155.
21. Runguphan W., Maresh J.J., O'Connor S.E. Silencing of tryptamine biosynthesis for production of nonnatural alkaloids in plant cultures. Proc Natl Acad Sci USA 2009, 106:13673-13678.
22. Bernahardt P., McCoy E., O'Connor S.E. Rapid identification of enzyme variants for reengineered alkaloid biosynthesis in periwinkle. Chem Biol 2007, 14:888-897.
23. Runguphan W., O'Connor S.E. Metabolic reprogramming of periwinkle plant culture. Nat Chem Biol 2009, 5:151-153.
24. Runguphan W., Qu X., O'Connnor S.E. Integrating carbon-halogen bond formation into medicinal plant metabolism. Nature 2010, 18:461-464.
25. Glenn W.S., Nims E., O'Connor S.E. Reengineering a tryptophan halogenase to chlorinate a direct alkaloid precursor. J Am Chem Soc 2011, 133:19346-19349.
26. Facchini P., De Luca V. Opium poppy and Madagascar periwinkle: model non-model systems to investigate alkaloid biosynthesis in plants. Plant J 2008, 54:763-784.
27. Hagel J.M., Facchini P.J. Dioxygenases catalyze the O-demethylation steps of morphine biosynthesis in opium poppy. Nat Chem Biol 2010, 6:273-275.
28. Runguphan W., Glenn W.S., O'Connor S.E. Redesign of a dioxygenase in morphine biosynthesis. Chem Biol 2012, 19:674-678.
29. Winzer T., Gazda V., He Z., Kaminski F., Kern M., Larson T.R., Li Y., Meade F., Teodor R., Vaistij F.E., et al. A Papaver somniferum 10-gene cluster for synthesis of the anticancer alkaloid noscapine. Science 2012, 336:1704-1708.
30. Allen R.S., Milligate A.G., Chilty J.A., Thisleton J., Miller J.A., Fist A.J., Gerlach W.L., Lancin P.J. RNAi-mediated replacement of morphine with the nonnarcotic alkaloid reticuline in opium poppy. Nat Biotechnol 2004, 22:1559-1566.
31. Park S.-U., Yu M., Facchini P.J. Modulation of berberine bridge enzyme levels in transgenic root cultures of California poppy alters the accumulation of benzophenathridine alkaloids. Plant Mol Biol 2003, 51:153-164.
32. Park S.-U., Facchini P.J. Antisense RNA-mediated suppression of benzophenathridine alkaloid biosynthesis in transgenic cell cultures of California poppy. Plant Physiol 2002, 128:696-706.
33. Fujii N., Inui T., Iwasa K., Morishige T., Sato F. Knockdown of berberine bridge enzyme by RNAi accumulates (S)-reticuline and activates a silent pathway in cultured California poppy cells. Transgenic Res 2007, 16:363-375.
34. Minami H., Kim J.S., Ikezawa N., Takemura T., Katayama T., Kumagai H., Sato F. Microbial production of plant benzylisoquinoline alkaloids. Proc Natl Acad Sci USA 2008, 105:7393-7398.
35. Hawkins K.M., Smolke C.D. Production of benzylisoquinoline alkaloids in Saccharomyces cerevisiae. Nat Chem Biol 2008, 4:564-573.
36. Nakagawa A., Minami H., Kim J.-S., Koyangi T., Katayama T., Sato F., Kumagai H. A bacterial platform for fermentative production of plant alkaloids. Nat Commun 2011, 2.
37. Geu-Flores F., Nielsen M.T., Nafisi M., Møldrup M.E., Olsen C.E., Motawia M.S., Halkier B.A. Glucosinolate engineering identifies a gamma-glutamyl peptidase. Nat Chem Biol 2009, 5:575-577.
38. Ratzka A., Vogel H., Kliebensten D.J., Mitchell-Olds T., Kroymann J. Disarming the mustard oil bomb. Proc Natl Acad Sci USA 2002, 99:11223-11228.
39. Wittstock U., Burow M. Tipping the scales - specifier proteins in glucosinolate hydrolysis. IUBMB Life 2007, 59:744-751.
40. Mikkelsen M.D., Buron L.D., Salomonse B., Olsen C.E., Hansen B.G., MortenSen U.H., Halkier B.A. Microbial production of indolylglucosinolate through engineering of a multi-gene pathway in a versatile yeast expression platform. Metab Eng 2012, 14:104-111.
41. Møldrup M.E., Geu-Flores F., Olsen C.E., Halkier B.A. Modulation of sulfur metabolism enables efficient glucosinolate engineering. BMC Biotechnol 2011, 11.
42. Mikkelsen M.D., Buron L.D., Salomonsen B., Olsen C.E., Hansen B.G., Mortensen U.H., Halkier B.A. Microbial production of indolylglucosinolate through engineering of a multi-gene pathway in a versatile yeast expression platform. Metab Eng 2012, 2:104-111.
43. Møldrup M.E., Geu-Flores F., de Vos M., Olsen C.E., Sun J., Jander G., Halkier B.A. Engineering of benzylglucosinolate in tobacco provides proof-of-concept for dead-end trap crops genetically modified to attract Plutella xylostella (diamondback moth). Plant Biotechnol J 2012, 10:435-442.
44. Liscombe D.K., Usera A.R., O'Connor S.E. Homolog of tocopherol C methyltransferases catalyzes N methylation in anticancer alkaloid biosynthesis. Proc Natl Acad Sci USA 2010, 107:18793-18798.
45. Peretz Y., Mozes-Koch R., Akad F., Tanne E., Czosnek H., Sela I. A universal expression/silencing vector in plants. Plant Physiol 2007, 145:1251-1263.
46. Weeks A.M., Chang M.C.Y. Constructing de novo biosynthetic pathways for chemical synthesis in living cells. Biochemistry 2011, 50:5404-5418.
47. Dueber J.E., Wu G.C., Malmirchegini G.R., Moon T.S., Petzold C.J., Ullal A.V., Prather K.L.J., Keasling J.D. Synthetic protein scaffolds provide modular control over metabolic flux. Nat Biotechnol 2009, 27:753-759.
48. Naqvi S., Farré G., Sanahuja G., Capell T., Zhu C., Christou P. Where more is better: multigene engineering in plants. Trends Plant Sci 2009, 15:48-56.
49. Nour-Eldin H., Geu-Flores F., Halkier B.A. USER cloning and USER fusion: the ideal cloning techniques for small and big laboratories. Plant Secondary Metabolism Engineering, Methods in Molecular Biology 2010, 185-200. Springer Science+Business Media, LLC. A.G. Fett-Netto (Ed.).
50. Mozes-Koch R., Gover O., Tanne E., Peretz Y., Maori E., Chernin L., Sela I. Expression of an entire bacterial operon in plants. Plant Physiol 2012, 158:1883-1892.
51. Chang Al, Wolf J.J., Smolke C.D. Synthetic RNA switches as a tool for temporal and spatial control over gene expression. Curr Opin Biotechnol 2012, 23:1-10.
52. Agapakis C.M., Boyle P.M., Silver P.A. Natural strategies for the spatial optimization of metabolism in synthetic biology. Nat Chem Biol 2012, 8:527-535.
53. Goddijin O.J., Pennings E.J., van der Helm P., Schilperoot R.A., Verpoorte R., Hoge J.H. Overexpression of a tryptophan decarboxylase cDNA in Catharanths roseus crown gall calluses results in increased tryptamine levels but not in increased terpenoid indole alkaloid production. Transgenic Res 1995, 4:315-323.
54. Suttipanta N., Pattanaik S., Kulshrestha M., Patra B., Singh S.K., Yuan L. The transcription factor CrWRKY1 positively regulates the terpenoid indole alkaloid biosynthesis in Catharanthus roseus. Plant Physiol 2011, 157:2081-2093.
55. Hughes E.H., Hong S.B., Gibson S.I., Shanks J.V., San K.Y. Expression of a feedback-resistant anthranilate synthase in Catharanthus roseus hairy roots provides evidence for tight regulation of terpenoid indole alkaloid levels. Biotechnol Bioeng 2004, 86:718-727.
56. Peebles C.A., Hong S.B., Gibson S.I., Shanks J.V., San K.Y. Effects of terpenoid precursor feeding on Catharanthus roseus hairy roots over-expressing the alpha or the alpha and beta subunits of anthranilate synthase. Biotechnol Bioeng 2006, 93:534-540.
57. Goklany S., Loring R.H., Glick J., Lee-Parsons C.W. Assessing the limitations to terpenoid indole alkaloid biosynthesis in Catharanthus roseus hairy root cultures through gene expression profiling and precursor feeding. Biotechnol Prog 2009, 25:1289-1296.
58. McCoy E., O'Connor S.E. Directed biosynthesis of alkaloid analogs in the medicinal plant Catharanthus roseus. J Am Chem Soc 2006, 128:14276-14277.
59. Wijekoon C.P., Facchini P.J. Systematic knockdown of morphine pathway enzymes in opium poppy using virus-induced gene silencing. Plant J 2012, 69:1052-1063.