Use of Transformed Roots for Root Development and Metabolism Studies and Progress in Characterizing Root-Specific Gene Expression

  • John D. Hamill
  • Stephen F. Chandler
Part of the Basic Life Sciences book series (BLSC, volume 62)


Following reports in the early 1980s that adventitious roots that were transformed with Agrobacterium rhizogenes often grow rapidly in hormone-free medium in vitro, there has been an upsurge in the use of transformed root cultures as a system to study root metabolism and associated root biology. As DNA transfer is involved in the interaction between A. rhizogenes and higher plants, there has also been a great deal of interest in using this bacterium as a vector to genetically manipulate plants. More than 460 plant species from over 100 families have been transformed by A. rhizogenes (Porter, 1991) and in many cases axenic transformed roots have been reported to grow rapidly in vitro (Hamill and Rhodes, 1992). In general, such transformed root cultures are quite stable at the gross chromosomal level, so long as the integrity of the meristem is not disturbed, e.g., by the addition of phytohormones to the medium (Aird et al., 1988a, b). Transformed root cultures have been used for secondary metabolite studies and also, to a lesser extent, to examine the interactions between soil organisms and roots of higher plants (Hamill and Rhodes, 1992). The recovery and growth of plants in soil demonstrates that roots containing Ri T-DNA can provide nutrient and water uptake requirements, though few studies have critically evaluated the differences between normal and transformed roots with respect to these functions.


Hairy Root Lateral Root Root Culture Hairy Root Culture Indole Alkaloid 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Ahn, J.C., Paek, Y.W., Kang, Y.H., and Hwang, B., 1992, Production of anthocyanin by culture of hairy roots of Raphanus sativus, Korean J. Bot. 35:35.Google Scholar
  2. Aird, E.L.H., Hamill, J.D., and Rhodes, M.J.C., 1988a, Cytogenetic analysis of hairy root cultures from a number of plant species transformed by Agrobacterium rhizogenes, Plant Cell Tissue Organ Cult. 15:47CrossRefGoogle Scholar
  3. Aird, E.L.H., Hamill, J.D., Robins, R.J., and Rhodes, M.J.C., 1988b, Chromosome stability in transformed hairy root cultures and the properties of variant lines of Nicotiana rustica hairy roots, in: “Manipulating Secondary Metabolism in Culture,” R.J. Robins, and M.J.C. Rhodes, eds., Cambridge Univ. Press, Cambridge.Google Scholar
  4. Altamura, M.M., Archiletti, T., Capone, I., and Costantino, P., 1991, Histological analysis of the expression of Agrobacterium rhizogenes rol B-GUS gene fusions in transgenic tobacco, New Phytol. 118:118.CrossRefGoogle Scholar
  5. Asamizu, T., Akiyama, K., and Yasuda, I., 1988, Anthoquinones production by hairy root culture in Cassia obtusifolia, Yakagaku zasshi 108:108.Google Scholar
  6. Bassil, N.V., Proebsting, W.M., Moore, L.W., and Lightfoot, D.A., 1991, Propagation of Hazelnut stem cuttings using Agrobacterium rhizogenes, Hortic. Sci. 26:26.Google Scholar
  7. Benfey, P.N., Ling, R., and Chua, N.H., 1990, Combinatorial and synergistic properties of CaMV35S enhancer subdomains, EMBO J. 9:9.Google Scholar
  8. Benfey, P.N., Ren, L., and Chua, N.H., 1989, The CaMV35S enhancer contains at least two domains which can confer different developmental and tissue specific expression patterns, EMBO J. 8:8.Google Scholar
  9. Berlin, J., Dietze, P., Fecker, L., Goddijn, O., and Hoge, J.H.C., 1991a, Production of high levels of serotonin in Peganum cultures by expression of a foreign plant tryptophan decarboxylase, in: “Abstracts 3rd Int. Cong. Plant Mol. Biol.,” R.B. Hallick, ed., Tucson.Google Scholar
  10. Berlin, J., Fecker, L., Ruegenhagen, C., Sator, C., Strack, D., Witte, L., and Wray, V., 1991b, Isoflavone glycoside formation in transformed and non-transformed suspension and hairy root cultures of Lupinus polyphyllus and Lupinus hartwegii, Z. Naturforsch. (C) 46:725.Google Scholar
  11. Berlin, J., Kuzokina, I.N., Ruegenhagen, C., Fecker, L., Commandeur, U., and Wray, V.L., 1992, Hairy root cultures of Peganum harmala: characterization of cell lines and effects of culture conditions on the accumulation of beta-carboline alkaloids and seratonin, Z. Naturforsch. (C) 47:47.Google Scholar
  12. Bogusz, D., Appleby, C.A., Landsmann, J., Dennis, E.S., Trinick, M.J., and Peacock, W.J., 1988, Functioning hemoglobin genes in a non-nodulating plant, Nature 331:178.PubMedCrossRefGoogle Scholar
  13. Bogusz, D., Llewellyn, D.J., Craig, S., Dennis, E.S., Appleby, C.A., and Peacock, W.J., 1990, Non-legume hemoglobin genes retain organ specific expression in heterologous transgenic plants, Plant Cell 2:2.Google Scholar
  14. Bouchez, D., Tokuhisa, J.G., Llewellyn, D.J., Dennis, E.S., and Ellis, J.G., 1989, The ocs-element is a component of the promoters of several T-DNA and plant viral genes, EMBO J. 8:8.Google Scholar
  15. Bracher, D., and Kutchan, T.M., 1992, Strictosidine synthase from Rauvolfia serpentina: analysis of a gene involved in indole alkaloid biosynthesis, Arch. Biochem. Biophys. 294:294.CrossRefGoogle Scholar
  16. Capone, I., Spano, L., Cardarelli, M., Bellincampi, D., Petit, A., and Costantino, P., 1989, Induction and growth properties of carrot roots with different complements of Agrobacterium rhizogenes T-DNA, Plant Mol. Biol. 13:13.CrossRefGoogle Scholar
  17. Capone, L, Ardarelli, M., Mariotti, D., Pomponi, M., De Paolis, A., and Costantino, P., 1991, Different promoter regions control level and tissue specificity of expression of Agrobacterium rhizogenes rol B gene in plants, Plant Mol. Biol. 16:16.CrossRefGoogle Scholar
  18. Chamberlain, D.A., Wilson, G., and Ryan, M.F., 1991, Trans-2-nonenal insect repellent, insecticide and flavour compound in carrot roots, cell suspension and hairy root cultures, J. Chem. Ecol. 17:17.CrossRefGoogle Scholar
  19. Christen, P., Roberts, M.F., Phillipson, J.D., and Evans, W.C., 1989, High yield production of tropane alkaloids by hairy-root cultures of a Datura Candida hybrid, Plant Cell Rep. 8:8.CrossRefGoogle Scholar
  20. Comai, L., Moran, P., and Maslyar, D., 1990, Novel and useful properties of a chimeric plant promoter combining CaMV35S and MAS elements, Plant Mol Biol. 15:15.CrossRefGoogle Scholar
  21. Conkling, M.A., Cheng, C.L., Yamamoto, Y.T., and Goodman, H.M., 1990, Isolation of transcriptionally regulated root specific genes from tobacco, Plant Physiol. 93:93.CrossRefGoogle Scholar
  22. Constabel, C.P., and Towers, G.H.N., 1988, Thiarubrine accumulation in hairy root cultures of Chaenactis douglasii, J. Plant Physiol. 133:133.CrossRefGoogle Scholar
  23. Croes, A.F., van den Berg, A.J.R., Bosveld, M., Breteler, H., and Wullems, G.J., 1989, Thiophene accumulation in relation to morphology in roots of Tagetes patula: Effects of auxin and transformation by Agrobacterium, Planta 179:179.CrossRefGoogle Scholar
  24. Davioud, E., Kan, C., Hamon, J., Tempé, J., and Husson, H.P., 1989, Production of indole alkaloids by in vitro root cultures from Catharanthus trichophyllus, Phytochem. 28:28.Google Scholar
  25. Deno, H., Yamagata, T., Emoto, T., Yoshioka, T., Yamada, Y., and Fijita, Y., 1987, Scopalamine production by root cultures of Duboisa myoporoides, II. Establishment of a hairy root culture by infection with Agrobacterium rhizogenes, J. Plant Physiol. 131:131.CrossRefGoogle Scholar
  26. de Pater, B.S., and Schilperoort, R.A., 1992, Structure and expression of a root-specific rice gene, Plant Mol. Biol. 18:18.CrossRefGoogle Scholar
  27. Dietrich, R.A., Radke, S.E., and Harada, J.T., 1992, Downstream DNA sequences are required to activate a gene expressed in the root cortex of embryos and seedlings, Plant Cell 4:4.Google Scholar
  28. Dynan, W.S., 1989, Modularity in promoters and enhancers, Cell 58:58.CrossRefGoogle Scholar
  29. Durand-Tardif, M., Broglie, R., Slighton, J., and Tepfer, D., 1985, Structure and expression of Ri T-DNA from Agrobacterium rhizogenes in Nicotiana tabaccum: organ and phenotypic specificity, J. Mol. Biol. 186:186.CrossRefGoogle Scholar
  30. Estruch, J.J., Schell, J., and Spena, A., 1991a, The protein encoded by the rol B plant oncogene hydrolyses indole glucosides, EMBO J., 10:3125.Google Scholar
  31. Estruch, J.J., Chriqui, D., Grossman, K., Schell, J., and Spena, A., 1991b, The plant oncogene rol C is responsible for the release of cytokinins from glucoside conjugates, EMBO J. 10:2889.PubMedGoogle Scholar
  32. Fitter, A.H., 1991, Characteristics and functions of root systems, in: “Plant Roots: The Hidden Half,” Y. Waisel, A. Eshel, and U. Kafkafi, eds., Marcel Dekker, New York.Google Scholar
  33. Flores, H.E., Pickard, J J., and Hoy, M.W., 1988, Production of polyacetylenes and thiophenes in heterotrophic and photosynthetic root cultures of Asteraceae, in: “Chemistry and Biology of Naturally Occurring Acetylenes and Related Compounds (NOARC). Bioactive Molecules,” J. Lam, H. Breheler, T. Arnason, and L. Hansen, eds., 7:233.Google Scholar
  34. Flores, H.E., and Filner, P., 1985, Metabolic relationships of putrescine, GABA and alkaloids in cell and root cultures of Solanaceae, in: “Primary and Secondary Metabolism of Plant Cell Cultures”, K.H. Nuemann, W., Barz, and E. Reinhard, eds., Springer-Verlag, Berlin.Google Scholar
  35. Fromm, H., Katagiri, F., and Chua, N.H., 1989, An octopine synthase enhancer element directs tissue specific expression and binds ASF-1, a factor from tobacco nuclear extracts, Plant Cell 1:1.Google Scholar
  36. Furze, J.M., Rhodes, M.J.C., Parr, AJ., Robins, RJ., Whitehead, J.M., and Threlfall, D.R., 1991, Abiotic factors elicit sesquiterpenoid phytoalexin production but not alkaloid production in transformed roots of Datura stramonium, Plant Cell Rep. 10:10.CrossRefGoogle Scholar
  37. Hamill, J.D., and Rhodes, M.J.C., 1992, Manipulating secondary metabolism in culture, in: “Biosynthesis and Manipulation of Plant Products, Plant Biotechnology,” vol. 3, D. Grierson, ed., Chapman and Hall, London.Google Scholar
  38. Hamill, J.D., Robins, RJ., and Rhodes, M.J.C., 1989, Alkaloid production by transformed root cultures of Cinchona ledgeriana, Planta Med. 55:55.CrossRefGoogle Scholar
  39. Hamill, J.D., Parr, A.J., Robins, R.J., and Rhodes, M.J.C., 1986, Secondary product formation by cultures of Beta vulgaris and Nicotiana rustica transformed with Agrobacterium rhizogenes, Plant Cell Rep. 5:5.CrossRefGoogle Scholar
  40. Hamill, J.D., Robins, R.J., Parr, AJ., Evans, D.M., Furze, J.M., and Rhodes, M.J.C., 1990, Overexpressing a yeast ornithine decarboxylase gene in transgenic roots of Nicotiana rustica can lead to enhanced nicotine accumulation, Plant Mol. Biol. 15:15.CrossRefGoogle Scholar
  41. Handa, T., 1992, Genetic transformation of Antirrhinum majus L. and inheritance of altered phenotype induced by Ri T-DNA, Plant Sci. 81:81.CrossRefGoogle Scholar
  42. Hashimoto, T., Hayashi, A., Amano, Y., Kohno, J., Iwanari, H., Usuda, S., and Yamada, Y., 1991, Hyosycamine 6ß-hydroxylase, an enzyme involved in tropane alkaloid biosynthesis, is localised at the pericycle of the root, J. Biol. Chem. 266:266.Google Scholar
  43. Hauth, S., and Beiderbeck, R., 1992, In vitro culture of Agrobacterium rhizogenes induced hairy roots by Salix alba, Silvae Genetica 41:41.Google Scholar
  44. Hoff, T., Stummann, B.M., and Henningsen, K.W., 1991, Cloning and expression of a gene encoding a root specific nitrate reductase in bean (Phaseolus vulgaris), Physiol. Plant. 82:82.CrossRefGoogle Scholar
  45. Hu, Z.B., and Alfermann, A.W., 1993, Diterpenoid production in hairy root cultures of Salvia miltiorrhiza, Phytochem. 32:32.Google Scholar
  46. Hwang, B., Ko, K.M., Hwang, K.H., Hwang, S J., and Kang, Y.H., 1992, Production of saponin by hairy root cultures of ginseng (Panax ginseng), Korean J. Bot. 34:34.Google Scholar
  47. Ishimaru, K., Yonemitsu, H., and Shimomura, K., 1991, Lobetyolin and lobetyol from hairy root culture of Lobelia inflata, Phytochem. 30:30.Google Scholar
  48. Ishimaru, K., Sadoshima, S., Neer, S., Koyama, K., Takahashi, K., and Shimomura, K., 1992, A polyacetylene gentiobioside from hairy roots of Lobelia inflata, Phytochem. 31:31.Google Scholar
  49. Jung, G., and Tepfer, D., 1987, 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. 50:50.CrossRefGoogle Scholar
  50. Kamada, H., Okamura, N., Satake, M., Harada, M., and Shimomura, K., 1986, Alkaloid production by hairy root cultures in Atropa belladonna, Plant Cell Rep. 5:5.CrossRefGoogle Scholar
  51. Katagiri, F., Lam, E., and Chua, N.H., 1989, Two tobacco DNA-binding proteins with homology to the nuclear factor CREB, Nature 340:340.CrossRefGoogle Scholar
  52. Keller, B., and Baumgartner, C., 1991, Vascular specific expression of the bean GRP 1.8 gene is negatively regulated, The Plant Cell 3:3.Google Scholar
  53. Keller, B., and Lamb, C.J., 1989, Specific expression of a novel cell wall hydroxyproline rich glycoprotein gene in lateral root induction, Genes Devel. 3:3.Google Scholar
  54. Lam, E., Benfey, P., Gilmartin, P., Fang, R., and Chua, N.H., 1989, Site specific mutations alter in vitro factor binding and change promoter expression pattern in transgenic plants, Proc. Natl. Acad. Sci. (USA) 86:86.Google Scholar
  55. Lambert, C., and Tepfer, D., 1991, Use of Agrobacterium rhizogenes to create chimeric apple trees through genetic grafting, Bio/Technol. 9:9.CrossRefGoogle Scholar
  56. Langridge, W.H.R., Fitzgerald, K.J., Koncz, C., Schell, J., and Szalay, A.A., 1989, Dual promoter of Agrobacterium tumefaciens mannopine synthase genes is regulated by plant growth hormones, Proc. Natl. Acad. Sci. (USA) 86:86.CrossRefGoogle Scholar
  57. Leach, F., and Aoyagi, K., 1991, Promoter analysis of the highly expressed rol C and rol D root inducing genes of Agrobacterium rhizogenes: enhancer and tissue specific DNA determinants are dissociated, Plant Sci. 79:79.CrossRefGoogle Scholar
  58. Linsey, K., Wei, W., Clarke, M.C., McArdle, H.F., Rooke, L.M., and Topping, J.F., 1993, Tagging genomic sequences that direct transgene expression by activation of a promoter trap in plants, Trangenic Res. 2:2.Google Scholar
  59. Maclsaac, S.A., Sawhney, V.K., and Pohorecky, Y., 1989, Regulation of lateral root formation in lettuce (Lactuca sativa) seedling roots: Interacting effects of-naphthalene acetic acid and kinetin, Physiol. Plant. 77:77.Google Scholar
  60. MacRae, S., 1991, Agrobacterium-modialed transformation of eucalypts to improve rooting ability, in: “IUFRO Symp. on Intensive Forestry: The Role of Eucalypts,” September, 1991, Durban.Google Scholar
  61. Mano, Y., Ohkawa, H., and Yamada, Y., 1989, Production of tropane alkaloids by hairy root cultures of Duboisia leichhardtii transformed by Agrobacterium rhizogenes, Plant Sci. 59:59.CrossRefGoogle Scholar
  62. Mano, Y., Nabeshima, S., Matsui, C., and Ohkawa, H., 1986, Production of tropane alkaloids by hairy root cultures of Scopolia japonica, Agric. Biol. Chem. 50:50.CrossRefGoogle Scholar
  63. Marchant, Y.Y., 1988, Agrobacterium rhizogenes — transformed root cultures for the study of polyacetylene metabolism and biosynthesis, in: “Chemistry and Biology of Naturally-occurring Acetylenes and Related Compounds (NOARC): Bioactive Molecules,” J. Lam, H. Breheler, T. Arnason, and L. Hansen, eds., 7:217.Google Scholar
  64. Matsuda, J., Okabe, S., Hashimoto, J., and Yamada, Y., 1991, Molecular cloning of hyoscyamine 6 ß-hydroxylase, a 2-oxoglutarate-dependent dioxygenase from cultured roots of Hyoscyamus niger, J. Biol. Chem. 266:266.Google Scholar
  65. Matsumoto, T., and Tanaka, N., 1991, Production of phytoecdysteroids by hairy root cultures of Ajuga reptans, Agric. Biol. Chem. 55:55.Google Scholar
  66. Maurel, C., Brevet, J., Barbier-Brygoo, H., Guern, J., and Tempé, J., 1990, Auxin regulates the promoter of the root inducing rol B gene of Agrobacterium rhizogenes in transgenic tobacco, Mol. Gen. Genet. 223:223.CrossRefGoogle Scholar
  67. Maurel, C., Barbier-Brygoo, H., Brevet, J., Spena, A., Tempé, J., and Guern, J., 1991, Single rol genes from the Agrobacterium rhizogenes TL T-DNA alter some of the cellular responses to auxin in Nicotiana tabac urn, Plant Physiol. 97:97.CrossRefGoogle Scholar
  68. Morris, P., and Robbins, M.P., 1992, Condensed tannin formation by Agrobacterium rhizogenes transformed root and shoot organ cultures of Lotus corniculatus, J. Exp. Bot. 43:43.CrossRefGoogle Scholar
  69. Mukundan, U., and Hjortso, M., 1990, Thiophene accumulation in hairy roots of Tagetes patula in response to fungal elicitors, Biotech. Lett. 12:12.CrossRefGoogle Scholar
  70. Murashige, T., and Skoog, F., 1962, A revised medium for rapid growth and bioassays with tobacco tissue cultures, Physiol. Plant. 15:15.CrossRefGoogle Scholar
  71. Nabeshima, S., Maro, Y., and Ohkawa, H., 1986, Production of tropane alkaloids of hairy root cultures of Scopolia japonica, Symbiosis 2:2.Google Scholar
  72. Ott, R.W., and Chua, N.H., 1990, Enhancer sequences from Arabidopsis thaliana obtained by library transformation of Nicotiana tabacum, Mol. Gen. Genet. 223:223.CrossRefGoogle Scholar
  73. Parr, A.J., 1992, Alternative metabolic fates of hygrine in transformed root cultures of Nicandra physaloides, Plant Cell Rep. 11:11.Google Scholar
  74. Parr, A.J., and Hamill, J.D., 1987, Relationship between Agrobacterium rhizogenes transformed hairy roots and intact uninfected Nicotiana plants, Phytochem. 26:26.CrossRefGoogle Scholar
  75. Parr, A.J., Peerless, A.C.J., Hamill, J.D., Walton, N.J., Robins, R.J., and Rhodes, M.J.C., 1988, Alkaloid production by transformed root cultures of Catharanthus roseus, Plant Cell Rep. 7:7.CrossRefGoogle Scholar
  76. Parr, A.J., Payne, J., Eagles, J., Chapman, B.T., Robins, R.J., and Rhodes, M.J.C., 1990, Variation in tropane alkaloid accumulation within the Solanaceae and strategies for its exploitation, Phytochem. 29:29.CrossRefGoogle Scholar
  77. Patena, I., Sutter, E., and Dandekar, A.M., 1988, Root induction by Agrobacterium rhizogenes in a difficult-to-root woody species, Acta Hortic. 227:227.Google Scholar
  78. Payne, J., Hamill, J.D., Robins, R.J., and Rhodes, M.J.C., 1987, Production of hyoscyamine by hairy root cultures of Datura stramonium, Planta Med. 53:53.Google Scholar
  79. Porter, J., 1991, Host range and implications of plant infection by Agrobacterium rhizogenes, Crit. Rev. Plant Sci. 10:10.CrossRefGoogle Scholar
  80. Rhodes, M.J.C., Hilton, M., Parr, A.J., Hamill, J.D., and Robins, R.J., 1986, Nicotine production by hairy root cultures of Nicotiana rustica: fermentation and product recovery, Biotech. Lett. 8:8.CrossRefGoogle Scholar
  81. Robins, R.J., Parr, A.J., Payne, J., Walton, N.J., and Rhodes, M.J.C., 1990, Factors affecting tropane-alkaloid production in a transformed root culture of a Datura Candida X D. aurea hybrid, Planta 18:18.Google Scholar
  82. Robins, R.J., Parr, A.J., Bent, E.G., and Rhodes, M.J.C., 1991, Studies on the biosynthesis of tropane-alkaloids in Datura stramonium L. transformed root cultures. I. The kinetics of alkaloid production and the influence of feeding intermediate metabolites, Planta 183:183.Google Scholar
  83. Rugini, E., 1992, Involvement of polyamines in auxin and Agrobacterium rhizogenes induced rooting of fruit trees in vitro, J. Amer. Soc. Hortic. Sci. 117:117.Google Scholar
  84. Saito, K., Yamazaki, M., Shimomura, K., Yoshimatsu, K., and Murakoshi, T., 1990, Genetic transformation of foxglove (Digitalis purpured) by chimeric foreign genes and production of cardioactive glycosides, Plant Cell Rep. 9:9.CrossRefGoogle Scholar
  85. Saito, K., Yamazaki, M., Kaneko, H., Murakoshi, I., Fukuda, Y., and Van Montagu, M., 1991, Tissue-specific and stress-enhancing expression of the TR promoter for mannopine synthase in transgenic medicinal plants, Planta 184:184.CrossRefGoogle Scholar
  86. Sato, K., Yamazaki, T., Okugawa, E., Yoshihira, K., and Shimomura, K., 1991, Anthraquinone production by transformed root cultures of Rubia tinctorun, Phytochem. 30:30.CrossRefGoogle Scholar
  87. Sauerwein, M., and Shimomura, K., 1991, Alkaloid production in hairy roots of Hyoscyamus albus transformed by Agrobacteriwn rhizogenes, Phytochem. 30:30.Google Scholar
  88. Sauerwein, M., Ishimaru, K., and Shimomura, K., 1991a, Indole alkaloids in hairy roots of Amsonia elliptica, Phytochem. 30:1153.CrossRefGoogle Scholar
  89. Sauerwein, M., Ishimaru, K., and Shimomura, K., 1991b, A piperidone alkaloid from Hyoscyamus albus roots transformed with Agrobacterium rhizogenes, Phytochem. 30:2977.CrossRefGoogle Scholar
  90. Sauerwein, M., Yamazaki, T., and Shimomura, K., 1991c Hernandulcin in hairy root cultures of Lippia dulcis, Plant Cell Rep. 9:579.Google Scholar
  91. Sharp, J.M., and Doran, P.M., 1990, Characteristics of growth and tropane alkaloid synthesis in Atropa belladonna roots transformed by Agrobacterium rhizogenes, J. Biotechnol. 16:171.CrossRefGoogle Scholar
  92. Shimomura, K., Sudo, H., Saga, H., and Kamada, H., 1991, Shikonin production and secretion by hairy root cultures of Lithospermum erythrorhizon, Plant Cell Rep. 10:10.CrossRefGoogle Scholar
  93. Shirsat, A.H., Wilford, N., Evans, I.M., Gatehouse, L.N., and Croy, R.D.N., 1991, Expression of a Brassica napus extensin gene in the vascular system of transgenic tobacco and rape plants, Plant Mol Biol. 17:17.CrossRefGoogle Scholar
  94. Soo, K.K., Ebizuka, Y., Noguchi, H., and Sankawa, U., 1988, Production of secondary metabolites by hairy roots and regenerated plants transformed with Ri plasmids, Chem. Pharm. Bull. 36:36.Google Scholar
  95. Spena, A., Schmlling, T., Koncz, C., and Schell, J.S., 1987, Independent and synergistic activity of rol A, B and C loci in stimulating abnormal growth in plants, EMBO J. 6:6.Google Scholar
  96. Tepfer, D., 1984, Transformation of several species of higher plants by Agrobacterium rhizogenes: sexual transmission of the transformed genotype and phenotype, Cell 37:37.CrossRefGoogle Scholar
  97. Toivonen, L., Balsevich, J., and Kurz, G.W., 1989, Indole alkaloid production by hairy root cultures of Catharanthus roseus, Plant Cell, Tissue Organ Cult. 18:18.Google Scholar
  98. Trypsteen, M., van Lijsebettens, M., van Severen, R., and van Montagu, M., 1991, Agrobacterium rhizogenes-mediated transformation of Echinacea purpurea, Plant Cell Rept. 10:85.CrossRefGoogle Scholar
  99. Valveekens, D., Van Montagu, M., and Van Lijsebettens, M., 1988, Agrobacterium tumefaciens mediated transformation of Arabidopsis thaliana root expiants by using kanamycin selection, Proc. Natl. Acad Sci. (USA) 85:85.CrossRefGoogle Scholar
  100. van der Zaal, E.J., Droog, F.N.J., Boot, C.J.M., Hensgens, L.A.M., Hoge, J.H.C., Schilperoort, R.A., and Libbenga, K.R., 1991, Promoters of auxin-induced genes from tobacco can lead to auxin-inducible and root tip-specific expression, Plant Mol. Biol. 16:16.CrossRefGoogle Scholar
  101. Walton, N.J., Robins, R.J., and Peerless, A.C.J., 1990, Enzymes of N-methylputrescine biosynthesis in relation to hyoscyamine formation in transformed root cultures of Datura stramonium and Atropa belladonna, Planta 182:182.CrossRefGoogle Scholar
  102. Westcott, R., 1988, Thiophene production from Tagetes hairy roots, in: “Manipulating Secondary Metabolism in Culture,” R.J. Robins, and M.J.C Rhodes, eds., Cambridge Univ. Press, Cambridge.Google Scholar
  103. Wightman, F., Schneider, E.A., and Thimann, V.K., 1980, Hormonal factors controlling the initiation and development of lateral roots. II. Effects of exogenous growth factors on lateral root formation in pea roots, Physiol. Plant 49:49.CrossRefGoogle Scholar
  104. Willyams, D., Whiteman, P., Cameron, J., and Chandler, S., 1992, Inter-and intra-family variability for rooting capacity in micropropagated Eucalyptus globulus and Eucalyptus nitens, in: “AFOCEL/ IUFRO Symp. on Mass Production Technology for Genetically Improved Fast Growing Forest Trees,” 1992, Bordeaux.Google Scholar
  105. Wilson, P.D.G., Hilton, M.G., Meehan, P.T.H., Waspe, C.R., and Rhodes, M.J.C., 1990, The cultivation of transformed roots from laboratory to pilot plant, in: “Progress in Plant Cellular and Molecular Biology,” H.J.J. Nijkamp, L.H.W. van der Plas, and J. van Aartrijk, eds., Kluwer Academic Pubs., Dordrecht.Google Scholar
  106. Yamamoto, Y.T., Taylor, C.G., Acedo, G.N., Cheng, C.L., and Conkling, M.A., 1991, Characterization of cis-acting sequences regulating root-specific gene expression in tobacco, Plant Cell 3:3.Google Scholar
  107. Yamazaki, T., Flores, H.E., Shimomura, K., and Yoshihira, K., 1991, Examination of steviol glucosides production by hairy root and shoot cultures of Stevia rebaudiana, J. Nat. Prod. (Lloydia) 54:986.Google Scholar
  108. Yonemitsu, H., Shimomura, K., Satake, M., Mochida, S., Tanaka, M., Endo, T., and Kaji, A., 1990, Lobeline production by hairy root culture of Lobelia inflata L., Plant Cell Rep. 9:307.CrossRefGoogle Scholar
  109. Yoshikawa, T., and Furuya, T., 1987, Saponin production by cultures of Panax ginseng transformed with Agrobacterium rhizogenes, Plant Cell Rep. 6:6.Google Scholar

Copyright information

© Springer Science+Business Media New York 1994

Authors and Affiliations

  • John D. Hamill
    • 1
  • Stephen F. Chandler
    • 2
  1. 1.Department of Genetics and Developmental BiologyMonash UniversityClayton, MelbourneAustralia
  2. 2.Calgene Pacific Pty LtdCollingwood, MelbourneAustralia

Personalised recommendations