Skip to main content

Genetic Engineering Potential of Hairy Roots of Poppy (Papaver spp.) for Production of Secondary Metabolites, Phytochemistry, and In Silico Approaches

  • Chapter
  • First Online:
Biotechnological Approaches for Medicinal and Aromatic Plants

Abstract

Opium poppy is one of the most important medicinal plants, because of its secondary metabolites (alkaloids). Opium as such is an important product, which has many uses and abuses. Its alkaloids are widely used in modern pharmacopeia. Agrobacterium rhizogenes (hairy roots), mediated hairy root culture, is also used for secondary metabolite production under in vitro conditions. Hairy roots are able to grow fast without phytohormones and to produce the metabolites of the mother plant. India is the only country where UN has given license to produce opium from latex. The application of opiate alkaloids, mainly in hydrochloride, sulfate, and phosphate forms, is restricted in some well-defined therapeutic fields. A major component among alkaloids is morphine, having analgesic in nature and used mainly to control severe pain and sedative effects. Poppy seeds have been described as tonic and aphrodisiac, promote luster of the body, enhance capacity to muscular work, and allay nervous excitement. Plant of such economic importance is affected by various biotic and abiotic factors leading to yield loss. Biotic factors include fungi, bacteria, viruses, nematodes, and birds too. This important plant has huge prospects in pharma industry, and on other hand, it is facing lots of challenges in the form of illicit trade, drug abuse, and biotic and abiotic stresses.

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

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 139.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 179.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 249.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Afzali, M., Ghaeli, P., Khanavi, M., Parsa, M., Montazeri, H., Ghahremani, M. H., & Ostad, S. N. (2006). Non-additive opium alkaloids selectively induced apoptosis in cancer cells compared to normal cells. Daru, 23, 16–23.

    Article  CAS  Google Scholar 

  • Allen, R. S., Millgate, A. G., Chitty, J. A., Thisleton, J., Miller, J. A., Fist, A. J., et al. (2004). RNAi-mediated replacement of morphine with the nonnarcotic alkaloid reticuline in opium poppy. Nature Biotechnology, 22, 1559–1566. https://doi.org/10.1038/nbt1033.

  • Angerhofer, C. K., Guinaudeau, H., Wongpanich, V., Pezzuto, J. M., & Cordell, G. A. (1999). Antiplasmodial and cytotoxic activity of natural bisbenzylisoquinoline alkaloids. Journal of Natural Products, 62, 59–66.

    Article  PubMed  CAS  Google Scholar 

  • Aoki, S., & Syono, K. (1999). Synergistic function of rolB, rolC, ORF13 and ORF14 of TL-DNA of agrobacterium rhizogenes in hairy root induction in Nicotiana tabacum. Plant & Cell Physiology, 40, 252–256.

    Article  CAS  Google Scholar 

  • Aruna, K., & Shivaramakrishnan, V. M. (1992). Anticarcinogenic effects of some Indian plants. Food and Chemical Toxicology, 30, 953–956.

    Article  PubMed  CAS  Google Scholar 

  • Balbi, G. (1960). Poppy seed oil in manufacture of paints and varnishes. Oleria, 14, 97–104.

    CAS  Google Scholar 

  • Battersby, A. R., & Harper, B. J. T. (1958). Biogenesis of morphine. Chemistry and Industry (London), 2, 365–366.

    Google Scholar 

  • Belny, M., Herouart, D., Thomasset, B., David, H., Jacquin-Dubreuil, A., & David, A. (1997). Transformation of Papaver somniferum cell suspension cultures with sam-1 from A. thaliana results in cell lines of different S-adenosyl-L-methionine syn-thase activity. Physiologia Plantarum, 99, 233–240.

    Article  CAS  Google Scholar 

  • Benk, E. (1987). Seeds usable as nuts. Industrille Obst und Gemueseverwertung, 72, 282–284.

    Google Scholar 

  • Bentley, K. W., Boura, A. L., Fitzgerald, A. E., Hardy, D. G., McCoubrey, A., Aikman, M. L., & Lister, R. E. (1965). Compounds possessing morphine-Antagonising or powerful analgesic properties. Nature, 206, 102–103.

    Article  PubMed  CAS  Google Scholar 

  • Bentley, K. W., Hardy, D. G., & Meek, B. (1967). Novel analgesics and molecular rearrangements in the morphine-thebaine group. II. Alcohols derived from 6,14-endo-etheno- and 6,14-endo-ethanotetrahydrothebaine. Journal of the American Chemical Society, 89(13), 3273–3280.

    Article  PubMed  CAS  Google Scholar 

  • Berlin, J., Ruegenhagen, C., Dietze, P., Fecker, L. F., Goddijn, O. J. M., & Hoge, J. H. C. (1993). Increased production of serato-nin by suspension and root cultures of Peganum harmala transformed with a tryptophan decarboxylase cDNA clone from Cathranthus roseus. Transgenic Research, 2, 336–344.

    Article  CAS  Google Scholar 

  • Bernath, J. (1998). Poppy: The genus (Medicinal and Aromatic Plants. Industrial Profiles). Amsterdam: Harwood Academic Publishers.

    Google Scholar 

  • Berre, J. (1984). Relief of pain in intensive care patients. Resuscitation, 11(3–4), 157–164.

    Article  PubMed  CAS  Google Scholar 

  • Binns, A. N., & Tomashow, J. V. (1988). Cell biology of agrobacterium infection and transformation of plants. Annual Review of Microbiology, 42, 575–606.

    Article  CAS  Google Scholar 

  • Blechert, S., Brodschelm, W., Holder, S., Kammerer, L., Kutchan, T. M., Mueller, M. J., Xia, Z. Q., & Zenk, M. H. (1995). The octadecanoid pathway: Signal molecules for the regulation of secondary pathways. Proceedings of the National Academy of Sciences, USA.

    Google Scholar 

  • Breall, J. A., Areosty, J. M., & Simons, M. (2005). Overview of the management of unstable angina and acute non-ST elevation (non-Q wave) myocardial infarction. Up To Date online, 12.3.

    Google Scholar 

  • Brillanceau, M. H., David, C., & Tempe, J. (1989). Genetic transformation of Catharanthus roseus G. Don by agrobacterium rhizogenes. Plant Cell Reports, 8, 63–66.

    Article  PubMed  CAS  Google Scholar 

  • Camacho, M. D., Phillipson, D., Croft, S. L., Rock, P., Marshall, S. J., & Schiff, P. L., Jr. (2002). In vitro activity of Triclisia patens and some bisbenzylisoquinoline alkaloids against Leishmania donovani and Trypanosoma brucei brucei. Phytotherapy Research, 16, 432–436.

    Article  CAS  Google Scholar 

  • Chavadej, S., Brission, N., McNeil, J. N., & De, L. V. (1994). Redirection of tryptophan leads to production of low indole glucosinolate canola. Proceedings of the National Academy of Sciences of the United States of America, 91, 2166–2170.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Chen, Q., Peng, W. L., Qi, S. J., & Xu, A. L. (2002). Apoptosis of human highly metastatic lung cancer cell line 95-D induced by acutiaporberine, a novel bisalkaloid derived from Thalictrum acutifolium. Planta Medica, 68, 550–553.

    Article  PubMed  CAS  Google Scholar 

  • Cheney, R. H. (1964). Therapeutic potential of Eschscholtziae californicae herba. Quarterly Journal of Crude Drugs, 3, 413–416.

    Article  Google Scholar 

  • Chilton, M. D., Tepfer, D. A., Petit, A., David, C., Casse-Delbart, F., & Tempe, J. (1982). Agrobacterium rhizogenes inserts T-DNA into the genomes of the host plant root cells. Nature, 295, 432–434.

    Article  CAS  Google Scholar 

  • Christrup, L. L. (1997). Morphine metabolites. Acta Anaesthesiologica Scandinavica, 41(1 Pt 2), 116–122.

    Article  PubMed  CAS  Google Scholar 

  • Cline, S. D., & Coscia, C. J. (1988). Stimulation of sanguinarine production by combined fungal elicitation and hormonal deprivation in cell suspension culture of papaver bracteatum. Plant Physiology, 86, 161–165.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Coffin, P., Sherman, S., & Curtis, M. (2010). Underestimated and overlooked: A global review of drug overdose and overdose prevention. In C. Cook (Ed.), global state of harm reduction: Key issues for broadening the response. London: International Harm Reduction Association.

    Google Scholar 

  • Courtwright, D. T. (2009). Forces of habit drugs and the making of the modern world (1st ed.pp. 36–37). Cambridge, MA: Harvard University Press.

    Google Scholar 

  • Dewick, P. M. (2002). Alkaloids. In Medicinal natural products (2nd ed.). New York: Wiley.

    Google Scholar 

  • Diamond, A., & Penix, I. D. (2016). Metabolic engineering for the production of plant isoquinoline alkaloids. Plant Biotechnology Journal, 7(2), 1319–1328.

    Article  CAS  Google Scholar 

  • Dinda, A., Gitman, M., & Singhal, P. C. (2005). Immunomodulatory effect of morphine: Therapeutic implications. Expert Opinion on Drug Safety, 4(4), 669–675.

    Article  PubMed  CAS  Google Scholar 

  • Downs, C. G., Christey, M. C., Davies, K. M., King, G. A., Seelye, J. F., Sinclair, B. K., & Stevenson, D. G. (1994). Hairy roots of Brassica napus: II glutamine synthase over expression alters ammonia assimilation and the response to phosphinothricin. Plant Cell Reports, 14, 41–46.

    PubMed  CAS  Google Scholar 

  • Dzink, J. L., & Socransky, S. S. (1985). Comparative in vitro activity of sanguinarine against oral microbial isolates. Antimicrobial Agents Chemotherapy, 27, 663–665.

    Article  PubMed  CAS  Google Scholar 

  • Facchini, P. J. (2001). Alkaloid biosynthesis in plants: Biochemistry, cell biology, molecular regulation, and metabolic engineering application. Annual Review of Plant Physiology and Plant Molecular Biology, 52, 29–66.

    Article  PubMed  CAS  Google Scholar 

  • Facchini, P. J., & De Luca, V. (1994). Differential and tissue-specific expression of a gene family for tyrosine/DOPA decarboxylase in opium poppy. Journal of Biological Chemistry, 28, 26684–26690.

    Google Scholar 

  • Facchini, P. J., & Luca, V. D. (2008). Opium poppy and Madagascar periwinkle: Model non-model systems to investigate alkaloid biosynthesis in plants. The Plant Journal, 54(2), 763–784.

    Article  PubMed  CAS  Google Scholar 

  • Facchini, P. J., & Luca, D. V. (1995). Phloem-specific expression of Tyrosine/Dopa Decarboxylase genes and the biosynthesis of isoquinoline alkaloids in opium poppy. Plant Cell, 7(11), 1811–1821.

    Google Scholar 

  • Facchini, P. J., & Park, S. U. (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, P. J., Penzes, C., Johnson, A. G., & Bull, D. (1996a). Molecular characterization of barbering bridge enzyme genes from opium poppy. Plant Physiology, 112, 1669–1677.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Facchini, P. J., Johnson, A. G., Poupart, J., & De Luca, V. (1996b). Uncoupled defense gene expression and antimicrobial alkaloid accumulation in elicited opium poppy cell cultures. Plant Physiology, 111, 687–697.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Fedde, F. (1909). In A. Engler (Ed.), Das Pflanzenfamilien (Vol. 40). Leipzig: Wilhelm Engelmann.

    Google Scholar 

  • Fisher, G. L. (Ed.). (2009). Encyclopedia of substance abuse prevention treatment & recovery (p. 564). Los Angeles: SAGE.

    Google Scholar 

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

    Google Scholar 

  • Flores, H. E., & Filner, P. (1985). Metabolic relationships of putrescine, GABA and alkaloids in cell and root cultures of Solanaceae. In K. H. Neumann, W. Barz, & E. Reinhard (Eds.), Primary and secondary metabolism of plant cell cultures (pp. 174–185). Berlin: Springer.

    Chapter  Google Scholar 

  • Flores, H. E., & Medina-Bolivar, F. (1995). Root culture and plant natural products: “Unearthing” the hidden half of plant metabolism. Plant Tissue Culture and Biotechnology, 1, 59–74.

    Google Scholar 

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

    Article  Google Scholar 

  • Giri, A., & Narasu, M. L. (2000). Transgenic hairy roots: Recent trends and applications. Biotechnology Advances, 18, 1–22.

    Article  PubMed  CAS  Google Scholar 

  • Glare, P. A., & Walsh, T. D. (1991). Clinical pharmacokinetics of morphine. Therapeutic Drug Monitoring, 13(1), 1–23.

    Article  PubMed  CAS  Google Scholar 

  • Gottlieb, O. R., Kaplan, M. A. C., & Zocher, D. H. T. (1993). A chemosystematic overview of Magnoliidae, Ranunculidae, Caryophyllidae and Hamamelididae. In K. Kubitzki, J. G. Rohwer, & V. Bittrich (Eds.), The families and genera of vascular plants (Vol. II). Springer Berlin.

    Google Scholar 

  • Hagel, J. M., Macleod, B. P., & Facchini, P. J. (2007). Ii.2 opium poppy. In E. C. Pua & M. R. Davey (Eds.), Biotechnology in agriculture and forestry, Transgenic Crops VI (Vol. 61). Heidelberg: Springer.

    Google Scholar 

  • Hamill, J. D., Parr, A. J., Rhodes, M. J. C., Robins, R. J., & Walton, N. J. (1987). New routes to plant secondary products. BioTechnology, 5, 800–804.

    CAS  Google Scholar 

  • Hamill, J. D., Robins, R. J., Parr, A. J., Evans, P. M., Furze, J. D., & Rhodes, M. J. C. (1990). Over expressing a yeast ornithine de-carboxylase gene in transgenic roots of Nicotiana rustica can lead to enhanced nicotine accumulation. Plant Molecular Biology, 15, 27–38.

    Article  PubMed  CAS  Google Scholar 

  • Hammer, K., & Fritisch, R. (1977). The question of ancestral species of cultivated poppy (P. somniferum L.). Kulture Pflanze, 25, 113.

    Article  Google Scholar 

  • Hassel, S. J., & Sawe, J. (1993). Morphine pharmacokinetics and metabolism in humans. Enterohepatic cycling and relative contribution of metabolites to active opioid concentrations. Clinical Pharmacokinectics, 24(4), 344–354.

    Article  Google Scholar 

  • Hashimoto, T., Matsuda, J., & Yamada, Y. (1993). Two-step epoxidation of hyoscyamine to scopolamine is catalyzed by bifunctional hyoscyamine 6b-hydroxylase. FEBS Letters, 329, 35–39.

    Google Scholar 

  • Hirshi, N. J., & Hrishi, K. (1960). Studies on the correlation between male sterility and flower colour in the F2 of an interspecific cross between Papaver setigerum and P. somniferum. Genetica, 31, 410.

    Article  Google Scholar 

  • https://www.drugabuse.gov/publications/drugfacts/heroin

  • Huang, F. C., & Kutchan, T. M. (2000). Distribution of morphinan and benzophenanthridine alkaloid gene transcript accumulation in Papaver somniferum. Phytochemistry, 53, 555–564.

    Article  PubMed  CAS  Google Scholar 

  • Huffman, G. A., White, F. F., Gordon, M. P., & Nester, E. W. (1984). Hairy root-inducing plasmid: Physical map and homology to tumor inducing plasmids. Journal of Bacteriology, 157, 269–276.

    PubMed  PubMed Central  CAS  Google Scholar 

  • Husain, A., & Sharma, J. R. (1983). The Opium Poppy (Medicinal and Aromatic Plants Series-I). Lucknow: Central Institute of Medicinal and Aromatic Plants.

    Google Scholar 

  • Kamei, J. (1996). Role of opioidergic and serotonergic mechanisms in cough and antitussives. Pulmonary Pharmacology, 9(5–6), 349–356.

    Article  PubMed  CAS  Google Scholar 

  • Kamo, K. K., Kimoto, W., Hsu, A. F., Mahlberg, P. G., & Bills, D. D. (1982). Morphinan alkaloids in cultured tissues and redifferentiated organs of Papaver somniferum. Phytochemistry, 21, 219–222.

    Article  CAS  Google Scholar 

  • Khan, N., Woodruff, T. M., & Smith, M. T. (2014). Establishment and characterization of an optimized mouse model of multiple sclerosis-induced neuropathic pain using behavioral, pharmacologic, histologic and immunohistochemical methods. Pharmacology, Biochemistry, and Behavior, 126, 13–27.

    Article  PubMed  CAS  Google Scholar 

  • Kutchan, T. M., & Zenk, M. H. (1993). Enzymology and molecular biology of benzophenanthridine alkaloid biosynthesis. Journal of Plant Research, 3, 165–173.

    Google Scholar 

  • Kutchan, T. M., Rush, M. D., & Coscia, C. J. (1986). Subcellular localization of alkaloids and dopamine in different vacuolar compartments of Papaver bracteatum. Plant Physiology, 81, 161–166.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Larkin, P. J., Miller, J. A., Allen, R. S., Chitty, J. A., Gerlach, W. L., Frick, S., Kutchan, T. M., & Fist, A. J. (2007). Increasing morphinan alkaloid production by over-expressing codeinone reductase in transgenic Papaver somniferum. Plant Biotechnology Journal, 5, 26–37.

    Article  PubMed  CAS  Google Scholar 

  • Laurain-Mattar, D., Gillet-Manceau, F., Buchon, L., Nabha, S., Fliniaux, M.-A., & Jacquin-Dubreuil, A. (1999). Somatic embryogenesis and rhizogenesis of tissue cultures of two genotypes of Papaver somniferum: Relationships to alkaloid production. Planta Medica, 65, 167–170.

    Article  PubMed  CAS  Google Scholar 

  • Lesk, A. M. (2000). Introduction to bioinformatics. Oxford: Oxford University Press.

    Google Scholar 

  • Liu, J. K., & Couldwell, W. T. (2005). Intra-arterial papaverine infusions for the treatment of cerebral vasospasm induced by aneurysmal subarachnoid hemorrhage. Neurocritical Care, 2(2), 124–132.

    Article  PubMed  Google Scholar 

  • Lodhi, A. H., Bongaerts, R. J. M., Verpoorte, R., Coomber, S. A., & Charlwood, B. V. (1996). Expression of bacterial isochoris-mate synthase (E C 5.4.99.6) in transgenic root cultures of Rubia peregrina. Plant Cell Reports, 16, 54–57.

    Article  PubMed  CAS  Google Scholar 

  • McCarthy, L. M., Wetzel, J. K. S., Eisenstein, T. K., & Rogers, T. J. (2001). Opioids, opioid receptors, and the immune response. Drug and Alcohol Dependence, 62, 111–123.

    Article  PubMed  CAS  Google Scholar 

  • Meijerink, W. J. H. J., Molina, P. E., & Abumrad, N. N. (1999). Mammalian opiate alkaloid synthesis: Lessons derived from plant biochemistry. Shock, 12(3), 165–173.

    Article  PubMed  CAS  Google Scholar 

  • Merck, G. (1848). Vorläufige Notiz über eine neue organische base im opium [Preliminary notice of a new organic base in opium]. Annalen der Chemie und Pharmacie, 66, 125–128.

    Article  Google Scholar 

  • Ming, H., Jiang, L., Ren, Z., Wang, G., & Wang, J. (2016). Noscapine targets EGFRp-Tyr1068 to suppress the proliferation and invasion of MG63 cells. Scientific Reports, 6. https://doi.org/10.1038/srep37062.

  • Nader, B. L., Taketa, A. T., Pereda-Miranda, R., & Villarreal, M. L. (2006). Production of triterpenoids in liquid-cultivated hairy roots of Galphimia glauca. Planta Medica, 72, 842–844.

    Article  PubMed  CAS  Google Scholar 

  • Narcotic Drugs. (2014). International Narcotics Control Board. 2015 pp. 21, 30. ISBN: 9789210481571. https://www.incb.org/documents/Narcotic-Drugs/Technical-Publications/2014/Narcotic_Drugs_Report_2014.pdf

  • Neligan, A. R. (1927). The opium question. London: Bale and Curnow.

    Google Scholar 

  • Nergiz, C., & Oltes, S. (1994). The proximate composition and some minor constituents of poppy seeds. Journal of the Science of Food and Agriculture, 66, 117–120.

    Article  CAS  Google Scholar 

  • Nessler, C. L., Allen, R. D., & Galewsky, S. (1985). Identification and characterization of latex-specific proteins in opium poppy. Plant Physiology, 79, 499–504.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Ohlsson, S., Holm, L., Myrberg, O., Sundström, A., & Yue, Q. Y. (2008). Noscapine may increase the effect of warfarin. British Journal of Clinical Pharmacology, 65(2), 277–278.

    Article  PubMed  CAS  Google Scholar 

  • Oksman-Caldentey, & Arroo, R. (2000). Regulation of tropane alkaloid metabolism in plants and plant cell cultures. In R. Verpoorte & A. W. Alfermann (Eds.), Metabolic engineering of plant secondary metabolism (pp. 253–281). Dordrecht: Kluwer Academic Press.

    Chapter  Google Scholar 

  • Page, G. G., Ben-Eliyahu, S., & Yirmiya, R. (1993). Morphine attenuates surgery-induced enhancement of metastatic colonization in rats. Pain, 54(1), 21–28.

    Article  PubMed  CAS  Google Scholar 

  • Park, S. U., & Facchini, P. J. (2000a). Agrobacterium rhizogenes-mediated transformation of opium poppy, Papaver somniferum L., and California poppy, Eschscholzia californica Cham., root cultures. Journal of Experimental Biology, 51, 1005–1016.

    Google Scholar 

  • Park, S. U., & Facchini, P. J. (2000b). Agrobacterium-mediated genetic transformation of California poppy, Eschscholzia californica Cham., via somatic embryogenesis. Plant Cell Reports, 19, 421–426.

    Google Scholar 

  • Park, S. U., Yu, M., & Facchini, P. J. (2003). Modulation of berberine bridge enzyme levels in transgenic root cultures of California poppy alters the accumulation of benzophenanthridine alkaloids. Plant Molecular Biology, 51, 153–164.

    Article  PubMed  CAS  Google Scholar 

  • Phillipson, J. D. (1983). Lntraspecific variation and alkaloids of Papaver species. Planta Medica, 48, 187–192.

    Article  PubMed  CAS  Google Scholar 

  • Poser, C. M. (1974). Letter: Papaverine in prophylactic treatment of migraine. Lancet, 1(7869), 1209–1222.

    Google Scholar 

  • Preininger, V. (1985). Chemotaxonomy of the Papaveraceae alkaloids. In J. D. Phillipson, M. F. Roberts, & M. H. Zenk (Eds.), The chemistry and biology of isoquinoline alkaloids (pp. 23–37). Berlin: Springer.

    Chapter  Google Scholar 

  • Rhodes, M. J. C., Robins, R. J., Hamill, J. D., Parr, A. J., Hilton, M. G., & Walton, N. J. (1990). Properties of transformed root cultures. In B. V. Charlwood, & M. J. C. Rhodes (Eds.), Secondary products from plant tissue culture (Proceedings of the Phytochemical Society of Europe, pp. 201–225). Oxford: Clarendon Press.

    Google Scholar 

  • Roberts, M. F. (1988). lsoquinolines (papaver alkaloids). In F. Constabel & I. K. Vasil (Eds.), Cell culture and somatic cell genetics of plants (Vol. 5, pp. 315–334). New York: Academic.

    Google Scholar 

  • Roberts, M. F., Carthy, D. M., Kutchan, T. M., & Coscia, C. J. (1983). Localization of enzymes and alkaloidal metabolites in Papaver latex. Archives of Biochemistry and Biophysics, 222, 599–609.

    Article  PubMed  CAS  Google Scholar 

  • Rutherfold, R. M., Azher, T., & Gilmartin, J. J. (2002). Dramatic response to nebulized morphine in an asthmatic patient with severe chronic cough. Irish Medical Journal, 95(4), 113–114.

    Google Scholar 

  • Schroeder, K., & Fahey, T. (2004). Over-the-counter medications for acute cough in children and adults in ambulatory settings. Cochrane Database of Systematic Reviews, 4, CD001831.

    Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Schumacher, H. (1983). Alkaloid biosynthesis. Planta Medica, 48, 212–222.

    Article  PubMed  CAS  Google Scholar 

  • Schumacher, H. M., Gundlach, H., Fiedler, F., & Zenk, M. H. (1987). Elicitation of benzophenanthridine alkaloid synthesis in Eschscholtzia cell cultures. Plant Cell Reports, 6, 410–413.

    PubMed  CAS  Google Scholar 

  • Seifert, F., Todorov, D. K., Hutter, K. J., & Zeller, W. J. (1996). Cell cycle effects of thaliblastine. Journal of Cancer Research and Clinical Oncology, 122, 707–710.

    Article  PubMed  CAS  Google Scholar 

  • Sevon, N., & Oksman-Caldentey, K. M. (2002). Agrobacterium rhizogenes-mediated transformation: Root cultures as a source of alkaloids. Planta Medica, 68, 859–868.

    Article  PubMed  CAS  Google Scholar 

  • Sharafi, A., Sohi, H. H., Mousavi, A., Azadi, P., & Khalifani Razavi, B. H. K. (2013a). Metabolic engineering of morphinan alkaloids by over-expression of codeinone reductase in transgenic hairy roots of Papaver bracteatum, the Iranian poppy. Biotechnology Letters, 35, 445–453.

    Article  PubMed  CAS  Google Scholar 

  • Sharafi, A., Mousavi, A., Sohi, H. H., Azadi, P., Dehsara, B., & Khalifani, B. H. (2013b). Enhanced morphinan alkaloid production in hairy root cultures of Papaver bracteatum by over-expression of salutaridinol 7-o-acetyltransferase gene via Agrobacterium rhizogenes mediated transformation. World Journal of Microbiology, 29(11), 2125–2131.

    Article  CAS  Google Scholar 

  • Sharma, P. V. (1973). Drugs and landmarks of the history of Indian medicine. Journal of Research in Indian medicine, 8(4), 86.

    Google Scholar 

  • Sharma, D. (1980). Pollen morphology of two cultivars of P. somniferum L. Current Science, 49, 710.

    Google Scholar 

  • Sharma, J. R., & Singh, O. P. (1983). Genetics and genetic improvement. In A. Husain & J. R. Sharma (Eds.), The Opium Poppy (pp. 39–68). Lucknow: Central Institute of Medicinal and Aromatic Plants.

    Google Scholar 

  • Shukla, S., & Singh, S. P. (2003). Exploitation of inter-specific crosses and its prospects for developing novel plant type in opium poppy (Papaver somniferum L.). In P. C. Trivedi (Ed.), Herbal drugs and biotechnology (pp. 210–239). Jaipur: Pointer Publisher.

    Google Scholar 

  • Sillanpää, M., & Koponen, M. (1978). Papaverine in the prophylaxis of migraine and other vascular headache in children. Acta Paediatrica Scandinavica, 67(2), 209–212.

    Article  PubMed  Google Scholar 

  • Singh, H. P., Singh, S. P., Singh, A. K., & Patra, N. K. (1999). The component of genetic variances in biparental progenies of opium poppy (Papaver somniferum). Journal of Medicine in Aromatic Plant Science, 21, 724–726.

    Google Scholar 

  • Singh, H., Singh, P., Kumari, K., Chandra, A., Dass, S. K., & Chandra, R. (2013). A review on noscapine, and its impact on heme metabolism. Current Drug Metabolism, 14(3), 351–360.

    Article  PubMed  CAS  Google Scholar 

  • Slightom, J. L., Durand-Tardif, M., Jouanin, L., & Tepfer, D. (1986). Nucleotide sequence analysis of TL-DNA of agrobacterium rhizogenes agropine type plasmid. The Journal of Biological Chemistry, 261, 108–121.

    PubMed  CAS  Google Scholar 

  • Susanne, F., Julie, A. C., Robert, K., Jürgen, S., Robert, S. A., Philip, J. L., & Toni, M. K. (2004). Transformation of opium poppy (Papaver somniferumL.) with antisense berberine bridge enzyme gene (anti-bbe) via somatic embryogenesis results in an altered ratio of alkaloids in latex but not in roots. Transgenic Research, 13(6), 607–613.

    Google Scholar 

  • Takeuchi, K., Sakamoto, S., Nagayoshi, Y., Nishizawa, H., & Matsubara, J. (2004). Reactivity of the human internal thoracic artery to vasodilators in coronary artery bypass grafting. European Journal of Cardio-Thoracic Surgery, 26(5), 956–959.

    Article  PubMed  Google Scholar 

  • Tepfer, M., & Casse-Delbart, F. (1987). Agrobacterium rhizogenes as a vector for transforming higher plants. Microbiological Sciences, 4, 24–28.

    PubMed  CAS  Google Scholar 

  • Tetenyi, P. (1997). Opium poppy (Papaver somniferum): Botany and horticulture. In Jules & Janick (Eds.), Horticultural reviews (Vol. 19, pp. 373–408).

    Google Scholar 

  • Tiwari, R. K., Trivedi, M., Guang, Z. C., Guo, G. Q., & Zheng, G. C. (2007). Genetic transformation of Gentiana macrophylla with agrobacterium rhizogenes: Growth and production of secoiridoid glucoside gentiopicroside in transformed hairy root cultures. Plant Cell Reports, 26, 199–210.

    Article  PubMed  CAS  Google Scholar 

  • Tiwari, R. K., Trivedi, M., Guang, Z. C., Guo, G. Q., & Zheng, G. C. (2008). Agrobacterium rhizogenes mediated transformation of Scutellaria baicalensis and production of flavonoids in hairy roots. Biologia Plantarum, 52(1), 26–35.

    Article  CAS  Google Scholar 

  • Trease, G., & Evans, W. C. (1972). Pharmacognosy (10th ed.). London: Bailliere Tindall.

    Google Scholar 

  • Tshibangu, J. N., Wright, A. D., & Konig, G. M. (2003). HPLC isolation of the anti-plasmodially active bisbenzylisoquinone alkaloids present in roots of Cissampelos mucronata. Phytochemical Analysis, 14, 13–22.

    Article  PubMed  CAS  Google Scholar 

  • Veslovskaya, M. A. (1976). The poppy. New Delhi/New York: American Publishing Co., (translated from Russian).

    Google Scholar 

  • Vijayan, N. (1977). Brief therapeutic report: Papaverine prophylaxis of complicated migraine. Headache, 17(4), 159–162.

    Article  PubMed  CAS  Google Scholar 

  • Walsh, T. D. (1984). Oral morphine in chronic cancer pain. Pain, 18(1), 1–11.

    Article  PubMed  CAS  Google Scholar 

  • Warner, M., Trinidad, J. P., Bastian, B. A., Minino, A. M., & Hedegaard, H. (2016). Drugs most frequently involved in drug overdose deaths: United States, 2010-2014. National Vital Statistics Reports, 65(10), 1–15.

    PubMed  Google Scholar 

  • Weber, T., & Kim, H. U. (2016). The secondary metabolite bioinformatics portal: Computational tools to facilitate synthetic biology of secondary metabolite production. Synthetic and Systems Biology, 1(2), 69–79.

    Article  Google Scholar 

  • White, P. T., & Raymer, S. (1985, February). The poppy. Natural Geography, 143–189.

    Google Scholar 

  • White, F. F., Taylor, B. H., Huffman, G. A., Gordon, M. P., & Nester, E. W. (1985). Molecular and genetic analysis of the transferred DNA regions of the root-inducing plasmid of agrobacterium rhizogenes. Journal of Bacteriology, 164, 33–44.

    PubMed  PubMed Central  CAS  Google Scholar 

  • WHO. (1996). Cancer pain relief: With a guide to opioid availability (2nd ed.). Geneva: World Health Organization.

    Google Scholar 

  • WHO Model List of Essential Medicines (19th List). (2015, April). World Health Organization. http://www.who.int/medicines/publications/essentialmedicines/EML2015_8-May-15.pdf

  • Yadav, H. K., Shukla, S., & Singh, S. P. (2006). Genetic variability and interrelationship among opium and its alkaloids in opium poppy (Papaver somniferum L.). Euphytica, 150, 207–214.

    Article  CAS  Google Scholar 

  • Ye, K., Ke, Y., Keshava, N., Shanks, J., Kapp, J. A., Tekmal, R. R., Petros, J., & Joshi, H. C. (1998). Opium alkaloid noscapine is an antitumor agent that arrests metaphase and induces apoptosis in dividing cells. Proceedings of the National Academy of Sciences of the United States of America, 95, 1601–1606.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Yoshikawa, T., & Furuya, T. (1985). Morphinan alkaloid production by tissue cultures differentiated from cultured cells of Papaver somniferum. Planta Medica, 2, 110–113.

    Article  Google Scholar 

  • Yoshimatsu, K., & Shimomura, K. (1992). Transformation of opium poppy (Papaver somniferum L.) with agrobacterium rhizogenes MAFF 03-01724. Plant Cell Reports, 11, 132–136.

    Article  PubMed  CAS  Google Scholar 

  • Yun, D. J., Hashimoto, T., & Yamada, Y. (1992). Metabolic engineering of medicinal plants: transgenic Atropa belladonna with an improved alkaloid composition. Proceedings of the National Academy of Sciences of the United States of America, 89, 11799–11803.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Zenk, M. H. (1985). Enzymology of benzylisoquinoline alkaloid formation. In J. D. Phillipson, M. F. Roberts, & M. H. Zenk (Eds.), The chemistry and biology of lsoquinoline alkaloids (pp. 240–256). Berlin: Springer.

    Chapter  Google Scholar 

  • Zenk, M. H., & Juenger, M. (2007). Evolution and current status of the phytochemistry of nitrogenous compounds. Phytochemistry, 68, 2757–2772.

    Article  PubMed  CAS  Google Scholar 

  • Ziegler, J. R., & Facchini, P. J. (2008). Alkaloid biosynthesis: Metabolism and trafficking. Annual Review of Plant Biology, 59, 735–769.

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Rajesh K. Tiwari .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2018 Springer Nature Singapore Pte Ltd.

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Trivedi, M., Singh, A., Johri, P., Singh, R., Tiwari, R.K. (2018). Genetic Engineering Potential of Hairy Roots of Poppy (Papaver spp.) for Production of Secondary Metabolites, Phytochemistry, and In Silico Approaches. In: Kumar, N. (eds) Biotechnological Approaches for Medicinal and Aromatic Plants. Springer, Singapore. https://doi.org/10.1007/978-981-13-0535-1_26

Download citation

Publish with us

Policies and ethics