Transcript and metabolite profiling in cell cultures of 18 plant species that produce benzylisoquinoline alkaloids

Phytochemistry

Volumn 77, Issue , 2012, Pages 79-88

  Farrow, Scott C ^a   Hagel, Jillian M ^a   Facchini, Peter J ^a  

^a UNIVERSITY OF CALGARY   (Canada)

Author keywords

Benzylisoquinoline alkaloids; Gene discovery; Plant cell culture; Ranunculales; Targeted metabolite profiling; Transcriptomics

Indexed keywords

ALKALOID; BENZYLISOQUINOLINE DERIVATIVE; MESSENGER RNA;

ARTICLE; BIOSYNTHESIS; CELL CULTURE; CHEMISTRY; EXPRESSED SEQUENCE TAG; GENETICS; METABOLISM; NUCLEIC ACID DATABASE; RANUNCULACEAE;

ALKALOIDS; BENZYLISOQUINOLINES; CELLS, CULTURED; DATABASES, NUCLEIC ACID; EXPRESSED SEQUENCE TAGS; RANUNCULACEAE; RNA, MESSENGER;

RANUNCULALES;

EID: 84859159395     PISSN: 00319422     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.phytochem.2012.02.014     Document Type: Article

References (67)

1. S.F. Altschul, W. Gish, W. Miller, E.W. Myers, and D.J. Lipman Basic localalignment search tool J. Mol. Biol. 215 1990 403 410
2. Angiosperm Phylogeny Group III An update of the Angiosperm phylogeny group classification for the orders and families of flowering plants: APG III Bot. J. Linn. Soc. 161 2009 105 121
3. T.Z. Berardini, S. Mundodi, L. Reiser, E. Huala, M. Garcia-Hernandez, P. Zhang, L.A. Mueller, J. Yoon, A. Doyle, G. Lander, N. Moseyko, D. Yoo, I. Xu, B. Zoeckler, M. Montoya, N. Miller, D. Weems, and S.Y. Rhee Functional annotation of the Arabidopsis genome using controlled vocabularies Plant Physiol. 135 2004 745 755
4. D.A. Bird, V.R. Franceschi, and P.J. Facchini A tale of three cell types: alkaloid biosynthesis is localized to sieve elements in opium poppy Plant Cell 15 2003 2626 2635
5. M. Cai, Y. Zhou, X. Wang, R. Li, X. Liao, and L. Ding Rapid structural characterization of isomeric benzo[c]phenanthridine alkaloids from the roots of Zanthoxylum nitidium by liquid chromatography combined with electrospray ionization tandem mass spectrometry Rapid Commun. Mass Spectrom. 21 2007 1931 1936
6. J.E. Carlson, J.H. Leebens-Mack, P.K. Wall, L.M. Zahn, L.A. Mueller, L.L. Landherr, Y. Hu, D.C. Ilut, J.M. Arrington, S. Choirean, A. Becker, D. Field, S.D. Tanksley, H. Ma, and C.W. dePamphilis EST database for early flower development in California poppy (Eschscholzia californica Cham., Papaveraceae) tags over 6000 genes from a basal eudicot Plant Mol. Biol. 62 2006 351 369
7. J.-B.F. Charron, G. Breton, J. Danyluk, I. Muzac, R.K. Ibrahim, and F. Sarhan Molecular and biochemical characterization of a cold-regulated phosphoethanolamine N-methyltransferase from wheat Plant Physiol. 129 2002 363 373
8. G.J. Chintalwar, S. Gupta, and V.A. Bapat Protoberberine alkaloids from callus and cell suspension cultures of Tinospora cordifolia Pharm. Biol. 41 2003 81 86
9. S.D. Cline Differential enhancement of benzo[c]phenanthridine alkaloid content in cell suspension cultures of Sanguinaria canadensis under conditions of combined hormonal deprivation and fungal elicitation J. Nat. Prod. 56 1993 1219 1228
10. P. Deevanhxay, M. Suzuki, N. Maeshibu, H. Li, K. Tanaka, and S. Hirose Simultaneous characterization of quaternary alkaloids, 8-oxoprotoberberine akaloids, and a steroid compound in Coscinium fenestratum by liquid chromatography hybrid ion trap time-of-flight mass spectrometry J. Pharm. Biomed. Anal. 50 2009 413 425
11. M.L. Díaz Chávez, M. Rolf, A. Gesell, and T.M. Kutchan Characterization of two methylenedioxy bridge-forming cytochrome P450-dependent enzymes of alkaloid formation in the Mexican prickly poppy Argemone mexicana Arch. Biochem. Biophys. 507 2011 186 193
12. C. Dumontet, and M.J. Jordan Microtubule-binding agents: a dynamic field of cancer therapeutics Nat. Rev. 9 2010 790 803
13. N. Fabre, C. Claparols, S. Richelme, M.-L. Angelin, I. Fourasté, and C. Moulis Direct characterization of isoquinoline alkaloids in a crude plant extract by ion-pair liquid chromatography-electrospray ionization tandem mass spectrometry: example of Eschscholzia californica J. Chromatogr. A 904 2000 35 46
14. P.J. Facchini, and S.U. Park Developmental and inducible accumulation of gene transcripts involved in alkaloid biosynthesis in opium poppy Phytochemistry 64 2003 177 186
15. O. Gamborg, R. Miller, and K. Ojima Nutrient requirements of suspension cultures of soybean root cells Exp. Cell Res. 50 1968 151 158
16. A.M. Gioacchini, Z. Czarnocki, Z. Arazny, I. Munari, and P. Traldi Electrospray ionization, accurate mass measurements and multistage mass spectrometry experiments in the characterization of stereoisomeric isoquinoline alkaloids Rapid Commun. Mass Spectrom. 14 2000 1592 1599
17. T. Grothe, R. Lenz, and T.M. Kutchan Molecular characterization of the salutaridinol 7-O-acetyltransferase involved in morphine biosynthesis in opium poppy Papaver somniferum J. Biol. Chem. 276 2001 30717 30723
18. J.M. Hagel, and P.J. Facchini Novel O-demethylases of morphine biosynthesis in opium poppy Nat. Chem. Biol. 6 2010 273 275
19. J.M. Hagel, and P.J. Facchini Biochemistry and occurrence of O-demethylation in plant metabolism Front. Physiol. 1 2010 14
20. J.M. Hagel, R. Krizevski, K. Kilpatrick, Y. Sitrit, F. Marsolais, E. Lewinsohn, and P.J. Facchini Expressed sequence tag analysis of khat (Catha edulis) provides a putative molecular biochemical basis for the biosynthesis of phenylpropylamino alkaloids Gen. Mol. Biol. 34 2011 640 646
21. K.M. Hawkins, and C.D. Smolke Production of benzylisoquinoline alkaloids in Saccharomyces cerevisiae Nat. Chem. Biol. 4 2008 564 573
22. T. Hefner, J. Arend, H. Warzecha, K. Siems, and J. Stöckigt Arbutin synthase, a novel member of the NRD1b glycosyltransferase family, is a unique multifunctional enzyme converting various natural products and xenobiotics Bioorg. Med. Chem. 10 2002 1731 1741
23. V.R. Hegde, P. Dai, C. Ladislaw, M.G. Patel, M.S. Puar, and J.A. Pachter D4 dopamine receptor-selective compounds from the Chinese plant Phoebe chekiangensis Bioorg. Med. Chem. Lett. 7 1997 1207 1212
24. I. Hook, H. Sheridan, and G. Wilson Alkaloids of cell cultures derived from strains of Papaver bracteatum Phytochemistry 27 1989 2137 2141
25. S.M. Hu, S.X. Xu, X.S. Yao, C.B. Cui, Y. Tezuka, and T. Kikuchi Dauricoside, a new glycosidal alkaloid having an inhibitory activity against blood-platelet aggregation Chem. Pharm. Bull. 41 1993 1866 1868
26. A. Ikuta, and H. Itokawa Alkaloids of tissue cultures of Nandina domestica Phytochemistry 27 1988 2143 2145
27. K. Iwasa, T. Takahashi, Y. Nishiyama, M. Moriyasu, M. Sugiura, A. Takeuchi, C. Tode, H. Tokuda, and K. Takeda Online structural elucidation of alkaloids and other constituents in crude extracts and cultured cells of Nandina domestica by combination of LC-MS/MS, LC-NMR, and LC-CD analyses J. Nat. Prod. 71 2008 1376 1385
28. K. Iwasa, W. Cui, T. Takahashi, Y. Nishiyama, M. Kamigauchi, J. Koyama, A. Takeuchi, M. Moriyasu, and K. Takeda Biotransformation of phenolic tetrahydroprotoberberines in plant cell cultures followed by LC-NMR, LC-MS, and LC-CD J. Nat. Prod. 73 2010 115 122
29. P.W. Jeffs The protoberberine alkaloids R. Helmuth, F. Manske, The Alkaloids vol. 9 1967 Academic Press London 41 115
30. N. Kashiwaba, M. Ono, J. Toda, H. Suzuki, and T. Sano Aporphine glycosides from Stephania cepharantha seeds J. Nat. Prod. 63 2000 477 479
31. S. Kim, D.E. Soltis, P.S. Soltis, M.J. Zanis, and Y. Suh Phylogenetic relationships among early-diverging eudicots based on four genes: were the eudicots ancestrally woody? Mol. Phylogenet. Evol. 31 2004 16 30
32. M.E. Kolewe, V. Gaurav, and S.C. Roberts Pharmaceutically active natural product synthesis and supply via plant cell culture technology Mol. Pharm. 5 2008 243 256
33. W. Kong, J. Wei, P. Abidi, M. Lin, S. Inaba, C. Li, Y. Wang, Z. Wang, S. Si, H. Pan, S. Wang, J. Wu, Y. Wang, Z. Li, J. Liu, and J.D. Jiang Berberine is a novel cholesterol-lowering drug working through a unique mechanism distinct from statins Nat. Med. 10 2004 1344 1351
34. E.-J. Lee, and P.J. Facchini Norcoclaurine synthase is a member of the pathogenesis-related 10/Bet v1 protein family Plant Cell 22 2010 3489 3503
35. Y. Li, T. Zhang, X. Zhang, H. Xu, and C. Liu Chemical fingerprint analysis of Phellodendri amurensis cortex by ultra performance LC/Q-TOF-MS methods combined with chemometrics J. Sep. Sci. 33 2010 3347 3353
36. K. Likhitwitayawuid, C.K. Angerhofer, H. Chai, J.M. Pezzuto, G.A. Cordell, and N. Ruangrungsi Cytotoxic and antimalarial alkaloids from the tubers of Stephania pierrei J. Nat. Prod. 56 1993 1468 1478
37. D.K. Liscombe, and P.J. Facchini 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
38. D.K. Liscombe, B.P. MacLeod, N. Loukanina, O.I. Nandi, and P.J. Facchini Evidence for the monophyletic evolution of benzylisoquinoline alkaloid biosynthesis in angiosperms Phytochemistry 66 2005 2501 2520
39. D.K. Liscombe, J. Ziegler, J. Schmidt, C. Ammer, and P.J. Facchini Targeted metabolite and transcript profiling for elucidating enzyme function: isolation of novel N-methyltransferases from three benzylisoquinoline alkaloid-producing species Plant J. 60 2009 729 743
40. E. McCoy, and S.E. O'Connor Natural products from plant cell cultures F. Petersen, R. Amstutz, Progress in Drug Research vol. 65 2009 Birkhäuser Basel 331 370
41. P. Medvedev, M. Stanciu, and M. Brudno Computational methods for discovering structural variation with next-generation sequencing Nat. Methods Suppl. 6 2009 S13 S20
42. H. Minami, J.S. Kim, N. Ikezawa, T. Takemura, T. Katayama, H. Kumagai, and F. Sato Microbial production of plant benzylisoquinoline alkaloids Proc. Natl. Acad. Sci. USA 105 2008 7393 7398
43. O. Morozova, M. Mirst, and M.A. Marra Applications of new sequencing technologies for transcriptome analysis Ann. Rev. Genomics Hum. Genet. 10 2009 135 151
44. A. Nakagawa, H. Minami, J.-S. Kim, T. Koyanagi, T. Katayama, F. Sato, and H. Kumagai A bacterial platform for fermentative production of plant alkaloids Nat. Commun 2011 10.1038/ncomms1327
45. S. Neumann, and S. Böcker Computational mass spectrometry for metabolomics: identification of metabolites and small molecules Anal. Bioanal. Chem. 398 2010 2779 2788
46. M.L. Nuccio, M.J. Ziemak, S.A. Henry, E.A. Weretilnyk, and A.D. Hanson CDNA cloning of phosphoethanolamine N-methyltransferase from spinach by complementation in Schizosaccharomyces pombe and characterization of the recombinant enzyme J. Biol. Chem. 275 2000 14095 14101
47. V.K. Phan, V.M. Chau, T.D. Nguyen, V.K. La, T.H. Dan, H.N. Nguyen, X.C. Nguyen, T.H. Hoang, and V.L. Trinh Aporphine alkaloids, clerodane diterpenes, and other constituents from Tinospora cordifolia Fitoterapia 81 2010 485 489
48. K. Raith, R. Neubert, C. Poeaknapo, C. Boettcher, M.H. Zenk, and J. Schmidt Electrospray tandem mass spectrometric investigations of morphinans J. Am. Soc. Mass Spectrom. 14 2003 1262 1269
49. L. Ren, X. Xue, F. Zhang, Q. Xu, and X. Liang High performance liquid chromatography-mass spectroscopy analysis of protoberberine alkaloids in medicine herbs J. Sep. Sci. 30 2007 833 842
50. N. Samanani, D.K. Liscombe, and P.J. Facchini Molecular cloning and characterization of norcoclaurine synthase, an enzyme catalyzing the first committed step in benzylisoquinoline alkaloid biosynthesis Plant J. 40 2004 302 313
51. N. Samanani, J. Alcantara, R. Bourgault, K.G. Zulak, and P.J. Facchini Role of sieve elements and laticifers in the biosynthesis and accumulation of alkaloids in opium poppy Plant J. 47 2006 547 564
52. J. Schmidt, K. Raith, C. Boettcher, and M.H. Zenk Analysis of benzylisoquinoline type alkaloids by electrospray tandem mass spectrometry and atmospheric pressure photoionization Eur. J. Mass Spectrom. 11 2005 325 334
53. 6]-tyramine feeding Phytochemistry 68 2007 189 202
54. H.-M. Schumacher, and M.H. Zenk Partial purification and characterization of dihydrobenzo[c]phenanthridine oxidase from Eschscholzia californica cell suspension cultures Plant Cell Rep. 7 1988 43 46
55. A.T. Shulgin, and W.E. Perry The Simple Plant Isoquinolines 2002 Transform Press Berkeley, CA
56. S. Sturm, E.-V. Strasser, and H. Stuppner Quantification of Fumaria officinalis isoquinoline alkaloids by nonaqueous capillary electrophoresis- electrospray ion trap mass spectrometry J. Chromatogr. A. 1112 2006 331 338
57. R. Suau, B. Cabezudo, M. Valpuesta, N. Posadas, A. Diaz, and G. Torres Identification and quantification of isoquinoline alkaloids in the genus Sarcocapnos by GC-MS Phytochem. Anal. 16 2005 322 327
58. S.E. Unger, A. Vincze, and R.G. Coks Identification of quaternary alkaloids in mushroom by chromatography/secondary ion mass spectrometry Anal. Chem. 53 1981 976 981
59. M. Vogel, M. Lawson, W. Sippl, U. Conrad, and W. Roos Structure and mechanism of sanguinarine reductase, an enzyme of alkaloid detoxification J. Biol. Chem. 285 2010 18397 18406
60. P.K. Wall, J. Leebens-Mack, A.S. Chanderbali, A. Barakat, E. Wolcott, H. Liang, L. Landherr, L.P. Tomsho, Y. Hu, J.E. Carlson, H. Ma, S.C. Schulster, D.E. Soltis, P.S. Soltis, N. Altman, and C.W. dePamphilis Comparison of next generation sequencing technologies for transcriptome characterization BMC Genomics 10 2010 347
61. W. Wang, A.-M. Lu, Y. Ren, M.E. Endress, and Z.-D. Chen Phylogeny and classification of Ranunculales: evidence from four molecular loci and morphological data Perspect. Plant Ecol. 11 2009 81 110
62. W.N. Wu, and C.-H. Huang Structural elucidation of isoquinoline, benzylisoquinoline, aporphine, and phenanthrene alkaloids using API-ionspray tandem mass spectrometry Chin. Pharm. J. 58 2006 41 55
63. n J. Pharm. Biomed. Anal. 37 2005 437 446
64. L.M. Zahn, X. Ma, N.S. Altman, Q. Zhang, P.K. Wall, D. Tian, C.J. Gibas, R. Gharaibeh, J.H. Leebens-Mack, C.W. dePamphilis, and H. Ma Comparative transcriptomics among floral organs of the basal eudicot Eschscholzia californica as reference for floral evolutionary development studies Genome Biol. 11 2010 R101
65. Y. Zhang, Q. Shi, P. Shi, W. Zhang, and Y. Cheng Characterization of isoquinoline alkaloids, diterpinoids and steroids in the Chinese herb Jin-Guo-Lan (Tinospora sagittata and Tinospora capillipes) by high-performance liquid chromatography/electrospray ionization with multistage mass spectrometry Rapid Commun. Mass Spectrom. 20 2006 2328 2342
66. J. Ziegler, and P.J. Facchini Alkaloid biosynthesis: metabolism and trafficking Annu. Rev. Plant Biol. 59 2008 735 769
67. K.G. Zulak, A. Cornish, T.E. Daskalchuk, M.K. Deyholos, D.B. Goodenowe, P.M. Gordon, D. Klassen, L.E. Pelcher, C.W. Sensen, and P.J. Facchini 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