Planta Med 2002; 68(10): 859-868
DOI: 10.1055/s-2002-34924
Review
© Georg Thieme Verlag Stuttgart · New York

Agrobacterium rhizogenes-Mediated Transformation: Root Cultures as a Source of Alkaloids

Nina Sevón1 , Kirsi-Marja Oksman-Caldentey2
  • 1National Agency for Medicines, Helsinki, Finland
  • 2VTT Biotechnology, Espoo, Finland
Further Information

Publication History

Received: February 12, 2002

Accepted: May 25, 2002

Publication Date:
21 October 2002 (online)

Abstract

Hairy roots, transformed with Agrobacterium rhizogenes, have been found to be suitable for the production of secondary metabolites because of their stable and high productivity in hormone-free culture conditions. A number of plant species including many medicinal plants have been successfully transformed with Agrobacterium rhizogenes. Transformed root cultures have also been found to be a potential source of high-value pharmaceuticals. In this article the most important alkaloids produced by hairy roots are summarised. Several different methods have been used to increase the alkaloid accumulation in hairy root cultures. The selection of high productive root lines based on somaclonal variation offers an interesting option to enhance the productivity. Elicitors and modification of culture conditions have been shown to increase the growth and the alkaloid production in some cases. Genetic engineering is a modern tool to regulate the secondary metabolism also in hairy roots. However, our knowledge on biosynthesis of many alkaloids is still poor. Only a limited number of enzymes and their respective genes which regulate the biosynthetic pathways are fully characterised.

References

  • 1 Verpoorte R, Van der Heijden R, Memelink J. General Strategies. Metabolic Engineering of Plant Secondary Metabolism. In: Verpoorte R, Alfermann AW, editors Kluwer Academic Publishers Dordrech-Boston-London; 2000: 31-50
  • 2 Oksman-Caldentey K -M, Hiltunen R. Transgenic crops for improved pharmaceutical products.  Field Crops Res. 1996;  45 57-69
  • 3 Kutchan T. Alkaloid biosynthesis - the basis for metabolic engineering of medicinal plants.  Plant Cell. 1995;  7 1059-70
  • 4 Verpoorte R. Secondary metabolism. Metabolic Engineering of Plant Secondary Metabolism. In: Verpoorte R and Alfermann AW, editors Kluwer Academic Publishers Dordrech-Boston-London; 2000: 1-29
  • 5 Doran P. Prospects for production of plant chemicals from genetically transformed roots.  Aust J Biotechnol. 1989;  3 270-5
  • 6 Sevón N, Hiltunen R, Oksman-Caldentey K -M. Somaclonal variation in Agrobacterium transformed roots and protoplast-derived hairy root clones of Hyoscyamus muticus .  Planta Med. 1998;  64 37-41
  • 7 Wilson P DG. The Pilot-Scale Cultivation of Transformed Roots. Hairy Roots and Culture Applications. In: Doran PM, editor Harwood Academic Publishers Amsterdam; 1997: 179-90
  • 8 Sevón N. Tropane alkaloids in hairy roots and regenerated plants of Hyoscyamus muticus . PhD Thesis, University of Helsinki Helsinki, Finland; 1997
  • 9 Giri A, Narasu M L. Transgenic hairy roots: recent trends and applications.  Biotechnol Advances. 2000;  18 1-22
  • 10 Chilton M -D, Tepfer D A, Petit A, David C, Casse-Delbart F, Tempé J. Agrobacterium rhizogenes inserts T-DNA into the genomes of the host plant root cells.  Nature. 1982;  295 432-4
  • 11 Chilton M -D. Agrobacterium. A Memoir.  Plant Physiol. 2001;  125 9-14
  • 12 Gelvin S B. Crown gall disease and hairy root disease.  Plant Physiol. 1990;  92 281-5
  • 13 Zambryski P, Tempe J, Schell J. Transfer and function of T-DNA genes from Agrobacterium Ti-and Ri plasmids in plants.  Cell. 1989;  56 193-201
  • 14 Cardarelli M, Spanó L, Mariotti D, Mauro M L, Van Sluys M A, Costantino P. The role of auxin in hairy root induction.  Mol Gen Genet. 1987;  208 457-63
  • 15 Palazón J, Cusidó R M, Roig C, Piñol M T. Effect of rol genes from Agrobacterium rhizogenes TL-DNA on nicotine production in tobacco root cultures.  Plant Physiol Biochem. 1997;  35 155-62
  • 16 Shen W H, Petit A, Guern J, Tempé J. Hairy roots are more sensitive to auxin than normal roots.  Proc Natl Acad Sci. 1988;  85 3417-21
  • 17 Spanó L, Mariotti D, Pezzotti M, Damiani F, Arcioni S. Hairy root transformation in alfalfa (Medicago sativa L.)  Theor Appl Genet. 1987;  73 523-30
  • 18 Vanhala L, Eeva M, Lapinjoki S, Hiltunen R, Oksman-Caldentey K -M. Effect of growth regulators on transformed root cultures of Hyoscyamus muticus .  J Plant Physiol. 1998;  153 75-81
  • 19 Zhu J, Oger P M, Schrammeijer B, Hooykaas P JJ, Farrand S K, Winans S C. The bases of crown gall tumorigenesis. J Bacteriol 2000: 3885-95
  • 20 Rhodes M JC, Robins R J, Hamill J D, Parr A J, Hilton M G, Walton N J. Properties of transformed root cultures. In: Charlwood BV, Rhodes MJC, editors Secondary products from plant tissue cultures. Clarendon Press Oxford; 1990: 201-25
  • 21 Davioud E, Petit A, Tate M E, Ryder M H, Tempé J. Cucumopine - A new T-DNA-encoded opine in hairy root and crown gall.  Phytochemistry. 1988;  27 2429-33
  • 22 Isogai A, Fukuchi N, Hayashi M, Kamada H, Harada H, Suzuki A. Structure of a new opine mikimopine, in hairy root induced by Agrobacterium rhizogenes .  Agric Biol Chem. 1988;  52 3235-7
  • 23 White F F, Taylor B H, Huffman G A, Gordon M P, Nester E W. Molecular and genetic analysis of the transferred DNA regions of the root-inducing plasmid of Agrobacterium rhizogenes .  J Bacteriol. 1985;  164 33-44
  • 24 Rhodes M JC, Robins R J, Hamill J D, Parr A J, Walton N J. Secondary product formation using Agrobacterium rhizogenes- transformed ”hairy root” cultures.  TCA Newletters. 1987;  53 2-15
  • 25 Zupan J. The transfer of DNA from Agrobacterium tumefaciens into plants: a feast of fundamental insights.  Plant J. 2000;  23 11-28
  • 26 Tinland B. The integration of T-DNA into plant genomes.  Trends Plant Sci. 1996;  6 178-84
  • 27 Vilaine F, Casse-Delbart F. Independent induction of transformed roots by the TL and TR regions of the Ri plasmid of agropine type Agrobacterium rhizogenes .  Mol Gen Genet. 1987;  206 17-23
  • 28 Cardarelli M, Spanó L, De Paolis A, D' Mauro M L, Vitali G, Costantino P. Identification of the genetic locus responsible for non-polar root induction by Agrobacterium rhizogenes 1855.  Plant Mol Biol. 1985;  5 385-391
  • 29 Moyano E, Fornalé S, Palazón J, Cusidó R M, Bonfill M, Morales C. et al . Effect of Agrobacterium rhizogenes T-DNA on alkaloid production in Solanaceae plants.  Phytochemistry. 1999;  52 1287-92
  • 30 Binns A N. Cell biology of Agrobacterium infection and transformation of plants.  Ann Rev Microbiol. 1988;  42 575-606
  • 31 Zupan J R, Zambryski P. Transfer of T-DNA from Agrobacterium to the plant cell.  Plant Physiol. 1995;  107 1041-7
  • 32 Zambryski P. Basic processes underlying Agrobacterium-mediated DNA trasfer to plant cells.  Annu Rev Genet. 1988;  22 1-30
  • 33 Murashige T, Skoog F. A revised medium for rapid growth and bioassys with tobacco tissue cultures.  Physiol Plant. 1962;  15 473-9
  • 34 Gamborg O L, Miller R A, Ojima K. Nutrient requirements of suspension cultures of soybean root cells.  Exp Cell Res. 1968;  50 151-58
  • 35 Deno H, Yamagata H, Emoto T, Yoshioka T, Yamada Y, Fujita Y. Scopolamine production by root cultures of Duboisia myoporoides II. Establishment of a hairy root culture by infection with Agrobacterium rhizogenes .  J Plant Physiol. 1987;  131 315-23
  • 36 Vanhala L, Hiltunen R, Oksman-Caldentey K -M. Virulence of different Agrobacterium strains on hairy root formation of Hyoscyamus muticus .  Plant Cell Rep. 1995;  14 236-40
  • 37 Jung G, Tepfer D. Use of genetic transformation by the Ri T-DNA of Agrobacterium rhizogenes to stimulate biomass and tropane alkaloid production in Atropa belladonna and Calystegia sepium roots grown in vitro .  Plant Sci. 1987;  50 145-51
  • 38 Hamill J D, Robins R J, Rhodes M JC. Alkaloid production by transformed root cultures of Cinchona ledgeriana .  Planta Med. 1989;  55 354-7
  • 39 Banerjee S, Naqvi A A, Mandal S, Ahuja P S. Transformation of Withania somnifera (L) Dunal by Agrobacterium rhizogenes: Infectivity and phytochemical studies.  Phytother Res. 1994;  8 452-5
  • 40 Trypsteen M, Van Lijsebettens M, Van Severen R, Van Montagu M. Agrobacterium rhizogenes-mediated transformation of Echinacea purpurea .  Plant Cell Rep. 1991;  10 85-9
  • 41 Godwin I, Todd G, Ford-Lloyd B, Newbury H J. The effects of acetosyringone and pH on Agrobacterium mediated transformation vary according to plant species.  Plant Cell Rep. 1991;  9 671-5
  • 42 Flores H E, Hoy M W, Pickard J J. Secondary metabolites from root cultures.  Trends Biotechnol. 1987;  5 64-8
  • 43 Tepfer D. Transformation of several species of higher plants by Agrobacterium rhizogenes: sexual transmission of the transformed genotype and phenotype.  Cell. 1984;  37 959-67
  • 44 Hamill J D, Rounsley S, Spencer A, Todd G, Rhodes M JC. The use of the polymerase chain reaction in plant transformation studies.  Plant Cell Rep. 1991;  10 221-4
  • 45 Sevón N, Dräger B, Hiltunen R, Oksman-Caldentey K -M. Characterization of transgenic plants derived from hairy roots of Hyoscyamus muticus .  Plant Cell Rep. 1997;  14 738-42
  • 46 Sevón N, Hiltunen R, Oksman-Caldentey K -M. Chitosan increases hyoscyamine content in hairy root cultures of Hyoscyamus muticus .  Pharm Pharmacol Lett. 1992;  2 96-9
  • 47 Hamill J D, Parr A J, Robins R J, Rhodes M JC. Secondary product formation by cultures of Beta vulgaris and Nicotiana rustica transformed with Agrobacterium rhizogenes .  Plant Cell Rep. 1986;  5 111-4
  • 48 Parr A J, Hamill J D. Relationship between Agrobacterium rhizogenes transformed hairy roots and intact, uninfected Nicotiana plants.  Phytochemistry. 1987;  26 3241-5
  • 49 Boitel-Conti M, Gontier E, Laberche J C, Ducrocq C, Sangwan-Norreel B S. Permeabilization of Datura innoxia hairy roots for release of stored tropane alkaloids.  Planta Med. 1995;  61 287-90
  • 50 Mano Y, Ohkawa H, Yamada Y. Production of tropane alkaloids by hairy root cultures of Duboisia leichhardtii transformed by Agrobacterium rhizogenes .  Plant Sci. 1989;  59 191-201
  • 51 Bhadra R, Vani S, Shanks J V. Production of indole alkaloids by selected hairy root lines of Catharanthus roseus .  Biotechnol Bioeng. 1993;  41 581-92
  • 52 Oksman-Caldentey K -M, Sevón N, Vanhala L, Hiltunen R. Effect of nitrogen and sucrose on the primary and secondary metabolism of transformed root cultures of Hyoscyamus muticus .  Plant Cell Tissue Organ Cult. 1994;  38 263-72
  • 53 Nabeshima S, Mano Y, Okhawa H. Production of tropane alkaloids by hairy root cultures of Scopolia japonica .  Symbiosis. 1986;  2 11-8
  • 54 Tepfer D. Genetic transformation using Agrobacterium rhizogenes .  Physiol Plant. 1990;  79 140-6
  • 55 Saito K, Yamazaki M, Murakoshi I. Transgenic medicinal plants: Agrobacterium-mediated foreign gene transfer and production of secondary metabolites.  J Nat Prod. 1992;  55 149-62
  • 56 Saito K, Yamazaki M, Kawaguchi A, Murakoshi I. Metabolism of Solanaceous alkaloids in transgenic plant teratomas integrated with genetically engineered genes.  Tetrahedron. 1991;  47 5955-68
  • 57 Larkin P J, Scowcroft W R. Somaclonal variation - A novel source of variability from cell cultures for plant improvement.  Theor Appl Genet. 1981;  60 197-214
  • 58 Oksman-Caldentey K -M, Strauss A. Somaclonal variation of scopolamine content in protoplast-derived cell cultures clones of Hyoscyamus muticus .  Planta Med. 1986;  52 6-12
  • 59 Oksman-Caldentey K -M, Vuorela H, Strauss A, Hiltunen R. Variation in the tropane alkaloid content of Hyoscyamus muticus plants and cell culture clones.  Planta Med. 1987;  53 349-54
  • 60 Oksman-Caldentey K -M, Vuorela H, Isenegger M, Strauss A, Hiltunen A. Selection for high tropane alkaloid content in Hyoscyamus muticus plants.  Plant Breed. 1987;  99 318-26
  • 61 Berlin J. Screening and selection for variant cell lines with increased levels of secondary metabolites. In: Charlwood BV, Rhodes MJC, editors Secondary products from plant tissue cultures. Oxford Science Publication, Clarendon Press 1990: 119-37
  • 62 Yukimune Y, Hara Y, Yamada Y. Tropane alkaloid production in root cultures of Duboisia myoporoides obtained by repeated selection.  Biosci Biotech Biochem. 1994;  58 1443-6
  • 63 Robins R J, Hamill J D, Parr A J, Smith K, Walton N J, Rhodes M JC. Potential for use of nicotinic acid as a selective agent for isolation of high nicotine-producing lines of Nicotiana rustica hairy root cultures.  Plant Cell Rep. 1987;  6 122-6
  • 64 Medina-Bolivar F, Flores H E. Selection for hyoscyamine and cinnamoyl putrescine overproduction in cell and root cultures of Hyoscyamus muticus .  Plant Physiol. 1995;  108 1553-60
  • 65 Sevón N, Oksman-Caldentey K -M, Hiltunen R. Efficient regeneration of plants from hairy root-derived protoplasts of Hyoscyamus muticus .  Plant Cell Rep. 1995;  14 738-42
  • 66 Furze J M, Hamill J D, Parr A J, Robins R J, Rhodes M JC. Variations in morphology and nicotine alkaloid accumulation in protoplast-derived hairy root cultures of Nicotiana rustica .  J Plant Physiol. 1987;  131 237-46
  • 67 Toivonen L. Utilization of hairy root cultures for production of secondary metabolites.  Biotechnol Prog. 1993;  9 12-20
  • 68 Toivonen L, Ojala M, Kauppinen V. Studies on the optimization of growth and indole alkaloid production by hairy root cultures of Catharanthus roseus .  Biotechnol Bioeng. 1991;  37 673-80
  • 69 Hilton M G, Wilson P DG. Growth and uptake of sucrose and mineral ions by transformed root cultures of Datura stramonium, Datura candida x aurea, Datura wrightii, Hyoscyamus muticus and Atropa belladonna .  Planta Med. 1995;  61 345-50
  • 70 Christen P, Aoki T, Shimomura K. Characteristics of growth and tropane alkaloid production in Hyoscyamus albus hairy roots transformed with Agrobacterium rhizogenes A4.  Plant Cell Rep. 1992;  11 597-600
  • 71 Morgan J A, Barney C S, Penn A H, Shanks J V. Effects of buffered media upon growth and alkaloid production of Catharanthus roseus hairy roots.  Appl Microbiol Biotechnol. 2000;  53 262-65
  • 72 Rhodes M JC, Parr A J, Giulietti A. Aird ELH. Influence of exogenous hormones on the growth and secondary metabolite formation in transformed root cultures.  Plant Cell Tissue Org Cult. 1994;  38 143-51
  • 73 Arroo R RJ, Develi A, Meijers H, Van de Westerlo E, Kemp A K, Croes A F. et al . Effect of exogenous auxin on root morphology and secondary metabolism in Tagetes patula hairy root cultures.  Physiol Plant. 1995;  93 233-40
  • 74 Toivonen L, Laakso S, Rosenqvist H. The effect of temperature on hairy root cultures of Catharanthus roseus: Growth, indole alkaloid accumulation and membrane lipid composition.  Plant Cell Rep. 1992;  11 395-9
  • 75 Bhadra R, Shanks J V. Statistical design of the effect of inoculum conditions on growth of hairy root cultures of Catharanthus roseus .  Biotechnol Tech. 1995;  9 681-6
  • 76 Zehra M, Banerjee S, Sharma S, Kumar S. Influence of Agrobacterium rhizogenes strains on biomass and alkaloid productivity in hairy root lines of Hyoscyamus muticus and H. albus .  Planta Med. 1999;  65 60-3
  • 77 Payne J, Hamill J D, Robins R J, Rhodes M JC. Production of hyoscyamine by ”hairy root” cultures of Datura stramonium .  Planta Med. 1987;  53 474-8
  • 78 Bensaddek L, Gillet F, Saucedo J EN, Fliniaux M -A. The effect of nitrate and ammonium concentrations on growth and alkaloid accumulation of Atropa belladonna hairy roots.  J Biotech. 2001;  85 35-40
  • 79 Eilert U. Elicitation: Methodology and aspects of application. In: Constabel F, Vasil IK, editors Cell culture and somatic genetics of plants. Vol. 4 Academic press Inc San Diego, New York, Berkley, Boston, London, Sydney, Tokyo, Toronto; 1987: 153-88
  • 80 DiCosmo F, Misawa M. Eliciting secondary metabolism in plant cell cultures.  Trends Biotech. 1985;  3 318-22
  • 81 Brodelius P, Pedersen H. Increasing secondary metabolite production in plant-cell culture by redirecting transport.  TIBTECH. 1993;  11 30-6
  • 82 Buitelaar R M, Leenen E JTM, Geurtsen G, Æ de G root, Tramper J. Effects of the addition of XAD-7 and of elicitor treatment on growth, thiophene production, and excretion by hairy roots of Tagetes patula .  Enzyme Microb Technol. 1993;  15 670-6
  • 83 Pitta-Álvarez S I, Spollansky T C, Giulietti A M. Scopolamine and hyoscyamine production by hairy root cultures of Brugmansia candida: influence of calcium chloride, hemicellulase and theophylline.  Biotechnol Lett. 2000;  22 1653-6
  • 84 Pitta-Álvarez S I, Spollansky T C, Giulietti A M. The influence of different biotic and abiotic elicitors on the production and profile of tropane alkaloids in hairy root cultures of Brugmansia candida .  Enzyme Microb Technol. 2000;  26 252-8
  • 85 Cusidó R M, Palazón J, Piñol M T, Bonfill M, Morales C. Datura metel: in vitro production of tropane alkaloids.  Planta Med. 1999;  65 144-48
  • 86 Brodelius P, Funk C, Häner A, Villegas M. A prosedure for the determination of optimal chitosan concentration for elicitation of cultured plant cells.  Phytochemistry. 1989;  28 2651-4
  • 87 Dörnenburg H, Knorr D. Strategies for the improvement of secondary metabolite production in plant cell cultures.  Enzyme Microb Technol. 1995;  17 674-84
  • 88 Davioud E, Kan C, Hamon J, Tempé J, Husson H -P. Production of indole alkaloids by in vitro root cultures from Catharanthus trichophyllus .  Phytochemistry. 1989;  28 2675-80
  • 89 Toivonen L, Ojala M, Kauppinen V. Indole alkaloid production by hairy root cultures of Catharanthus roseus: growth kinetics and fermentation.  Biotechology Lett. 1990;  12 519-24
  • 90 Wilson P DG. The cultivation of transformed roots from laboratory to pilot plant. Progress in plant cellular and molecular biology. In: Nijkamp HJJ, van der Plas LHW, van Aartrijk J, editors Kluwer Academic Publishers Dordrech,-Boston, London; 1990: 700-5
  • 91 Eibl R, Lettenbauer C, Eibl D, Röll M. Experiences in the application of the wave bioreactors.  Bioforum. 1999;  3 110-2
  • 92 Eibl R, Eibl D. Bioreactors for plant cell and tissue cultures. Plant Biotechnology and Transgenic Plants. In: Oksman-Caldentey K-M, Barz W, editors Marcel & Dekker New York; 2002; Chapter 8
  • 93 Verpoorte R, van der Heijden R, Memelink J. Engineering the plant cell factory for secondary metabolite production.  Transg Res. 2000;  9 323-43
  • 94 Saito K, Kaneko H, Yamazaki M, Yoshida M, Murakoshi I. Stable transfer and expression of chimeric genes in licorice (Glycyrrhiza uralensis) using an Ri plasmid binary vector.  Plant Cell Rep. 1990;  8 18-21
  • 95 Saito K, Yamazaki M, Shimomura K, Yoshimatsu K, Murakoshi I. Genetic transformation of foxglove (Digitalis purpurea) by chimeric foreign genes and production of cardioactive glycosides.  Plant Cell Rep. 1990;  9 121-4
  • 96 Saito K, Noji M, Ohmori S, Imai Y, Murakoshi I. Integration and expression of a rabbit liver cytochrome P-450 gene in transgenic Nicotiana tabacum .  Proc Natl Acad Sci USA. 1991;  88 7041-5
  • 97 Yun D -J, Hashimoto T, Yamada Y. Metabolic engineering of medicinal plants: Transgenic Atropa belladonna with an improved alkaloid composition.  Proc Natl Acad Sci. 1992;  89 11 799-803
  • 98 Hashimoto T, Yun D -J, Yamada Y. Production of tropane alkaloids in genetically engineered root cultures.  Phytochemistry. 1993;  32 713-8
  • 99 Jouhikainen K ., Lindgren L, Jokelainen T, Hiltunen R, Teeri T H, Oksman-Caldentey K -M. Enhancement of scopolamine production in Hyoscyamus muticus L. hairy root cultures by genetic engineering.  Planta. 1999;  208 545-51
  • 100 Oksman-Caldentey K M, Arroo R. Regulation of tropane alkaloid metabolism in plants and plant cell cultures. Metabolic Engineering of Plant Secondary Metabolism. In: Verpoorte R, Alfermann AW, editors Kluwer Academic Publishers Dordrech, Boston, London; 2000: 253-81
  • 101 De Luca V. Metabolic engineering of crops with tryptophan decarboxylase of Catharanthus roseus. Metabolic engineering of plant secondary metabolism. In: Verpoorte, R, Alfermann AW, editors Kluwer Academic Publishers Dordrecht; 2000: 179-94
  • 102 Giri A, Banerjee S, Ahuja P S, Giri C C. Production of hairy roots in Aconitum heterophyllum wall. Using Agrobacterium rhizogenes .  In vitro Cell Biol-Plant. 1997;  33 280-84
  • 103 Kamada H, Okamura N, Satake M, Harada H, Shimomura K. Alkaloid production by hairy root cultures in Atropa belladonna .  Plant Cell Rep. 1986;  5 239-42
  • 104 Lee K T, Suzuki T, Yamakawa T, Kodama T, Igarashi Y, Shimomura K. Production of tropane alkaloids by transformed root cultures of Atropa belladonna in stirred bioreactors with a stainless steel net.  Plant Cell Rep. 1999;  18 567-71
  • 105 Nakanishi F, Sasaki K, Shimomura K. Isolation and identification of littorine from hairy roots of Atropa belladonna .  Plant Cell Rep. 1998;  18 249-51
  • 106 Giulietti A M, Parr A J, Rhodes M JC. Tropane alkaloid production in transformed root cultures of Brugmansia candida .  Planta Med. 1993;  59 428-31
  • 107 Geerlings A, Hallard D, Martinez Caballero A, Lopez Cardosi I, van der Heijden R, Verpoorte R. Alkaloid production of Cinchona officinalis (”Ledgeriana”) hairy root culture containing constitutive expression constructs of tryptophan decarboxylase and stryctosidine synthase cDNAs from Catharanthus roseus .  Plant Cell Rep. 1999;  19 191-6
  • 108 Hallard D, Geerlings A, van der Heijden R, Lopez cardoso I, Hoge J HC, Verpoorte R. Metabolic engineering of terpenoid indole and quinoline alkaloid biosynthesis in hairy root cultures. Hairy roots. In: Doran PM, editor Harwood Academic Publishers Amsterdam; 1997: 43-9
  • 109 Christen P, Roberts M F, Phillipson J D, Evans W C. High-yield production of tropane alkaloids by hairy-root cultures of a Datura candida hybrid.  Plant Cell Rep. 1989;  8 75-7
  • 110 Shimomura K, Sauerwein M, Ishimaru K. Tropane alkaloids in adventitious and hairy root cultures of Solanaceous plants.  Phytochemistry. 1991;  30 2275-8
  • 111 Altabella T, Palazón J, Ribó M, Angel E, Piñol M T. Comparative study of tropane alkaloid production in transformed roots of Datura stramonium and Scopolia carniolica .  Plant Physiol. 1994;  13 113-23
  • 112 Jaziri M, Legros M, Homes J, Vanhaelen M. Tropine alkaloids production by hairy root cultures of Datura stramonium and Hyoscyamus niger .  Phytochemistry. 1988;  27 419-20
  • 113 Zabetakis I, Edwards R, OŽHagan D. Elicitation of tropane alkaloid biosynthesis in transformed root cultures of Datura stramonium .  Phytochemistry. 1999;  50 53-6
  • 114 Sauerwein M, Wink M. On the role of opines in plants transformed with Agrobacterium rhizogenes: Tropane alkaloid metabolism, insect-toxicity and allelophathic properties.  J Plant Physiol. 1993;  142 446-51
  • 115 Palazón J, Cusidó R M, Roig C, Piñol M T. Expression of the rolC gene and nicotine production in transgenic roots and their regenerated plants.  Plant Cell Rep. 1998;  17 384-90
  • 116 Hamill J D, Robins R J, Parr A J, Evans D M, Furze JM and Rhodes M JC. Over-expressing a yeast ornithine decarboxylase gene in transgenic roots of Nicotiana rustica can lead to enhanced nicotine accumulation.  Plant Mol Biol. 1990;  15 27-38
  • 117 Berlin J, Kuzovkina I M, Rügenhagen C, Fecker L, Commandeur U, Wray V. Hairy root cultures of Peganum harmala II. Characterization of cell lines and effect of culture conditions on the accumulation of β-carboline alkaloids and serotonin.  Z Naturforch C Biosci. 1992;  47 222-30
  • 118 Mano Y, Nabeshima S, Matsui C, Ohkawa H. Production of tropane alkaloids by hairy root cultures of Scopolia japonica .  Agric Biol Chem. 1986;  50 2715-22
  • 119 Hallard D. Transgenic plant cells for the production of indole alkaloids. PhD thesis, University of Leiden The Netherlands; 2000
  • 120 Vázquez-Flota F, Moreno-Valenzuela O, Miranda-Ham M L, Coello-Coello J, Loyola-Vargas V M. Catharanthine and ajmalicine synthesis in Catharanthus roseus hairy root cultures.  Plant Cell Tissue Organ Cult. 1994;  38 73-9
  • 121 Sim S J, Chang H N, Liu J R, Jung K H. Production and secretion of indole alkaloids in hairy root cultures of Catharanthus roseus: Effects of in situ adsorption, fungal elicitation and permeabilization.  J Ferm Bioeng. 1994;  78 229-34
  • 122 Furze J M, Rhodes M JC, Parr A J, Robins R J, Whitehead I M, Threlfall D R. Abiotic factors elicit sesquiterpenoid phytoalexin production but not alkaloid production in transgenic root cultures of Datura stramonium .  Plant Cell Rep. 1991;  10 111-4
  • 123 Signs M W, Flores H E. Elicitation of sesquiterpene phytoalexin biosynthesis in transformed root cultures of Hyoscyamus muticus .  Plant Physiol. 1989;  89 Supp. 135
  • 124 Dunlop D S, Curtis W R. Synergistic response of plant hairy-root cultures to phosphate limitation and fungal elicitation.  Biotechnol Prog. 1991;  7 434-8
  • 125 Pannuri S, Ramakrishna R, McNeill D, Curtis W R. Interpreting the role of phosphorus and growth rate in enhanced fungal induction of sesquiterpenes from Hyoscyamus muticus root cultures.  Appl Microbiol Biotechnol. 1993;  38 550-5
  • 126 Ramakrishna G, Signs M W. Reversed-phase liquid chromatographic isolation of lubimin and solavetivone from Hyoscyamus muticus ”hairy” root cultures.  J Chromatogr. 1993;  657 440-4
  • 127 Biondi S, Formale S, Oksman-Caldentey K -M, Eeva M, Agostani S, Bagni N. Jasmonates induce over-accumulation of methylputrescine and hydroycinnamoyl amide content in Hyoscyamus muticus L. root cultures.  Plant Cell Rep. 2000;  19 691-97
  • 128 Singh G, Gavrieli J, Oakey J S, Curtis W R. Interaction of methyl jasmonate, wounding and fungal elicitation during sesquiterpene induction in Hyoscyamus muticus in root cultures.  Plant Cell Rep. 1998;  17 391-5
  • 129 Wibberley M S, Lenton J R, Neill S J. Sesquiterpenoid phytoalexins produced by hairy roots of Nicotina tabacum .  Phytochemistry. 1994;  37 349-51

Dr. Kirsi-Marja Oksman-Caldentey

VTT Biotechnology

P.O. Box 1500

FIN-02044 VTT (Espoo)

Finland

Fax: +358-9-455-2103

Email: kirsi-marja.oksman@vtt.fi

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