Skip to main content
SpringerLink
Log in

Opium poppy: blueprint for an alkaloid factory

  • Original Paper
  • Published:
Phytochemistry Reviews Aims and scope Submit manuscript

Abstract

Opium poppy (Papaver somniferum) produces a large number of benzylisoquinoline alkaloids, including the narcotic analgesics morphine and codeine, and has emerged as one of the most versatile model systems to study alkaloid metabolism in plants. As summarized in this review, we have taken a holistic strategy—involving biochemical, cellular, molecular genetic, genomic, and metabolomic approaches—to draft a blueprint of the fundamental biological platforms required for an opium poppy cell to function as an alkaloid factory. The capacity to synthesize and store alkaloids requires the cooperation of three phloem cell types—companion cells, sieve elements, and laticifers—in the plant, but also occurs in dedifferentiated cell cultures. We have assembled an opium poppy expressed sequence tag (EST) database based on the attempted sequencing of more than 30,000 cDNAs from elicitor-treated cell culture, stem, and root libraries. Approximately 23,000 of the elicitor-induced cell culture and stem ESTs are represented on a DNA microarray, which has been used to examine changes in transcript profile in cultured cells in response to elicitor treatment, and in plants with different alkaloid profiles. Fourier transform-ion cyclotron resonance mass spectrometry and proton nuclear magnetic resonance mass spectroscopy are being used to detect corresponding differences in metabolite profiles. Several new genes involved in the biosynthesis and regulation of alkaloid pathways in opium poppy have been identified using genomic tools. A biological blueprint for alkaloid production coupled with the emergence of reliable transformation protocols has created an unprecedented opportunity to alter the chemical profile of the world’s most valuable medicinal plant.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

Abbreviations

4′OMT:

(R,S)-3′-hydroxy-N-methylcoclaurine 4′-O-methyltransferase

6OMT:

(R,S)-norcoclaurine 6-O-methyltransferase

7OMT:

(R,S)-reticuline 7-O-methyltransferase

BBE:

Berberine bridge enzyme

BIA:

Benzylisoquinoline alkaloid

CDO:

(S)-canadine oxidase

CFS:

(S)-cheilanthifoline synthase

CNMT:

(R,S)-coclaurine N-methyltransferase

COR:

Codeinone reductase

CYP719A1:

(S)-canadine synthase

CYP80B1:

(S)-N-methylcoclaurine 3′-hydroxylase

DBOX:

Dihydrobenzophenanthridine oxidase

DRS:

1,2-Dehydroreticuline synthase

DRR:

1,2-Dehydroreticuline reductase

dsRNA:

Double-stranded RNA

EMS:

Ethylmethane sulfonate

ER:

Endoplasmic reticulum

EST:

Expressed sequence tag

FT-ICR MS:

Fourier transform-ion cyclotron resonance mass spectrometry

GST:

Glutathione S-transferase

H1-NMR:

Proton nuclear magnetic resonance mass spectroscopy

HSS:

Homospermidine synthase

LC-MS/MS:

Liquid chromatography-tandem mass spectrometry

MSH:

(S)-N-methylstylopine 14-hydroxylase

NCS:

(S)-norcoclaurine synthase

PCR:

Polymerase chain reaction

P6H:

Protopine 6-hydroxylase

PNMT:

Putrescine N-methyltransferase

PTGS:

Post-transcriptional gene silencing

RNAi:

RNA interference

SAM:

(S)-adenosylmethionine

SAT:

Salutaridinol-7-O-acetyltransferase

SER:

Sieve element reticulum

siRNA:

RNA

SOMT:

(S)-scoulerine 9-O-methyltransferase

SOR:

Salutaridine:NADPH 7-oxidoreductase

SPS:

(S)-stylopine synthase

STOX:

(S)-tetrahydroprotoberberine oxidase

STR:

Strictosidine synthase

STS:

Salutaridine synthase

TDC:

Tryptophan decarboxylase

TILLING:

Targeting induced local lesions in genomes

TYDC:

Tyrosine decarboxylase

TNMT:

(S)-tetrahydroprotoberberine-cis-N-methyltransferase

TRV:

Tobacco rattle virus

VIGS:

Viral-induced gene silencing

References

  • Alcantara J, Bird DA, Francheschi VR, Facchini PJ (2005) Sanguinarine biosynthesis is associated with endoplasmic reticulum in cultured opium poppy cells after elicitor treatment. Plant Physiol 138:173–183

    Article  PubMed  CAS  Google Scholar 

  • Allen RS, Millgate AG, Chitty JA, Thisleton J, Miller JAC, Fist AG, Gerlach WA, Larkin PJ (2004) RNAi-mediated replacement of morphine with the nonnarcotic alkaloid reticuline in opium poppy. Nat Biotechnol 22:1559–1566

    Article  PubMed  CAS  Google Scholar 

  • Alosi MC, Melroy DL, Park PB (1988) The regulation of gelatin of phloem exudate from Cucurbita fruit by dilution, glutathione, and glutathione reductase. Plant Physiol 86:1089–1094

    PubMed  CAS  Google Scholar 

  • Amann M, Wanner G, Zenk MH (1986) Intracellular compartmentation of two enzymes of berberine biosynthesis in plant cell cultures. Planta 167:310–320

    Article  CAS  Google Scholar 

  • Andréasson E, Jørgensen LB, Høoglund A-S, Rask L, Meijer J (2001) Different myrosinase and idioblast distribution in Arabidopsis and Brassica napus. Plant Physiol 127:1750–1763

    Article  PubMed  Google Scholar 

  • Anke S, Niemüller D, Moll S, Hänsch R, Ober D (2004) Polyphyletic origin of pyrrolizidine alkaloids within the Asteraceae: evidence from differential tissue expression of homospermidine synthase. Plant Physiol 136:4037–4047

    Article  PubMed  CAS  Google Scholar 

  • Antti H, Bollard ME, Ebbels T, Keun H, Lindon JC, Nicholson, Holmes E (2002) Batch statistical processing of 1H NMR-derived urinary spectral data. J Chemometr 16:461–468

    Article  CAS  Google Scholar 

  • Arakawa H, Clark WC, Psenak M, Coscia CJ (1992) Purification and characterization of dihydrobenzophenanthridine oxidase from Sanguinaria canadensis cell cultures. Arch Biochem Biophys 299:1–7

    Article  PubMed  CAS  Google Scholar 

  • Barnes A, Bale J, Constantinidou C, Ashton P, Jones A, Pritchard J (2004) Determining protein identity from sieve element sap in Ricinis communis L. by quadrupole time of flight (Q-TOF) mass spectrometry. J Exp Bot 55:1473–1481

    Article  PubMed  CAS  Google Scholar 

  • Battersby AR, Hirst M, McCaldin R, Southgate R, Staunton J (1968) Alkaloid biosynthesis. Part XII. The biosynthesis of narcotine. J Chem Soc 17:2163–2172

    CAS  Google Scholar 

  • Bauer W, Zenk MH (1989) Formation of both methylenedioxy groups in the alkaloid (S)-stylopine is catalyzed by cytochrome P-450 enzymes. Tetrahedron Lett 30:5257–5260

    Article  CAS  Google Scholar 

  • Bauer W, Zenk MH (1991) Two methylenedioxy bridge forming cytochrome P-450 dependent enzymes are involved in (S)-stylopine biosynthesis. Phytochemistry 30:2953–2962

    Article  CAS  Google Scholar 

  • Belny M, Hérouart D, Thomasset B, David H, Jacquin-Dubreuil A, David A (1997) Transformation of Papaver somniferum cell suspension cultures with sam1 from A. thaliana results in cell lines of different S-adenosyl-l-methionine synthetase activity. Physiol Plant 99:233–240

    Article  CAS  Google Scholar 

  • Bino RJ, Hall RD, Feihn O, Kopka J, Saito K, Draper J, Nikolau BJ, Mendes P, Roessner-Tunali U, Beale MH, Trethewey RN, Lange BM, Wurtele ES, Sumner LW (2004) Potential of metabolomics as a functional genomics tool. Trends Plant Sci 9:418–425

    Article  PubMed  CAS  Google Scholar 

  • Bird DA, Facchini PJ (2001) Berberine bridge enzyme, a key branch-point enzyme in benzylisoquinoline alkaloid biosynthesis, contains a vacuolar sorting determinant. Planta 213:888–897

    PubMed  CAS  Google Scholar 

  • Bird DA, Francheschi VR, Facchini PJ (2003) A tale of three cell-types: alkaloid biosynthesis is localized to sieve elements in opium poppy. Plant Cell 15:2626–2635

    Article  PubMed  CAS  Google Scholar 

  • Bock A, Wanner G, Zenk MH (2002) Immunocytological localization of two enzymes involved in berberine biosynthesis. Planta 216:57–63

    Article  PubMed  CAS  Google Scholar 

  • Bourgault R, Zulak KG, Facchini PJ (2005) Applications of genomics in plant biology. In: Sensen CW (ed) Handbook of genome research: genomics, proteomics, metabolomics, bioinformatics, ethical and legal issues. WILEY-VCH Verlag GmbH & Co., KGaA, Weinheim Germany, pp 59–80

    Google Scholar 

  • Broeckling CD, Huhman DV, Farag MA, Smith JT, May GD, Mendes P, Dixon RA, Sumner LW (2004) Metabolic profiling of Medicago truncatula cell cultures reveals effects of biotic and abiotic elicitors on metabolism. J Exp Bot 56:323–336

    Article  PubMed  CAS  Google Scholar 

  • Burlat V, Oudin A, Courtois M, Rideau M, St-Pierre B (2004) Co-expression of three MEP pathway genes and geraniol 10-hydroxylase in internal phloem parenchyma of Catharanthus roseus implicates multicellular translocation of intermediates during the biosynthesis of monoterpene indole alkaloids and isoprenoid-derived primary metabolites. Plant J 38:131–141

    Article  PubMed  CAS  Google Scholar 

  • Cantrill LC, Overall RL, Goodwin PB (1999) Cell-to-cell communication via plant endomembranes. Cell Biol Int 23:653–661

    Article  PubMed  CAS  Google Scholar 

  • Chitty JA, Allen RS, Fist AJ, Larkin PJ (2003) Genetic transformation in commercial Tasmanian cultivars of opium poppy, Papaver somniferum, and movement of transgenic pollen in the field. Funct Plant Biol 30:1045–1058

    Article  CAS  Google Scholar 

  • Choi KB, Morishige T, Sato F (2001) Purification and characterization of coclaurine N-methyltransferase from cultured Coptis japonica cells. Phytochemistry 56:649–655

    Article  PubMed  CAS  Google Scholar 

  • Choi KB, Morishige T, Shitan N, Yazaki K, Sato F (2002) Molecular cloning and characterization of coclaurine N-methyltransferase from cultured cells of Coptis japonica. J Biol Chem 277:830–835

    Article  PubMed  CAS  Google Scholar 

  • Choi YH, Tapias EC, Kim HK, Lefeber AW, Erkelens C, Verhoeven JT, Brzin J, Zel J, Verpoorte R (2004a) Metabolic discrimination of Catharanthus roseus leaves infected by phytoplasma using 1H-NMR spectroscopy and multivariate data analysis. Plant Physiol 135:2398–2410

    Article  CAS  Google Scholar 

  • Choi YH, Hazekamp A, Peltenburg-Looman AMG, Frédérich M, Erkelens C, Lefeber AWM, Verpoorte R (2004b) NMR assignments of the major cannabinoids and cannabiflavonoids isolated from flowers of Cannabis sativa. Phytochem Anal 15:345–354

    Article  CAS  Google Scholar 

  • Chou WM, Kutchan TM (1998) Enzymatic oxidations in the biosynthesis of complex alkaloids. Plant J 15:289–300

    Article  PubMed  CAS  Google Scholar 

  • Dean JD, Goodwin PH, Hsiang T (2005) Induction of gluathione S-transferase genes of Nicotiana benthamiana following induction by Colletotrichum destructivum and C. obiculare and involvement of one in resistance. J Exp Bot 56:1525–1533

    Article  PubMed  CAS  Google Scholar 

  • Decker G, Wanner G, Zenk MH, Lottspeich F (2000) Characterization of proteins in latex of the opium poppy (Papaver somniferum) using two-dimensional gel electrophoresis and microsequencing. Electrophoresis 21:3500–3516

    Article  PubMed  CAS  Google Scholar 

  • De-Eknamkul W, Zenk MH (1992) Purification and properties of 1,2-dehydroreticuline reductase from Papaver somniferum seedlings. Phytochemistry 31:813–821

    CAS  Google Scholar 

  • Defernez M, Colquhoun IJ (2003) Factors affecting the robustness of metabolic fingerprinting using 1H NMR spectra. Phytochemistry 62:1009–1017

    Article  PubMed  CAS  Google Scholar 

  • Dieu P, Dunwell JM (1988) Anther culture with different genotypes of opium poppy (Papaver somniferum): effect of cold treatment. Plant Cell Tiss Organ Cult 12:263–271

    Article  Google Scholar 

  • Dittrich H, Kutchan TM (1991) Molecular cloning, expression, and induction of berberine bridge enzyme, an enzyme essential to the formation of benzophenanthridine alkaloids in the response of plants to pathogenic attack. Proc Natl Acad Sci USA 88:9969–9973

    Article  PubMed  CAS  Google Scholar 

  • Dubouzet JG, Morishige T, Fujii N, An CI, Fukusaki EI, Ifuku K, Sato F (2005) Transient RNA silencing of scoulerine 9-O-methyltransferase expression by double stranded RNA in Coptis japonica protoplasts. Biosci Biotechnol Biochem 69:63–70

    Article  PubMed  CAS  Google Scholar 

  • Eilert U, Kurz WGW, Constabel F (1985) Stimulation of sanguinarine accumulation in Papaver somniferum cell cultures by fungal elicitors. J Plant Physiol 119:65–76

    CAS  Google Scholar 

  • Facchini PJ (2001) Alkaloid biosynthesis in plants: biochemistry, cell biology, molecular regulation, and metabolic engineering applications. Annu Rev Plant Physiol Plant Mol Biol 52:29–56

    Article  PubMed  CAS  Google Scholar 

  • Facchini PJ, Bird DA, St-Pierre B (2004) Can Arabidopsis make complex alkaloids? Trends Plant Sci 9:116–122

    Article  PubMed  CAS  Google Scholar 

  • Facchini PJ, De Luca V (1994) Differential and tissue-specific expression of a gene family for tyrosine/dopa decarboxylase in opium poppy. J Biol Chem 269:16684–26690

    Google Scholar 

  • Facchini PJ, De Luca V (1995) Phloem-specific expression of tyrosine/dopa decarboxylase genes and the biosynthesis of isoquinoline alkaloids in opium poppy. Plant Cell 7:1811–1821

    Article  PubMed  CAS  Google Scholar 

  • Facchini PJ, Huber-Allanach KL, Tari LW (2000) Plant aromatic l-amino acid decarboxylases: evolution, biochemistry, regulation, and metabolic engineering applications. Phytochemistry 54:121–138

    Article  PubMed  CAS  Google Scholar 

  • Facchini PJ, Johnson AC, Poupart J, De Luca V (1996a) Uncoupled defense gene expression and antimicrobial alkaloid accumulation in elicited opium poppy cell cultures. Plant Physiol 111:687–697

    Article  CAS  Google Scholar 

  • Facchini PJ, Park SU (2003) Developmental and inducible accumulation of gene transcripts involved in alkaloid biosynthesis in opium poppy. Phytochemistry 64:177–186

    Article  PubMed  CAS  Google Scholar 

  • Facchini PJ, Penzes C, Johnson AG, Bull D (1996b) Molecular characterization of berberine bridge enzyme genes from opium poppy. Plant Physiol 112:1669–1677

    Article  CAS  Google Scholar 

  • Fan TW-M, Lane AN, Shenker M, Bartley JP, Crowley D, Higashi RM (2001) Comprehensive chemical profiling of gramineous plant root exudates using high-resolution NMR and MS. Phytochemistry 57:209–221

    Article  PubMed  CAS  Google Scholar 

  • Frederich M, Choi YH, Angenot L, Harnischfeger G, Lefeber AWM, Verpoorte R (2004) Metabolomic analysis of Strychnos nux-vomica, Strychnos icaja and Strychnos ignatii extracts by 1H nuclear magnetic resonance spectrometry and multivariate analysis techniques. Phytochemistry 65:1993–2001

    Article  PubMed  CAS  Google Scholar 

  • Frenzel T, Zenk MH (1990) S-Adenosyl-l-methionine:3′-hydroxy-N-methyl-(S)-coclaurine 4′-O-metyltransferase, a regio-and stereoselective enzyme of the (S)-reticuline pathway. Phytochemistry 29:3505–3511

    Article  CAS  Google Scholar 

  • Frick S, Chitty JA, Kramell R, Schmidt J, Allen RS, Larkin PJ, Kutchan TM (2004) Transformation of opium poppy (Papaver somniferum L.) with antisense berberine bridge enzyme gene (anti-bbe) via somatic embryogenesis results in an altered ratio of alkaloids in latex but not in roots. Trans Res 13:607–613

    Article  CAS  Google Scholar 

  • Frick S, Kramell R, Schmidt J, Fist AJ, Kutchan TM (2005) Comparative qualitative and quantitative determination of alkaloids in narcotic and condiment Papaver somniferum cultivars. J Nat Prod 68:666–673

    Article  PubMed  CAS  Google Scholar 

  • Gachon CMM, Langlois-Meurinne M, Henry Y, Saindrenan P (2005) Transcriptional co-regulation of secondary metabolism enzymes in Arabidopsis: functional and evolutionary implications. Plant Mol Biol 58:229–245

    Article  PubMed  CAS  Google Scholar 

  • Galneder E, Rueffer M, Wanner G, Tabata M, Zenk MH (1988) Alternative final steps in berberine biosynthesis in Coptis japonica cell cultures. Plant Cell Rep 7:1–4

    Article  CAS  Google Scholar 

  • Gang DR, Wang J, Dudareva N, Nam K, Simon JE, Lewinsohn E, Pichersky E (2001) An investigation of the storage and biosynthesis of phenylpropenes in sweet basil. Plant Physiol 125:539–555

    Article  PubMed  CAS  Google Scholar 

  • Gerardy R, Zenk MH (1993a) Purification and characterization of salutaridine: NADPH 7-oxidoreductase from Papaver somniferum. Phytochemistry 34:125–132

    Article  CAS  Google Scholar 

  • Gerardy R, Zenk MH (1993b) Formation of salutaridine from (R)-reticuline by a membrane-bound cytochrome P-450 enzyme from Papaver somniferum. Phytochemistry 32:79–86

    Article  Google Scholar 

  • Ghiorghita G, Elvira I, Gille V, Ecaterina J, Toth J (1982) Gamma radiation, ethylmethansulfonate and diethylsulfate treatments induced changes in morphine content and other biochemical parameters in Papaver somniferum. Rev Roum Biol Ser Biol Veg 27:121

    CAS  Google Scholar 

  • Gomes E, Sagot E, Gaillard C, Laquitane L, Ponssot B, Sanejouand Y-H, Delrot S, Coutos-Thevenot P (2003) Nonspecific lipid-transfer protein genes expression in grape (Vitis sp.) cells in response to fungal elicitor treatments. Mol Plant Microbe Interact 16:456–464

    PubMed  CAS  Google Scholar 

  • Gozler B, Gozler T, Shamma M (1983) Egenine: a possible intermediate in phthalideisoquinoline biogenesis. Tetrahedron 39:577–580

    Article  Google Scholar 

  • Greene EA, Codomo CA, Taylor NE, Henikoff JG, Till BJ, Reynolds SH, Enns LC, Burtner C, Johnson JE, Odden AR, Comai L, Henikoff S (2003) Spectrum of chemically induced mutations from a large-scale reverse-genetic screen in Arabidopsis. Genetics 164:731–740

    PubMed  CAS  Google Scholar 

  • Grothe T, Lenz R, Kutchan TM (2001) Molecular characterization of the salutaridinol 7-O-acetyltransferase involved in morphine biosynthesis in opium poppy Papaver somniferum. J Biol Chem 276:30717–30723

    Article  PubMed  CAS  Google Scholar 

  • Grover IS, Dhanju MS (1979) Effect of gamma radiation on the germination of Papaver somniferum and P. rhoeas. Ind J Plant Physiol 22:75

    Google Scholar 

  • Guterman I, Shalit M, Menda N, Piestun D, Dafny-Yelin M, Shalev G, Bar E, Davydov O, Ovadis M, Emanuel M, Wang J, Adam Z, Pichersky E, Lewinsohn E, Zamir D, Vainstein A, Weiss D (2002) Rose scent: genomics approach to discovering novel floral fragrance-related genes. Plant Cell 14:2325–2338

    Article  PubMed  CAS  Google Scholar 

  • Hancock RD, McRae D, Haupt S, Viola R (2003) Synthesis of l-ascorbic acid in the phloem. BMC Plant Biol 3:7

    Article  PubMed  Google Scholar 

  • Hashimoto T, Hayashi A, Amano Y, Kohno J, Iwanari H, Usuda S, Yamada Y (1991) Hyoscyamine 6β-hydroxylase, an enzyme involved in tropane alkaloid biosynthesis, is localized at the pericycle of the root. J Biol Chem 266:4648–4653

    PubMed  CAS  Google Scholar 

  • Hauschild K, Pauli HH, Kutchan TM (1998) Isolation and analysis of a gene bbe1 encoding the berberine bridge enzyme from the California poppy Eschscholzia californica. Plant Mol Biol 36:473–478

    Article  PubMed  CAS  Google Scholar 

  • Hause B, Hause G, Kutter C, Miersch O, Wasternack C (2003) Enzymes of jasmonate biosynthesis occur in tomato sieve elements. Plant Cell Physiol 44:643–648

    Article  PubMed  CAS  Google Scholar 

  • Helliwell CA, Waterhouse PM (2005) Constructs and methods for hairpin RNA-mediated gene silencing in plants. Methods Enzymol 392:24–35

    PubMed  CAS  Google Scholar 

  • Henikoff S, Comai L (2003) Single-nucleotide mutations for plant functional genomics. Annu Rev Plant Biol 54:375–401

    Article  PubMed  CAS  Google Scholar 

  • Hileman LC, Drea S, Martino G, Litt A, Irish VF (2005) Virus-induced gene silencing is an effective tool for assaying gene function in the basal eudicot species Papaver somniferum (opium poppy). Plant J 44:334–341

    Article  PubMed  CAS  Google Scholar 

  • Hirata K, Poeaknapo C, Schmidt J, Zenk MH (2004) 1,2-Dehydroreticuline synthase, the branch point enzyme opening the morphinan biosynthetic pathway. Phytochemistry 65:1039–1046

    Article  PubMed  CAS  Google Scholar 

  • Huang FC, Kutchan TM (2000) Distribution of morphinan and benzo[c]phenanthridine alkaloid gene transcript accumulation in Papaver somniferum. Phytochemistry 53:555–564

    Article  PubMed  CAS  Google Scholar 

  • Ikezawa N, Tanaka M, Nagayoshi M, Shinkyo R, Sakaki T, Inouye K, Sato F (2003) 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 278:38557–38565

    Article  PubMed  CAS  Google Scholar 

  • Ilahi I, Ghauri EG (1994) Regeneration in cultures of Papaver bracteatum as influenced by growth hormones and temperature. Plant Cell Tiss Organ Cult 38:81–83

    Article  CAS  Google Scholar 

  • Ilieva S, Mekhandzhier A, Mateeva D, Dimitrova S (1975) Biological and biochemical changes in P. somniferum L. under the influence of ionizing radiation. Herba Polonica 21:412

    Google Scholar 

  • Irmler S, Schröder G, St-Pierre B, Crouch NP, Hotze M, Schmidt J, Strack D, Matern U, Schröder J (2000) Indole alkaloid biosynthesis in Catharanthus roseus: new enzyme activities and identification of cytochrome P450 CYP72A1 as secologanin synthase. Plant J 24:797–804

    Article  PubMed  CAS  Google Scholar 

  • Iwasa K, Kamigauchi M (1996) 13-hydroxylation of tetrahydroberberine in cell suspension cultures of some Corydalis species. Phytochemistry 41:1511–1515

    Article  CAS  Google Scholar 

  • Junghanns KT, Kneusel RE, Gröger D, Matern U (1998) Differential regulation and distribution of acridone synthase in Ruta graveolens. Phytochemistry 49:403–411

    Article  PubMed  CAS  Google Scholar 

  • Kalde M, Barth M, Somssich IE, Lippok B (2003) Members of the Arabidopsis WRKY group III transcription factors are part of different plant defense signaling pathways. Mol Plant Microbe Interact 16:295–305

    PubMed  CAS  Google Scholar 

  • Kammerer L, De-Eknamkul W, Zenk MH (1994) Enzymatic 12-hydroxylation and 12-O-methylation of dihydrochelirubine in dihydromacarpine formation by Thalictrum bulgaricum. Phytochemistry 36:1409–1416

    Article  CAS  Google Scholar 

  • Kassemi MA, Jacquin A (2001) Somatic embryogenesis, rhizogenesis, and morphinan alkaloids production in two species of opium poppy. J Biomed. Biotechnol 1/2:70–78

    Article  Google Scholar 

  • Kehr J, Haebel S, Blechschmidt-Schneider S, Willmitzer L, Steup M, Fisahn J (1999) Analysis of phloem protein patterns from different organs of Cucurbita maxima Duch. by matrix-assisted laser desorption/ionization time of flight mass spectroscopy combined with sodium dodecyl sulfate-polyacrylamide gel electrophoresis. Planta 207:612–619

    Article  PubMed  CAS  Google Scholar 

  • Khanna KR, Singh UP (1971) Genetic effect of irradiation on opium poppy (P. somniferum). Sci Cult 26:556

    Google Scholar 

  • Khanna R, Mathur AK, Mehrotra NK (2005) Selection of 3-fluorotyrosine tolerant callus lines in two cultivars of opium poppy (Papaver somniferum L.) and regeneration of plants through somatic embryogenesis. Curr Sci 88:274–280

    CAS  Google Scholar 

  • Kim HK, Choi YH, Erkelens C, Lefeber AWM, Verpoorte R (2004a) Metabolic fingerprinting of Ephedra species using 1H-NMR spectroscopy and principal component analysis. Chem Pharm Bull 53:105–109

    Article  Google Scholar 

  • Kim HK, Choi YH, Luijendijk TJC, Vera Rocha RA, Verpoorte R (2004b) Comparison of extraction methods for secologanin and the quantitative analysis of secologanin from Symphoricarpos albus using 1H-NMR. Phytochem Anal 15:257–261

    Article  CAS  Google Scholar 

  • Koornneef M, Dellaert LWM, van der Veen JH (1982) EMS-and relation-induced mutation frequencies at individual loci in Arabidopsis thaliana (L.) Heynh. Mutation Res 93:109–123

    PubMed  CAS  Google Scholar 

  • Kraus PFX, Kutchan TM (1995) Molecular cloning and heterologous expression of a cDNA encoding berbamunine synthase, a C−O phenol-coupling cytochrome P-450 from the higher plant Berberis stolonifera. Proc Natl Acad Sci USA 92:2071–2075

    Article  PubMed  CAS  Google Scholar 

  • Kutchan TM, Bock A, Dittrich H (1994) Heterologous expression of strictosidine synthase and berberine bridge enzyme in insect cell culture. Phytochemistry 35:353–360

    Article  PubMed  CAS  Google Scholar 

  • Kutchan TM, Dittrich H (1995) Characterization and mechanism of the berberine bridge enzyme, a covalently flavinylated oxidase of benzophenanthridine alkaloid biosynthesis in higher plants. J Biol Chem 270:24475–24481

    Article  PubMed  CAS  Google Scholar 

  • Lange MB, Wildung MR, Stauber EJ, Sanchez C, Pouchnik D, 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

    Article  PubMed  CAS  Google Scholar 

  • Le Flem-Bonhomme V, Laurain-Mattar D, Fliniaux MA (2004) Hairy root induction of Papaver somniferum var. album, a difficult-to-transform plant, by A. rhizogenes LBA 9402. Planta 218:890–893

    Article  PubMed  CAS  Google Scholar 

  • Lei Z, Elmer AM, Watson BS, Dixon RA, Mendez, PJ, Sumner LW (2005) A two-dimentional electrophoresis proteomic reference map and systematic identification of 1367 proteins from a cell suspension culture of the model legume Medicago truncatula. Mol Cell Proteomics 4:1812–1825

    Article  PubMed  CAS  Google Scholar 

  • Lenz R, Zenk MH (1995a) Acetyl coenzyme A:salutaridinol-7-O-acetyltransferase from Papaver somniferum plant cell cultures. J Biol Chem 270:31091–31096

    Article  CAS  Google Scholar 

  • Lenz R, Zenk MH (1995b) Purification and properties of codeinone reductase (NADPH) from Papaver somniferum cell cultures and differentiated plants. Eur J Biochem 233:132–139

    Article  CAS  Google Scholar 

  • Li X, Song Y, Century K, Straight S, Ronald P, Dong X, Lassner M, Zhang Y (2001) A fast neutron deletion mutagenesis-based reverse genetics system for plants. Plant J 27:235–242

    Article  PubMed  CAS  Google Scholar 

  • Liscombe DK, Macleod BP, Loukanina N, Nandi OI, Facchini PJ (2005) Evidence for the monophyletic evolution of benzylisoquinoline alkaloid biosynthesis in angiosperms. Phytochemistry 66:1374–1393

    Article  PubMed  CAS  Google Scholar 

  • Logemann E, Tavernaro A, Schulz W, Somssich IE, Hahlbrock K (2000) UV light selectively coinduces supply pathways from primary metabolism and flavonoid secondary product formation in parsley. Proc Natl Acad Sci USA 97:1903–1907

    Article  PubMed  CAS  Google Scholar 

  • Lucas WJ, Yoo B-C, Kragler F (2001) RNA as a long-distance information macromolecule in plants. Nature Rev 2:849–857

    Article  CAS  Google Scholar 

  • Ma WG, Fukushi Y, Tahara S, Osawa T (2000) Fungitoxic alkaloids from Hokkaido Papaveraceae. Fitoterapia, 71:527–534

    Article  PubMed  CAS  Google Scholar 

  • Mahady GB, Beecher CW (1994) Elicitor-stimulated benzophenanthridine alkaloid biosynthesis in bloodroot suspension cultures is mediated by calcium. Phytochemistry 37:415–419

    Article  CAS  Google Scholar 

  • Mahady GB, Liu C, Beecher CWW (1998) Involvement of protein kinase and G proteins in the signal transduction of benzophenanthridine alkaloid biosynthesis. Phytochemistry 48:93–102

    Article  PubMed  CAS  Google Scholar 

  • Maldonado AM, Doerner P, Dixon RA, Lamb CJ, Cameron RK (2002) A putative lipid transfer protein involved in systemic resistance signalling in Arabidopsis. Nature 419:399–403

    Article  PubMed  CAS  Google Scholar 

  • McCallum CM, Comai L, Greene EA, Henikoff S (2000a) Targeted screening for induced mutations. Nat Biotechnol 18:455–457

    Article  CAS  Google Scholar 

  • McCallum CM, Comai L, Greene EA, Henikoff S (2000b) Targeting Induced Local Lesions IN Genomes (TILLING) for plant functional genomics. Plant Physiol 123:439–442

    Article  CAS  Google Scholar 

  • Menke FLH, Parchmann S, Mueller MJ, Kijne JW, Memelink J (1999a) Involvement of the octadecanoid pathway and protein phosphorylation in fungal elicitor-induced expression of terpenoid indole alkaloid biosynthetic genes in Catharanthus roseus. Plant Physiol 119:1289–1296

    Article  PubMed  CAS  Google Scholar 

  • Menke FLH, Champion A, Kijne JW, Memelink J (1999b) A novel jasmonate-and elicitor-responsive element in the periwinkle secondary metabolite biosynthetic gene Str interacts with a jasmonate-and elicitor-inducible AP2-domain transcription factor, ORCA2. EMBO J 18:4455–4463

    Article  CAS  Google Scholar 

  • Millgate AG, Pogson BJ, Wilson IW, Kutchan TM, Zenk MH, Gerlach WI, Fist AJ, Larkin PJ (2004) Morphine-pathway block in top1 poppies. Nature 431:413–414

    Article  PubMed  CAS  Google Scholar 

  • Moll S, Anke S, Kahmann U, Hansch R, Hartmann T, Ober D (2002) Cell-specific expression of homospermidine synthase, the entry enzyme of the pyrrolizidine alkaloid pathway in Senecio vernalis, in comparison with its ancestor, deoxyhypusine synthase. Plant Physiol 130:47–57

    Article  PubMed  CAS  Google Scholar 

  • Moniot JL, Shamma M (1976) The conversion of berberine into (±)−α-and (±)−β-hydrastine. J Am Chem Soc 98:6714–6715

    Article  PubMed  CAS  Google Scholar 

  • Morimoto S, Suemori K, Moriwaki J, Taura F, Tanaka H, Aso M, Tanaka M, Suemune H, Shimorhigashi Y, Shoyama Y (2001) Morphine in the opium poppy and its possible physiological function—biochemical characterization of the morphine metabolite, bismorphine. J Biol Chem 276:38179–38184

    Article  PubMed  CAS  Google Scholar 

  • Morishige T, Tsujita T, Yamada Y, Sato F (2000) Molecular characterization of the S-adenosyl-l-methionine: 3′-hydroxy-N-methylcoclaurine-4′-O-methyltransferase of isoquinoline alkaloid biosynthesis in Coptis japonica. J Biol Chem 275:23398–23405

    Article  PubMed  CAS  Google Scholar 

  • Morteza-Semnani K, Amin G, Shidfar MR, Hadizadeh H, Shafiee A (2003) Antifungal activity of the methanolic extract and alkaloids of Glaucium oxylobum. Fitoterapia 74:493–496

    Article  PubMed  CAS  Google Scholar 

  • Muemmler S, Rueffer M, Nagakura N, Zenk MH (1985) S-Adenosyl-l-methionine: (S)-scuolerine 9-O-methyltransferase, a highly stereo-and regio-specific enzyme in tetrahydroprotoberberine biosynthesis. Plant Cell Rep 4:36–39

    Article  CAS  Google Scholar 

  • Murata J, De Luca V (2005) Localization of tabersonine 16-hydroxylase and 16-OH tabersonine-16-O-methyltransferase to leaf epidermal cells defines them as a major site of precursor biosynthesis in the vindoline pathway in Catharanthus roseus. Plant J 44:581–594

    Article  PubMed  CAS  Google Scholar 

  • Nakajima K, Hashimoto T (1999) Two tropinone reductases, that catalyze opposite stereospecific reductions in tropane alkaloid biosynthesis, are localized in plant root with different cell-specific patterns. Plant Cell Physiol 40:1099–1107

    PubMed  CAS  Google Scholar 

  • Nam MH, Kim SI, Liu JR, Yang DC, Lim YP, Kwan K-H, Yoo JS, Park YM (2005) Proteomic analysis of Korean ginseng (Panax ginseng C.A. Meyer). J Chromatogr B 815:147–155

    Article  CAS  Google Scholar 

  • Nessler CL, Mahlberg PG (1977) Ontogeny and cytochemistry of alkaloidal vesicles in laticifers of Papaver somniferum L. (Papaveraceae). Am J Bot 64:541–551

    Article  Google Scholar 

  • Nessler CL (1982) Somatic embryogenesis in opium poppy, Papaver somniferum. Physiol Plant 55:453–458

    Article  Google Scholar 

  • Noutoshi Y, Ito T, Seki M, Nakashita H, Yoshida S, Marco Y, Shirasu K, Shinozaki K (2005) A single amino acid insertion in the WRKY domain of the Aribidopsis TIR-NBS-LRR-WRKY-type disease resistance protein SLH1 (sensitive to low humidity 1) causes activation of defense responses and hypersensitive cell death. Plant J 43:873–888

    Article  PubMed  CAS  Google Scholar 

  • Nyman U (1980) Selection for high thebaine/low morphine content in Papaver somniferum. L. Hereditas 93:121–124

    Article  CAS  Google Scholar 

  • O’Keefe BR, Beecher CWW (1994) Isolation and characterization of S-adenosyl-l-methionine:tetrahydroberberine-cis-N-methyltransferase from suspension cultures of Sanguinaria canadensis L. Plant Physiol 105:395–403

    PubMed  CAS  Google Scholar 

  • Oparka KJ, Turgeon R (1999) Sieve elements and companion cells—traffic control centers of the phloem. Plant Cell 11:739–750

    Article  PubMed  CAS  Google Scholar 

  • Østergaard L, Yanofsky MF (2004) Establishing gene function by mutagenesis in Arabidopsis thaliana. Plant Physiol 39:682–696

    Google Scholar 

  • Ounaroon A, Decker G, Schmidt J, Lottspeich F, Kutchan TM (2003) (R,S)-Reticuline 7-O-methyltransferase and (R,S)-norcoclaurine 6-O-methyltransferase of Papaver somniferum-cDNA cloning and characterization of methyl transfer enzymes of alkaloid biosynthesis in opium poppy. Plant J 36:808–819

    Article  PubMed  CAS  Google Scholar 

  • Ovecka M, Bobak M, Blehova A, Kristin J (1997) Papaver somniferum regeneration by somatic embryogenesis and shoot organogenesis. Biol Plant 40:321–328

    Article  Google Scholar 

  • Ovecka M, Bobak M, Samaj J (2000) A comparative structural analysis of direct and indirect shoot regeneration of Papaver somniferum L. in vitro. J Plant Physiol 157:281–289

    CAS  Google Scholar 

  • Park SU, Facchini PJ (1999) High-efficiency somatic embryogenesis and plant regeneration in California poppy, Eschscholzia californica. Chem Plant Cell Rep 19:421–426

    Article  Google Scholar 

  • Park SU, Facchini PJ (2000a) Agrobacterium-mediated transformation of opium poppy, Papaver somniferum L., via shoot organogenesis. J Plant Physiol 157:207–214

    CAS  Google Scholar 

  • Park SU, Facchini PJ (2000b) Agrobacterium rhizogenes-mediated transformation of opium poppy, Papaver somniferum L., and California poppy, Eschscholzia californica Cham., root cultures. J Exp Bot 51:1005–1016

    Article  CAS  Google Scholar 

  • Park SU, Facchini PJ (2000c) Agrobacterium-mediated genetic transformation of California poppy, Eschscholzia californica Cham., via somatic embryogenesis. Plant Cell Rep 19:1006–1012

    Article  CAS  Google Scholar 

  • Park SU, Johnson AG, Penzes-Yost C, Facchini PJ (1999) Analysis of promoters from tyrosine/dihydroxyphenylalanine decarboxylase and berberine bridge enzyme genes involved in benzylisoquinoline alkaloid biosynthesis in opium poppy. Plant Mol Biol 40:121–131

    Article  PubMed  CAS  Google Scholar 

  • Park SU, Facchini PJ (2001) Somatic embryogenesis from embryogenic cell suspension cultures of California poppy, Eschscholzia californica. Cham In Vitro Cell. Dev Biol Plant 37:35–39

    Article  CAS  Google Scholar 

  • Park SU, Yu M, Facchini PJ (2002) Antisense RNA-mediated suppression of benzophenanthridine alkaloid biosynthesis in transgenic cell cultures of California poppy. Plant Physiol 128:696–706

    Article  PubMed  CAS  Google Scholar 

  • Park SU, Yu M, Facchini PJ (2003) Modulation of berberine bridge enzyme levels in transgenic root cultures of California poppy alters the accumulation of benzophenanthridine alkaloids. Plant Mol Biol 51:153–164

    Article  PubMed  CAS  Google Scholar 

  • Pauli HH, Kutchan TM (1998) Molecular cloning and functional heterologous expression of two alleles encoding (S)-N-methylcoclaurine 3′-hydroxylase (CYP80B1), a new methyl jasmonate-inducible cytochrome P-450-dependent mono-oxygenase of benzylisoquinoline alkaloid biosynthesis. Plant J 13:793–801

    Article  PubMed  CAS  Google Scholar 

  • Pauw B, Hilliou FA, Martin VS, Chatel G, de Wolf CJ, Champion A, Pre M, van Duijn B, Kijne JW, van der Fits L, Memelink J (2004) Zinc finger proteins act as transcriptional repressors of alkaloid biosynthesis genes in Catharanthus roseus. J Biol Chem 279:52940–52948

    Article  PubMed  CAS  Google Scholar 

  • Perazzolli M, Romero-Puertas MC, Delledonne M (2006) Modulation of nitric oxide bioactivity by plant haemoglobins. J Exp Bot 57:479–488

    Article  PubMed  CAS  Google Scholar 

  • Pighin JA, Zheng H, Balakshin LJ, Goodman IP, Western TL, Jetter R, Kunst L, Samuels AL (2004). Plant cuticular lipid export requires an ABC transporter. Science 306:702–704

    Article  PubMed  CAS  Google Scholar 

  • Raharjo TJ, Widjaja I, Roytrakul S, Verpoorte R (2004) Comparitive proteomics of Cannabis sativa plant tissues. J Biomol Tech 15:97–106

    PubMed  Google Scholar 

  • Rosco A, Pauli HH, Priesner W, Kutchan TM (1997) Cloning and heterologous expression of cytochrome P-450 reductases from the Papaveraceae. Arch Biochem Biophys 348:369–377

    Article  PubMed  CAS  Google Scholar 

  • Rose JKC, Bashir S, Giovannoni JJ, Jahn MM, Subramanian Saravanan R (2004) Tackling the plant proteome: practical approaches, hurdles and experimental tools. Plant J 39:715–733

    Article  PubMed  CAS  Google Scholar 

  • Rueffer M, Zenk MH (1986) S-adenosyl-l-methionine: (S)-7,8,13,14-tetrahydroprotoberberine-cis-N-methyltransferase, a branch point enzyme in the biosynthesis of benzophenanthridine and protopine alkaloids. Tetrahedron Lett 27:5603–5604

    Article  CAS  Google Scholar 

  • Rueffer M, Zenk MH (1987a) Distant precursors of benzylisoquinoline alkaloids and their enzymatic formation. Z Naturforsch 42C:319–332

    Google Scholar 

  • Rueffer M, Zenk MH (1987b) Enzymatic formation of protopines by a microsomal cytochrome P-450 system of Corydalis vaginans. Tetrahedron Lett 28:5307–5310

    Article  CAS  Google Scholar 

  • Rueffer M, Zumstein G, Zenk MH (1990) Partial purification and properties of S-adenosyl-l-methionine: (S)-tetrahydroprotoberberine-cis-N-methyltransferase from suspension cultured cells of Eschscholtizia and Corydalis. Phytochemistry 12:3727–3733

    Article  Google Scholar 

  • Sagare AP, Lee YL, Lin TC, Chen CC, Tsay HS (2000) Cytokinin-induced somatic embryogenesis and plant regeneration in Corydalis yanhusuo (Fumariaceae)-a medicinal plant. Plant Sci 160:139–147

    Article  PubMed  CAS  Google Scholar 

  • Samanani N, Facchini PJ (2001) Isolation and partial characterization of norcoclaurine synthase, the first committed step in benzylisoquinoline alkaloid biosynthesis, from opium poppy. Planta 213:898–906

    Article  PubMed  CAS  Google Scholar 

  • Samanani N, Facchini PJ (2002) Purification and characterization of norcoclaurine synthase, the first committed enzyme in benzylisoquinoline alkaloid biosynthesis in plants. J Biol Chem 277:33878–33883

    Article  PubMed  CAS  Google Scholar 

  • Samanani N, Park SU, Facchini PJ (2002) In vitro regeneration and genetic transformation of the berberine-producing plant, Thalictrum flavum ssp. glaucum. Physiol Plant 116:79–86

    Article  PubMed  CAS  Google Scholar 

  • Samanani N, Liscombe DK, Facchini PJ (2004) Molecular cloning and characterization of norcoclaurine synthase, an enzyme catalyzing the first committed step in benzylisoquinoline alkaloid biosynthesis. Plant J 40:302–313

    Article  PubMed  CAS  Google Scholar 

  • Samanani N, Park SU, Facchini PJ (2005) Cell type-specific localization of transcripts encoding nine consecutive enzymes involved in protoberberine alkaloid biosynthesis. Plant Cell 17:915–926

    Article  PubMed  CAS  Google Scholar 

  • Samanani N, Alcantara J, Bourgault R, Zulak K, Facchini PJ (2006) Role of sieve elements and laticifers in the biosynthesis and accumulation of benzylisoquinoline alkaloids in opium poppy. Plant J 47:547–563

    Article  PubMed  CAS  Google Scholar 

  • Sariyar G (2002) Biodiversity in the alkaloids of Turkish Papaver species. Pure Appl Chem 74:557–574

    CAS  Google Scholar 

  • Sariyar G, Sari A, Freyer AJ, Guinaudeau H, Shamma M (1990) Quaternary isoquinoline alkaloids from Papaver species. J Nat Prod 53:1302–1306

    CAS  Google Scholar 

  • Sariyar G, Shamma M (1986) Six alkaloids from Papaver species. Phytochemistry 25:2403–2406

    Article  CAS  Google Scholar 

  • Saslowsky D, Winkel-Shirley B (2001) Localization of flavonoid enzymes in Arabidopsis roots. Plant J 27:37–48

    Article  PubMed  CAS  Google Scholar 

  • Sato F, Hashimoto T, Haciya A, Tamura K, Choi KB, Morishige T, Fujimoto H, Yamada Y (2001) Metabolic engineering of plant alkaloid biosynthesis. Proc Natl Acad Sci USA 98:367–372

    Article  PubMed  CAS  Google Scholar 

  • Sato F, Takeshita N, Fitchen JH, Fujiwara H, Yamada Y (1993) S-Adenosyl-l-methionine:scoulerine-9-O-methyltransferase from cultured Coptis japonica cells. Phytochemistry 32:659–664

    Article  CAS  Google Scholar 

  • Sato F, Tsujita T, Katagiri Y, Yoshida S, Yamada Y (1994) Purification and characterization of S-adenosyl-l-methionine:noncoclaurine 6-O-methyltransferase from cultured Coptis japonica cells. Eur J Biochem 225:125–131

    Article  PubMed  CAS  Google Scholar 

  • Schmeller T, Latz-Brüning B, Wink M (1997) Biochemical activities of berberine, palmitine and sanguinarine mediating chemical defense against microorganisms and herbivores. Phytochemistry 44:257–266

    Article  PubMed  CAS  Google Scholar 

  • Schuchmann R, Wellmann E (1983) Somatic embryogenesis of tissue cultures of Papaver somniferum and Papaver orientale and its relationship to alkaloid and lipid metabolism. Plant Cell Rep 2:88–91

    Article  CAS  Google Scholar 

  • Schumacher HM, Gundlach H, Fiedler F, Zenk MH (1987) Elicitation of benzophenanthridine alkaloid synthesis in Eschscholzia californica cell cultures. Plant Cell Rep 6:410–413

    CAS  Google Scholar 

  • Schumacher HM, Zenk MH (1988) Partial purification and characterization of dihydrobenzophenanthridine oxidase from Eschscholtzia californica cell suspension cultures. Plant Cell Rep 7:43–46

    Article  CAS  Google Scholar 

  • Sharma JR, Lal RK, Gupta AP, Misra HO, Singh NK, Pandey V (1999) Development of non-narcotic (opium-less and alkaloid-free) opium poppy, Papaver somniferum. Plant Breed 118:449–452

    Article  Google Scholar 

  • Shitan N, Bazin I, Dan K, Obata K, Kigawa K, Ueda K, Sato F, Forestier C, Yazaki K (2003) Involvement of CjMDR1, a plant multidrug-resistance-type ATP-binding cassette protein, in alkaloid transport in Coptis japonica. Proc Natl Acad Sci USA 100:751–756

    Article  PubMed  CAS  Google Scholar 

  • Shoji T, Yamada Y, Hashimoto T (2000) Jasmonate induction of putrescine N-methyltransferase genes in the root of Nicotiana sylvestris. Plant Cell Physiol 41:831–839

    Article  PubMed  CAS  Google Scholar 

  • Shoji T, Winz R, Iwase T, Nakajima K, Yamada Y, Hashimoto T (2002) Expression patterns of two tobacco isoflavone reductase-like genes and their possible roles in secondary metabolism in tobacco. Plant Mol Biol 50:427–440

    Article  PubMed  CAS  Google Scholar 

  • Solano R, Fuertes A, Sanchez-Pulido L, Valencia A, Paz-Ares J (1997) A single residue substitution causes a switch from the dual DNA binding specificity of plant transcription factor MYB.Ph3 to the animal c-MYB specificity. J Biol Chem 272:2889–2895

    Article  PubMed  CAS  Google Scholar 

  • Stadler R, Kutchan TM, Loeffler S, Nagakura N, Cassels B, Zenk MH (1987) Revision of the early steps of reticuline biosynthesis. Tetrahedron Lett 28:1251–1254

    Article  CAS  Google Scholar 

  • Stadler R, Kutchan TM, Zenk MH (1989) Norcoclaurine is the central intermediate in benzylisoquinoline alkaloid biosynthesis. Phytochemistry 28:1083–1086

    Article  CAS  Google Scholar 

  • Stadler R, Zenk MH (1993) The purification and characterization of a unique cytochrome P-450 enzyme from Berberis stolinifera plant cell cultures. J Biol Chem 268:823–831

    PubMed  CAS  Google Scholar 

  • Steffens P, Nagakura N, Zenk MH (1985) Purification and characterization of the berberine bridge enzyme from Berberis beaniana cell cultures. Phytochemistry 24:2577–2583

    Article  CAS  Google Scholar 

  • Stemple DL (2004) TILLING-a high-throughput harvest for functional genomics. Nature Rev 5:1–5

    Google Scholar 

  • Stenzel I, Hause B, Maucher H, Pitzschke A, Miersch O, Ziegler J, Ryan CA, Wasternack C (2003) Allene oxide cyclase dependence of the wound response and vascular bundle-specific generation of jasmonates in tomato-the amplification in wound signalling. Plant J 33:577–589

    Article  PubMed  CAS  Google Scholar 

  • St-Pierre B, Vazquez-Flota FA, De Luca V (1999) Multicellular compartmentation of Catharanthus roseus alkaloid biosynthesis predicts intercellular translocation of a pathway intermediate. Plant Cell 11:887–900

    Article  PubMed  CAS  Google Scholar 

  • Suzuki K, Yamada Y, Hashimoto T (1999) Expression of Atropa belladonna putrescine N-methyltransferase gene in root pericycle. Plant Cell Physiol 40:289–297

    PubMed  CAS  Google Scholar 

  • Szederkenyi J, Komor E, Schobert C (1997) Cloning of the cDNA for glutaredoxin, an abundant sieve-tube exudate protein from Ricinus communis L. and characterisation of the glutathione-dependent thiol-reduction system in sieve tubes. Planta 202:349–356

    Article  PubMed  CAS  Google Scholar 

  • Takeshita N, Fujiwara H, Mimura H, Fitchen JH, Yamada Y, Sato F (1995) Molecular cloning and characterization of S-adenosyl-l-methionine:scoulerine-9-O-methyltransferase from cultured cells of Coptis japonica. Plant Cell Physiol 36:29–36

    PubMed  CAS  Google Scholar 

  • Tanahashi T, Zenk MH (1990) Elicitor induction and characterization of microsomal protopine-6-hydroxylase, the central enzyme in benzophenanthridine alkaloid biosynthesis. Phytochemistry 29:1113–1122

    Article  CAS  Google Scholar 

  • Thureson-Klein Å (1970) Observations on the development and fine structure of the articulated laticifers of Papaver somniferum. Ann Bot 34:751–759

    Google Scholar 

  • Turner GW, Croteau R (2004) Organization of monoterpene biosynthesis in Mentha. Immunoocytochemical localizations of geranyl diphosphate synthase, limonine-6-hydroxylase, isopiperitenol dehydrogenase, and pulegone reductase. Plant Physiol 136:4215–4227

    Article  PubMed  CAS  Google Scholar 

  • Unterlinner B, Lenz R, Kutchan TM (1999) Molecular cloning and functional expression of codeinone reductase: the penultimate enzyme in morphine biosynthesis in the opium poppy Papaver somniferum. Plant J 18:465–475

    Article  PubMed  CAS  Google Scholar 

  • Urbanczyk-Wochniak E, Luedemann A, Kopka J, Selbig J, Roessner-Tunali U, Willmitzer L, Fernie AR (2003) Parallel analysis of transcript and metabolic profiles: a new approach in systems biology. EMBO Rep 4:1–5

    Article  CAS  Google Scholar 

  • van Bel AJE, Knoblauch M (2000) Sieve element and companion cell: the story of the comatose patient and the hyperactive nurse. Aust J Plant Physiol 27:477–487

    Google Scholar 

  • van der Fits L, Memelink J (2000) ORCA3, a jasmonate-responsive transcriptional regulator of plant primary and secondary metabolism. Science 289:295–297

    Article  PubMed  Google Scholar 

  • van der Fits L, Zhang H, Menke FLH, Deneka M, Memelink J (2000) A Catharanthus roseus BPF-1 homologue interacts with an elicitor-responsive region of the secondary metabolite biosynthetic gene Str and is induced by elicitor via a JA-independent signal transduction pathway. Plant Mol Biol 44:675–685

    Article  PubMed  Google Scholar 

  • van der Fits L, Hilliou F, Memelink J (2001) T-DNA activation tagging as a tool to isolate regulators of a metabolic pathway from a genetically non-tractable plant species. Transgenic Res 10:513–521

    Article  PubMed  Google Scholar 

  • Vilaine F, Palauqui J-C, Amselem J, Kusiak C, Lemoine R, Dinant S (2003) Towards deciphering phloem: a transcriptome analysis of the phloem of Apium gaveolens. Plant J 36:67–81

    Article  PubMed  CAS  Google Scholar 

  • Vom Endt D, Kijne JW, Memelink J (2002) Transcription factors controlling plant secondary metabolism: what regulates the regulators?. Phytochemistry 61:107–114

    Article  PubMed  CAS  Google Scholar 

  • Wagner U, Edwards R, Dixon DP, Mauch F (2002) Probing the diversity of the Arabidopsis glutathione S-transferase family. Plant Mol Biol 49:515–532

    Article  PubMed  CAS  Google Scholar 

  • Wakhlu AK, Bajwa PS (1986) Regeneration of uniform plants from somatic embryos of Papaver somniferum (opium poppy). Phytomorphology 36:101–105

    Google Scholar 

  • Walz C, Juenger M, Schad M, Kehr J (2002) Evidence for the presence and activity of a complete antioxidant defence system in mature sieve tubes. Plant J 31:189–197

    Article  PubMed  CAS  Google Scholar 

  • Walz C, Giavalisco P, Schad M, Juenger M, Klose J, Kehr J (2004) Proteomics of curcurbit phloem exudate reveals a network of defense proteins. Phytochemistry 65:1795–1804

    Article  PubMed  CAS  Google Scholar 

  • Ward JL, Harris C, Lewis J, Beale MH (2003) Assessment of 1H NMR spectroscopy and multivariate analysis as a technique for metabolic fingerprinting of Arabidopsis thaliana. Phytochemistry 62:949–957

    Article  PubMed  CAS  Google Scholar 

  • Waugh R, Leader DJ, McCallum N, Caldwell D (2006) Harvesting the potential of induced biological diversity. Trends Plant Sci 11:71–79

    Article  PubMed  CAS  Google Scholar 

  • Weid M, Ziegler J, Kutchan TM (2004) The roles of latex and the vascular bundle in morphine biosynthesis in the opium poppy, Papaver somniferum. Proc Natl Acad Sci USA 101:13957–13962

    Article  PubMed  CAS  Google Scholar 

  • Wesley SV, Helliwell C, Wang MB, Waterhouse P (2004) Post-transcriptional gene silencing in plants. Methods Mol Biol 265:117–129

    PubMed  CAS  Google Scholar 

  • Williams RD, Ellis BE (1989) Age and tissue distribution of alkaloids in Papaver somniferum. Phytochemistry 28:2085–2088

    Article  CAS  Google Scholar 

  • Yazaki K (2006) ABC transporters involved in the transport of plant secondary metabolites. FEBS Lett 580:1183–1191

    Article  PubMed  CAS  Google Scholar 

  • Ye K, Ke Y, Keshava N, Shanks J, Kapp JA, Tekmal RR, Petros J, Joshi HC (1998) Opium alkaloid noscapine is an antitumor agent that arrests metaphase and induces apoptosis in dividing cells. Proc Natl Acad Sci USA 95:1601–1606

    Article  PubMed  CAS  Google Scholar 

  • Ziegler J, Diaz-Chavez ML, Kramell R, Ammer C, Kutchan TM (2005) Comparative macroarray analysis of morphine containing Papaver somniferum and eight morphine-free Papaver species identifies an O-methyltransferase involved in benzylisoquinoline biosynthesis. Planta 222:458–471

    Article  PubMed  CAS  Google Scholar 

  • Zulak KG, Cornish A, Daskalchuk TE, Deyholos MK, Goodenowe DB, Gordon PMK, Klassen D, Pelcher LE, Sensen CW, Facchini PJ (2006) Gene transcript and metabolite profiling of elicitor-induced opium poppy cell cultures reveals the coordinate regulation of primary and secondary metabolism. Planta (in press)

Download references

Acknowledgements

We thank David Bird for the preparation of the electron and immunofluorescence micrograms. Research was funded by grants from the Natural Sciences and Engineering Research Council (NSERC) of Canada to P.J.F., who also holds the Canada Research Chair in Plant Biotechnology. J.M.H is the recipient of an Alberta Ingenuity doctoral scholarship. D.K.L. is the recipient of a NSERC postgraduate scholarship.

Author information

Authors and Affiliations

  1. Department of Biological Sciences, University of Calgary, Calgary, Alberta, Canada, T2N 1N4

    Peter J. Facchini, Jillian M. Hagel, David K. Liscombe, Natalia Loukanina, Benjamin P. MacLeod, Nailish Samanani & Katherine G. Zulak

Authors
  1. Peter J. Facchini
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jillian M. Hagel
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. David K. Liscombe
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Natalia Loukanina
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Benjamin P. MacLeod
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Nailish Samanani
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Katherine G. Zulak
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Peter J. Facchini.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Facchini, P.J., Hagel, J.M., Liscombe, D.K. et al. Opium poppy: blueprint for an alkaloid factory. Phytochem Rev 6, 97–124 (2007). https://doi.org/10.1007/s11101-006-9042-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11101-006-9042-0

Keywords

Search

Navigation