Evolutionary and cellular webs in benzylisoquinoline alkaloid biosynthesis

Current Opinion in Biotechnology

Volumn 19, Issue 2, 2008, Pages 173-180

  Liscombe, David K ^a   Facchini, Peter J ^a  

^a UNIVERSITY OF CALGARY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

BENZYLISOQUINOLINE ALKALOID; INTRAMOLECULAR COUPLING;

BIOACTIVITY; BIOSYNTHESIS; HYDROXYLATION; METABOLITES; METHYLATION; MOLECULAR WEIGHT;

AROMATIC COMPOUNDS;

AROMATIC AMINO ACID; BENZYLISOQUINOLINE ALKALOID; CODEINE; MORPHINE; TYROSINE DERIVATIVE; UNCLASSIFIED DRUG;

BIOCHEMISTRY; BIOLOGICAL ACTIVITY; BIOSYNTHESIS; CYTOLOGY; DRUG ACTIVITY; DRUG METABOLISM; DRUG STRUCTURE; ENZYME ANALYSIS; HYDROXYLATION; METABOLIC ENGINEERING; METABOLITE; METHYLATION; PRIORITY JOURNAL; REVIEW; TRANSCRIPTOMICS;

ALKALOIDS; BENZYLISOQUINOLINES; BIOTECHNOLOGY; EVOLUTION, MOLECULAR; METHYLTRANSFERASES; MODELS, BIOLOGICAL; MOLECULAR STRUCTURE; PLANT PROTEINS; PLANTS, GENETICALLY MODIFIED;

EID: 42249097714     PISSN: 09581669     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.copbio.2008.02.012     Document Type: Review

References (39)

1. Liscombe D.K., Macleod B.P., Loukanina N., Nandi O.I., and Facchini P.J. Evidence for the monophyletic evolution of benzylisoquinoline alkaloid biosynthesis in angiosperms. Phytochemistry 66 (2005) 1374-1393
2. Ziegler J., Voigtlander S., Schmidt J., Kramell R., Miersch O., Ammer C., Gesell A., and Kutchan T.M. Comparative transcript and alkaloid profiling in Papaver species identifies a short chain dehydrogenase/reductase involved in morphine biosynthesis. Plant J 48 (2006) 177-192. An example of how comparative transcript and metabolite profiling data can be integrated to identify novel biosynthetic genes. The methods described have led to the discovery of two genes involved in morphinan alkaloid biosynthesis, including salutaridine reductase, which is detailed in this paper.
3. Facchini P., Hagel J., Liscombe D., Loukanina N., MacLeod B., Samanani N., and Zulak K. Opium poppy: blueprint for an alkaloid factory. Phytochem Rev 6 (2007) 97-124
4. Minami H., Dubouzet E., Iwasa K., and Sato F. Functional analysis of norcoclaurine synthase in Coptis japonica. J Biol Chem 282 (2007) 6274-6282
5. Luk L.Y., Bunn S., Liscombe D.K., Facchini P.J., and Tanner M.E. Mechanistic studies on norcoclaurine synthase of benzylisoquinoline alkaloid biosynthesis: an enzymatic Pictet-Spengler reaction. Biochemistry 46 (2007) 10153-10161
6. Berkner H., Engelhorn J., Liscombe D.K., Schweimer K., Wohrl B.M., Facchini P.J., Rosch P., and Matecko I. High-yield expression and purification of isotopically labeled norcoclaurine synthase, a Bet v 1-homologous enzyme, from Thalictrum flavum for NMR studies. Protein Expr Purif 56 (2007) 197-204
7. Fisinger U., Grobe N., and Zenk M.H. Thebaine synthase: a new enzyme in the morphine pathway in Papaver somniferum. Nat Prod Commun 2 (2007) 249-253
8. Ikezawa N., Iwasa K., and Sato F. Molecular cloning and characterization of methylenedioxy bridge-forming enzymes involved in stylopine biosynthesis in Eschscholzia californica. FEBS J 274 (2007) 1019-1035
9. Liscombe D.K., and Facchini P.J. Molecular cloning and characterization of tetrahydroprotoberberine cis-N-methyltransferase, an enzyme involved in alkaloid biosynthesis in opium poppy. J Biol Chem 282 (2007) 14741-14751
10. Takeshita N., Fujiwara H., Mimura H., Fitchen J.H., Yamada Y., and Sato F. Molecular cloning and characterization of S-adenosyl-l-methionine: scoulerine-9-O-methyltransferase from cultured cells of Coptis japonica. Plant Cell Physiol 36 (1995) 29-36
11. Ikezawa N., Tanaka M., Nagayoshi M., Shinkyo R., Sakaki T., Inouye K., and Sato F. Molecular cloning and characterization of CYP719, a methylenedioxy bridge-forming enzyme that belongs to a novel P450 family, from cultured Coptis japonica cells. J Biol Chem 278 (2003) 38557-38565
12. Amann M., Nagakura N., and Zenk M.H. Purification and properties of (S)-tetrahydroprotoberberine oxidase from suspension-cultured cells of Berberis wilsoniae. Eur J Biochem 175 (1988) 17-25
13. Chen S., Galan M.C., Coltharp C., and O'Connor S.E. Redesign of a central enzyme in alkaloid biosynthesis. Chem Biol 13 (2006) 1137-1141
14. Maresh J.J., Giddings L.A., Friedrich A., Loris E.A., Panjikar S., Trout B.L., Stockigt J., Peters B., and O'Connor S.E. Strictosidine synthase: mechanism of a Pictet-Spengler catalyzing enzyme. J Am Chem Soc 130 (2008) 710-723
15. Inui T., Tamura K., Fujii N., Morishige T., and Sato F. Overexpression of Coptis japonica norcoclaurine 6-O-methyltransferase overcomes the rate-limiting step in benzylisoquinoline alkaloid biosynthesis in cultured Eschscholzia californica. Plant Cell Physiol 48 (2007) 252-262
16. Geissler R., Brandt W., and Ziegler J. Molecular modeling and site-directed mutagenesis reveal the benzylisoquinoline binding site of the short-chain dehydrogenase/reductase salutaridine reductase. Plant Physiol 143 (2007) 1493-1503
17. Weiss D., Baumert A., Vogel M., and Roos W. Sanguinarine reductase, a key enzyme of benzophenanthridine detoxification. Plant Cell Environ 29 (2006) 291-302
18. Ziegler J., Diaz-Chavez M.L., Kramell R., Ammer C., and Kutchan T.M. Comparative macroarray analysis of morphine containing Papaver somniferum and eight morphine free Papaver species identifies an O-methyltransferase involved in benzylisoquinoline biosynthesis. Planta 222 (2005) 458-471
19. Frick S., Kramell R., Schmidt J., Fist A.J., and Kutchan T.M. Comparative qualitative and quantitative determination of alkaloids in narcotic and condiment Papaver somniferum cultivars. J Nat Prod 68 (2005) 666-673
20. Facchini P.J., and Park S.U. Developmental and inducible accumulation of gene transcripts involved in alkaloid biosynthesis in opium poppy. Phytochemistry 64 (2003) 177-186
21. Roos W., Viehweger K., Dordschbal B., Schumann B., Evers S., Steighardt J., and Schwartze W. Intracellular pH signals in the induction of secondary pathways-the case of Eschscholzia californica. J Plant Physiol 163 (2006) 369-381
22. Zulak K.G., Cornish A., Daskalchuk T.E., Deyholos M.K., Goodenowe D.B., Gordon P.M., Klassen D., Pelcher L.E., Sensen C.W., and Facchini P.J. Gene transcript and metabolite profiling of elicitor-induced opium poppy cell cultures reveals the coordinate regulation of primary and secondary metabolism. Planta 225 (2007) 1085-1106. The first example of the application of large-scale genomic and metabolomic techniques to understanding benzylisoquinoline biosynthesis elucidates the interface between primary and secondary metabolism, establishing a blueprint for opium poppy cell cultures as alkaloid factories.
23. 1H NMR metabolomics reveals extensive reprogramming of primary and secondary metabolism in elicitor-treated opium poppy cell cultures. BMC Plant Biol 8 (2008) 5
24. 13C-labeled tyramine ruled out the generation of 4-hydroxyphenylaldehyde by oxidation of tyramine.
25. Kato N., Dubouzet E., Kokabu Y., Yoshida S., Taniguchi Y., Dubouzet J.G., Yazaki K., and Sato F. Identification of a WRKY protein as a transcriptional regulator of benzylisoquinoline alkaloid biosynthesis in Coptis japonica. Plant Cell Physiol 48 (2007) 8-18. This paper describes the screening of putative regulatory genes, which led to the isolation and characterization of the first transcription factor involved in BIA biosynthesis.
26. Viehweger K., Schwartze W., Schumann B., Lein W., and Roos W. The Gα protein controls a pH-dependent signal path to the induction of phytoalexin biosynthesis in Eschscholzia californica. Plant Cell 18 (2006) 1510-1523
27. Heinze M., Steighardt J., Gesell A., Schwartze W., and Roos W. Regulatory interaction of the Gα protein with phospholipase A(2) in the plasma membrane of Eschscholzia californica. Plant J 52 (2007) 1041-1051
28. Bird D.A., Franceschi V.R., and Facchini P.J. A tale of three cell types: alkaloid biosynthesis is localized to sieve elements in opium poppy. Plant Cell 15 (2003) 2626-2635
29. Samanani N., Alcantara J., Bourgault R., Zulak K.G., and Facchini P.J. The role of phloem sieve elements and laticifers in the biosynthesis and accumulation of alkaloids in opium poppy. Plant J 47 (2006) 547-563
30. Weid M., Ziegler J., and Kutchan T.M. The roles of latex and the vascular bundle in morphine biosynthesis in the opium poppy, Papaver somniferum. Proc Natl Acad Sci U S A 101 (2004) 13957-13962
31. Alcantara J., Bird D.A., Franceschi V.R., and Facchini P.J. Sanguinarine biosynthesis is associated with the endoplasmic reticulum in cultured opium poppy cells after elicitor treatment. Plant Physiol 138 (2005) 173-183
32. Samanani N., Park S.U., and Facchini P.J. Cell type-specific localization of transcripts encoding nine consecutive enzymes involved in protoberberine alkaloid biosynthesis. Plant Cell 17 (2005) 915-926
33. Allen R.S., Millgate A.G., Chitty J.A., Thisleton J., Miller J.A., Fist A.J., Gerlach W.L., and Larkin P.J. RNAi-mediated replacement of morphine with the nonnarcotic alkaloid reticuline in opium poppy. Nat Biotechnol 22 (2004) 1559-1566
34. Larkin P.J., Miller J.A., Allen R.S., Chitty J.A., Gerlach W.L., Frick S., Kutchan T.M., and Fist A.J. Increasing morphinan alkaloid production by over-expressing codeinone reductase in transgenic Papaver somniferum. Plant Biotechnol J 5 (2007) 26-37
35. Frick S., Kramell R., and Kutchan T.M. Metabolic engineering with a morphine biosynthetic P450 in opium poppy surpasses breeding. Metab Eng 9 (2007) 169-176
36. Allen R.S., Miller J.A., Chitty J.A., Fist A.J., Gerlach W.L., and Larkin P.J. Metabolic engineering of morphinan alkaloids by over-expression and RNAi suppression of salutaridinol 7-O-acetyltransferase in opium poppy. Plant Biotechnol J 6 (2007) 22-30
37. Fujii N., Inui T., Iwasa K., Morishige T., and Sato F. Knockdown of berberine bridge enzyme by RNAi accumulates (S)-reticuline and activates a silent pathway in cultured California poppy cells. Transgenic Res 16 (2007) 363-375
38. Apuya N.R., Park J.H., Zhang L., Ahyow M., Davidow P., Van Fleet J., Rarang J.C., Hippley M., Johnson T.W., Yoo H.D., et al. Enhancement of alkaloid production in opium and California poppy by transactivation using heterologous regulatory factors. Plant Biotechnol J 6 (2007) 160-175
39. Ikezawa N., Iwasa K., and Sato F. Molecular cloning and characterization of CYP80G2, a cytochrome P450 which catalyzes an intramolecular C-C phenol coupling of (S)-reticuline in magnoflorine biosynthesis, from cultured Coptis japonica cells. J Biol Chem 283 (2008) 8810-8821