The Effects of rol Genes of Agrobacterium rhizogenes on Morphogenesis and Secondary Metabolite Accumulation in Medicinal Plants

  • Sayantika Sarkar
  • Ipshita Ghosh
  • Dipasree Roychowdhury
  • Sumita JhaEmail author


Induction of hairy roots by Agrobacterium rhizogenes and regeneration of Ri-transformed plants from such transgenic roots are reported in a large number of taxonomically diverse plant species. Ri-transformed cultures (roots/calli/plants) have altered characteristics of their own compared to non-transformed ones. Four rol genes (rolA, rolB, rolC, rolD) of T-DNA of Ri-plasmid are known to be responsible for these phenomena. However, few attempts have been made to elucidate the role of individual rol genes on morphogenic ability. In addition, the effect of wild-type A. rhizogenes on the production of secondary metabolites is well studied in wide number of plant species. The popularity of this research has never declined through time which explains its immense value and provides a hope for a promising future. Based on such studies, several reviews have been written from time to time, explaining the ‘rol effect’ on secondary metabolite accumulation in medicinal plants and to discuss the advances in this field of research. However, investigations dealing with the effect of individual rol genes are comparatively less and need further attention. Therefore, in this chapter, we have discussed in detail the effects of each of the four rol genes individually or in combination on in vitro morphogenesis and secondary metabolite accumulation in medicinal plants.


Agrobacterium rhizogenes Medicinal plants Morphogenesis rol genes Secondary metabolites 



SJ is thankful to the National Academy of Sciences (NASI, Allahabad, India), for award of Platinum Jubilee Senior Scientist Fellowship and providing the financial support to continue the research.


  1. Alpizar, E., Dechamp, E., Lapeyre-Montes, F., et al. (2008). Agrobacterium rhizogenes-transformed roots of coffee (Coffea arabica): Conditions for long-term proliferation, and morphological and molecular characterization. Annals of Botany, 101(7), 929–940.PubMedPubMedCentralCrossRefGoogle Scholar
  2. Altamura, M. M., Capitani, F., Gazza, L., et al. (1994). The plant oncogene rolB stimulates the formation of flower and root meristemoids in tobacco thin cell layers. The New Phytologist, 126(2), 283–293.CrossRefGoogle Scholar
  3. Amanullah, B. M., Rizvi, Z. F., & Zia, M. (2016). Production of artemisinin and its derivatives in hairy roots of Artemisia dubia induced by rolA gene transformation. Pakistan Journal of Botany, 48(2), 699–706.Google Scholar
  4. Amselem, J., & Tepfer, M. (1992). Molecular basis of novel root phenotypes induced by Agrobacterium rhizogenes A4 on cucumber. Plant Molecular Biology, 19(3), 421–432.PubMedCrossRefGoogle Scholar
  5. Aoki, T., Matsumoto, H., Asako, Y., Matsunaga, Y., et al. (1997). Variation of alkaloid productivity among several clones of hairy roots and regenerated plants of Atropa belladonna transformed with Agrobacterium rhizogenes 15834. Plant Cell Reports, 16, 282–286.Google Scholar
  6. Arshad, W., Haq, I. U., Waheed, M. T., et al. (2014). Agrobacterium-mediated transformation of tomato with rolB gene results in enhancement of fruit quality and foliar resistance against fungal pathogens. PLoS One, 9(5), e96979. Scholar
  7. Bandyopadhyay, M., Jha, S., & Tepfer, D. (2007). Changes in morphological phenotypes and withanolide composition of Ri-transformed roots of Withania somnifera. Plant Cell Reports, 26(5), 599–609.PubMedCrossRefGoogle Scholar
  8. Basu, A., & Jha, S. (2014). Genetic transformation of Digitalis purpurea L. by Agrobacterium rhizogenes. Journal of the Botanical Society of Bengal, 68, 89–93.Google Scholar
  9. Basu, A., Joshi, R. K., & Jha, S. (2015). Genetic transformation of Plumbago zeylanica with Agrobacterium rhizogenes strain LBA 9402 and characterization of transformed root lines. Plant Tissue Culture Biotechnology, 25, 21–35.CrossRefGoogle Scholar
  10. Basu, A., Roychowdhury, D., Joshi, R. K., et al. (2017). Effects of cryptogein gene on growth, phenotype and secondary metabolite accumulation in co-transformed roots and plants of Tylophora indica. Acta Physiologiae Plantarum, 39(1), 3.CrossRefGoogle Scholar
  11. Batra, J., Dutta, A., Singh, D., et al. (2004). Growth and terpenoid indole alkaloid production in Catharanthus roseus hairy root clones in relation to left- and right-termini linked Ri T-DNA gene integration. Plant Cell Reports, 23(3), 148–154.PubMedCrossRefGoogle Scholar
  12. Bell, R. L., Scorza, R., Srinivasan, C., et al. (1999). Transformation of “Beurre Bosc” pear with the rolC gene. Journal of the American Society for Horticultural Science, 124(6), 570–574.Google Scholar
  13. Bettini, P., Michelotti, S., Bindi, D., et al. (2003). Pleiotropic effect of the insertion of the Agrobacterium rhizogenes rolD gene in tomato (Lycopersicum esculentum Mill.). Theoretical and Applied Genetics, 107(5), 831–836.PubMedCrossRefGoogle Scholar
  14. Bettini, P., Baraldi, R., Rapparini, F., et al. (2010). The insertion of the Agrobacterium rhizogenes rolC gene in tomato (Solanum lycopersicum L.) affects plant architecture and endogenous auxin and abscisic acid levels. Scientia Horticulturae, 123(3), 323–328.CrossRefGoogle Scholar
  15. Bettini, P. P., Marvasi, M., Fani, F., et al. (2016a). Agrobacterium rhizogenes rolB gene affects photosynthesis and chlorophyll content in transgenic tomato (Solanum lycopersicum L.) plants. Journal of Plant Physiology, 204, 27–35.PubMedCrossRefGoogle Scholar
  16. Bettini, P. P., Santangelo, E., Baraldi, R., et al. (2016b). Agrobacterium rhizogenes rolA gene promotes tolerance to Fusarium oxysporum f. sp. lycopersiciin transgenic tomato plants (Solanum lycopersicum L.). Journal of Plant Biochemistry and Biotechnology, 25(3), 225–233.CrossRefGoogle Scholar
  17. Bonhomme, V., Laurain-Mattar, D., & Fliniaux, M. A. (2000). Effects of the rolC gene on hairy root: Induction development and tropane alkaloid production by Atropa belladonna. Journal of Natural Products, 63(9), 1249–1252.PubMedCrossRefGoogle Scholar
  18. Bourgaud, F., Gravot, A., Milesi, S., et al. (2001). Production of plant secondary metabolites: A historical perspective. Plant Science, 161(5), 839–851.CrossRefGoogle Scholar
  19. Brillanceau, M. H., David, C., & Tempé, J. (1989). Genetic transformation of Catharanthus roseus G. Don by Agrobacterium rhizogenes. Plant Cell Reports, 8, 63–66.PubMedCrossRefGoogle Scholar
  20. Bulgakov, V. P. (2008). Functions of rol genes in plant secondary metabolism. Biotechnology Advances, 26(4), 318–324.PubMedCrossRefGoogle Scholar
  21. Bulgakov, V. P., Khodakovskaya, M. V., Labetskaya, N. V., et al. (1998). The impact of plant rolC oncogene on ginsenoside production by ginseng hairy root cultures. Phytochemistry, 49(7), 1929–1934.CrossRefGoogle Scholar
  22. Bulgakov, V. P., Tchernoded, G. K., Mischenko, N. P., et al. (2002). Effect of salicylic acid, methyl jasmonate, ethephon and cantharidin on anthraquinone production by Rubia cordifolia callus cultures transformed with the rolB and rolC genes. Journal of Biotechnology, 97(3), 213–221.PubMedCrossRefGoogle Scholar
  23. Bulgakov, V. P., Veselova, M. V., Tchernoded, G. K., et al. (2005). Inhibitory effect of the Agrobacterium rhizogenes rolC gene on rabdosiin and rosmarinic acid production in Eritrichium sericeum and Lithospermum erythrorhizon transformed cell cultures. Planta, 221(4), 471–478.PubMedCrossRefGoogle Scholar
  24. Bulgakov, V. P., Shkryl, Y. N., Veremeichik, G. N., et al. (2011). Application of Agrobacterium rol genes in plant biotechnology: A natural phenomenon of secondary metabolism regulation. In M. Alvarez (Ed.), Genetic transformation (pp. 261–271). Rijeka: InTech.Google Scholar
  25. Bulgakov, V. P., Shkryl, Y. N., Veremeichik, G. N., et al. (2013). Recent advances in the understanding of Agrobacterium rhizogenes-derived genes and their effects on stress resistance and plant metabolism. In P. Doran (Ed.), Biotechnology of hairy root systems. Advances in biochemical engineering/biotechnology (Vol. 134, pp. 1–22). Berlin/Heidelberg: Springer.CrossRefGoogle Scholar
  26. Capone, I., Spanò, L., Cardarelli, M., et al. (1989). Induction and growth properties of carrot roots with different complements of Agrobacterium rhizogenes T-DNA. Plant Molecular Biology, 13(1), 43–52.PubMedCrossRefGoogle Scholar
  27. Cardarelli, M., Mariotti, D., Pomponi, M., et al. (1987). Agrobacterium rhizogenes T-DNA genes capable of inducing hairy root phenotype. Molecular & General Genetics, 209(3), 475–480.CrossRefGoogle Scholar
  28. Carmi, N., Salts, Y., Dedicova, B., et al. (2003). Induction of parthenocarpy in tomato via specific expression of the rolB gene in the ovary. Planta, 217(5), 726–735.PubMedCrossRefGoogle Scholar
  29. Carneiro, M., & Vilaine, F. (1993). Differential expression of the rolA plant oncogene and its effect on tobacco development. The Plant Journal, 3(6), 785–792.PubMedCrossRefGoogle Scholar
  30. Chandra, S. (2012). Natural plant genetic engineer Agrobacterium rhizogenes: Role of T-DNA in plant secondary metabolism. Biotechnology Letters, 34(3), 407–415.PubMedCrossRefPubMedCentralGoogle Scholar
  31. Chaudhuri, K. N., Ghosh, B., Tepfer, D., et al. (2005). Genetic transformation of Tylophora indica with Agrobacterium rhizogenes A4: Growth and tylophorine productivity in different transformed root clones. Plant Cell Reports, 24, 25–35.PubMedCrossRefPubMedCentralGoogle Scholar
  32. Chaudhuri, K. N., Ghosh, B., Tepfer, D., et al. (2006). Spontaneous plant regeneration in transformed roots and calli from Tylophora indica: Changes in morphological phenotype and tylophorine accumulation associated with transformation by Agrobacterium rhizogenes. Plant Cell Reports, 25(10), 1059–1066.PubMedCrossRefPubMedCentralGoogle Scholar
  33. Chaudhuri, K. N., Das, S., Bandyopadhyay, M., et al. (2009). Transgenic mimicry of pathogen attack stimulates growth and secondary metabolite accumulation. Transgenic Research, 18(1), 121–134.PubMedCrossRefPubMedCentralGoogle Scholar
  34. Chilton, M. D., Tepfer, D. A., Petit, A., et al. (1982). Agrobacterium rhizogenes inserts T-DNA into the genomes of the host-plant root cells. Nature, 295, 432–434.CrossRefGoogle Scholar
  35. Choi, P. S., Kim, Y. D., Choi, K. M., et al. (2004). Plant regeneration from hairy-root cultures transformed by infection with Agrobacterium rhizogenes in Catharanthus roseus. Plant Cell Reports, 22, 828–831.PubMedCrossRefPubMedCentralGoogle Scholar
  36. Christey, M. C. (1997). Transgenic crop plants using Agrobacterium rhizogenes mediated transformation. In P. M. Doran (Ed.), Hairy roots: Culture and applications (pp. 99–111). Amsterdam: Harwood Academic Publishers.Google Scholar
  37. Christey, M. C. (2001). Use of Ri-mediated transformation for production of transgenic plants. In Vitro Cellular & Developmental Biology. Plant, 37(6), 687–700.CrossRefGoogle Scholar
  38. Costantino, P., Capone, I., Cardarelli, M., et al. (1994). Bacterial plant oncogenes: The rol genes’ saga. Genetica, 94(2), 203–211.PubMedCrossRefPubMedCentralGoogle Scholar
  39. Das, S., Jha, T. B., & Jha, S. (1996). Organogenesis and regeneration from pigmented callus in Camellia sinensis (L.) O. Kuntze cv. Nandadevi, an elite Darjeeling tea clone. Plant Science, 121, 207–212.CrossRefGoogle Scholar
  40. de Almeida, M., Graner, E. M., Brondani, G. E., et al. (2015). Plant morphogenesis: Theorical bases. Advances in Forestry Science, 2, 13–22.Google Scholar
  41. Dehio, C., Grossmann, K., Schell, J., et al. (1993). Phenotype and hormonal status of transgenic tobacco plants overexpressing the rolA gene of Agrobacterium rhizogenes T-DNA. Plant Molecular Biology, 23(6), 1199–1210.PubMedCrossRefGoogle Scholar
  42. Dilshad, E., Cusido, R. M., Estrada, K. R., et al. (2015a). Genetic transformation of Artemisia carvifolia Buch with rol genes enhances artemisinin accumulation. PLoS One, 10, e0140266.PubMedPubMedCentralCrossRefGoogle Scholar
  43. Dilshad, E., Cusido, R. M., Palazon, J., et al. (2015b). Enhanced artemisinin yield by expression of rol genes in Artemisia annua. Malaria Journal, 14(1), 424.PubMedPubMedCentralCrossRefGoogle Scholar
  44. Dilshad, E., Ismail, H., Cusido, R. M., et al. (2016). Rol genes enhance the biosynthesis of antioxidants in Artemisia carvifolia Buch. BMC Plant Biology, 16(1), 125.PubMedPubMedCentralCrossRefGoogle Scholar
  45. Dubrovina, A. S., Manyakhin, A. Y., Zhuravlev, Y. N., et al. (2010). Resveratrol content and expression of phenylalanine ammonia-lyase and stilbene synthase genes in rolC transgenic cell cultures of Vitis amurensis. Applied Microbiology and Biotechnology, 88(3), 727–736.PubMedCrossRefPubMedCentralGoogle Scholar
  46. Falasca, G., Altamura, M. M., D’Angeli, S., et al. (2010). The rolD oncogene promotes axillary bud and adventitious root meristems in Arabidopsis. Plant Physiology and Biochemistry, 48(9), 797–804.PubMedCrossRefPubMedCentralGoogle Scholar
  47. Fladung, M. (1990). Transformation of diploid and tetraploid potato clones with the rolC gene of Agrobacterium rhizogenes and characterization of transgenic plants. Plant Breeding, 104(4), 295–304.CrossRefGoogle Scholar
  48. 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/Heidelberg: Springer.CrossRefGoogle Scholar
  49. Gangopadhyay, M., Chakraborty, D., Bhattacharyya, S., et al. (2010). Regeneration of transformed plants from hairy roots of Plumbago indica. Plant Cell Tissue and Organ Culture, 102, 109–114.CrossRefGoogle Scholar
  50. Gorpenchenko, T. Y., Kiselev, K. V., Bulgakov, V. P., et al. (2006). The Agrobacterium rhizogenes rolC-gene-induced somatic embryogenesis and shoot organogenesis in Panax ginseng transformed calluses. Planta, 223(3), 457–467.PubMedCrossRefGoogle Scholar
  51. Grishchenko, O. V., Kiselev, K. V., Tchernoded, G. K., et al. (2013). The influence of the rolC gene on isoflavonoid production in callus cultures of Maackia amurensis. Plant Cell Tissue and Organ Culture, 113(3), 429–435.CrossRefGoogle Scholar
  52. Grishchenko, O. V., Kiselev, K. V., Tchernoded, G. K., et al. (2016). RolB gene-induced production of isoflavonoids in transformed Maackia amurensis cells. Applied Microbiology and Biotechnology, 100(17), 7479–7489.PubMedCrossRefGoogle Scholar
  53. Guillon, S., Trémouillaux-Guiller, J., Pati, P. K., et al. (2006). Hairy root research: Recent scenario and exciting prospects. Current Opinion in Plant Biology, 9(3), 341–346.PubMedCrossRefGoogle Scholar
  54. Häkkinen, S. T., Moyano, E., Cusidó, R. M., et al. (2016). Exploring the metabolic stability of engineered hairy roots after 16 years maintenance. Frontiers in Plant Science, 7, 1486. Scholar
  55. Halder, M., & Jha, S. (2016). Enhanced trans-resveratrol production in genetically transformed root cultures of Peanut (Arachis hypogaea L.). Plant Cell Tissue and Organ Culture, 124(3), 555–572.CrossRefGoogle Scholar
  56. Hamill, J. D., Parr, A. J., Rhodes, M. J., et al. (1987). New routes to plant secondary products. Nature Biotechnology, 5(8), 800–804.CrossRefGoogle Scholar
  57. Hicks, G. S. (1994). Shoot induction and organogenesis in vitro: A developmental perspective. In Vitro Cellular & Developmental Biology, 30(1), 10–15.CrossRefGoogle Scholar
  58. Holefors, A., Xue, Z. T., Welander, M., et al. (1998). Transformation of the apple rootstock M26 with the rolA gene and its influence on growth. Plant Science, 136(1), 69–78.CrossRefGoogle Scholar
  59. Ikeuchi, M., Ogawa, Y., Iwase, A., et al. (2016). Plant regeneration: Cellular origins and molecular mechanisms. Development, 143, 1442–1451.PubMedCrossRefPubMedCentralGoogle Scholar
  60. Ionkova, I., & Fuss, E. (2009). Influence of different strains of Agrobacterium rhizogenes on induction of hairy roots and lignan production in Linum tauricum ssp. tauricum. Pharmacognosy Magazine, 5(17), 14.Google Scholar
  61. Ismail, H., Dilshad, E., Waheed, M. T., et al. (2016). Transformation of Lactuca sativa L. with rolC gene results in increased antioxidant potential and enhanced analgesic, anti-inflammatory and antidepressant activities in vivo. 3 Biotechnology, 6(2), 215.Google Scholar
  62. Jouanin, L., Guerche, D., Pamboukdjian, N., et al. (1987). Structure of T-DNA in plants regenerated from roots transformed by Agrobacterium rhizogenes strain A4. Molecular & General Genetics, 206(3), 387–392.CrossRefGoogle Scholar
  63. Kamada, H., Okamura, N., Satake, M., et al. (1986). Alkaloid production by hairy root cultures in Atropa belladonna. Plant Cell Reports, 5(4), 239–242.PubMedCrossRefGoogle Scholar
  64. Kaneyoshi, J., & Kobayashi, S. (1999). Characteristics of transgenic trifoliate orange (Poncirus trifoliate Raf.) possessing the rolC gene of Agrobacterium rhizogenes Ri plasmid. Journal of the Japanese Society for Horticultural Science, 68(4), 734–738.CrossRefGoogle Scholar
  65. Karuppusamy, S. (2009). A review on trends in production of secondary metabolites from higher plants by in vitro tissue, organ and cell cultures. Journal of Medicinal Plant Research: Planta Medica, 3(13), 1222–1239.Google Scholar
  66. Khalili, S., Moieni, A., & Abdoli, M. (2015). Influence of different strains of Agrobacterium rhizogenes, culture medium, age and type of explant on hairy root induction in Echinacea angustifolia. IJGPB, 3(1), 56–49.Google Scholar
  67. Kim, Y. S., & Soh, W. Y. (1996). Amyloplast distribution in hairy roots induced by infection with Agrobacterium rhizogenes. Biological Sciences in Space, 10(2), 102–104.PubMedCrossRefGoogle Scholar
  68. Kim, J. S., Lee, S. Y., & Park, S. U. (2008). Resveratol production in hairy root culture of peanut, Arachis hypogaea L. transformed with different Agrobacterium rhizogenes strains. African Journal of Biotechnology, 7, 3788–3790.Google Scholar
  69. Kiselev, K. V., Dubrovina, A. S., Veselova, M. V., et al. (2007). The rolB gene-induced overproduction of resveratrol in Vitis amurensis transformed cells. Journal of Biotechnology, 128(3), 681–692.PubMedCrossRefGoogle Scholar
  70. Kodahl, N., Müller, R., & Lütken, H. (2016). The Agrobacterium rhizogenes oncogenes rolB and ORF13 increase formation of generative shoots and induce dwarfism in Arabidopsis thaliana (L.) Heynh. Plant Science, 252, 22–29.PubMedCrossRefGoogle Scholar
  71. Koltunow, A. M., Johnson, S. D., Lynch, M., et al. (2001). Expression of rolB in apomictic Hieracium piloselloides Vill. Causes ectopic meristems in planta and changes in ovule formation, where apomixis initiates at higher frequency. Planta, 214(2), 196–205.PubMedCrossRefGoogle Scholar
  72. Koshita, Y., Nakamura, Y., Kobayashi, S., et al. (2002). Introduction of the rolC gene into the genome of the Japanese persimmon causes dwarfism. Journal of the Japanese Society for Horticultural Science, 71(4), 529–531.CrossRefGoogle Scholar
  73. Kubo, T., Tsuro, M., Tsukimori, A., et al. (2006). Morphological and physiological changes in transgenic Chrysanthemum morifolium Ramat. ‘Ogura-nishiki’ with rolC. Journal of the Japanese Society for Horticultural Science, 75, 312–317.CrossRefGoogle Scholar
  74. Kumar, N., & Reddy, M. P. (2011). In vitro plant propagation: A review. Journal of Forest Science, 27, 61–72.Google Scholar
  75. Kurioka, Y., Suzuki, Y., Kamada, H., et al. (1992). Promotion of flowering and morphological alterations in Atropa belladonna transformed with a CaMV 35S-rolC chimeric gene of the Ri plasmid. Plant Cell Reports, 12(1), 1–6.PubMedCrossRefGoogle Scholar
  76. Landi, L., Capocasa, F., & Costantini, E. (2009). ROLC strawberry plant adaptability, productivity, and tolerance to soil-borne disease and mycorrhizal interactions. Transgenic Research, 18(6), 933–942.PubMedCrossRefGoogle Scholar
  77. Lee, M. H., Yoon, E. S., Jeong, J. H., et al. (2004). Agrobacterium rhizogenes-mediated transformation of Taraxacum platycarpum and changes of morphological characters. Plant Cell Reports, 22, 822–827.PubMedCrossRefGoogle Scholar
  78. Majumdar, S., Garai, S., & Jha, S. (2011). Genetic transformation of Bacopa monnieri by wild type strains of Agrobacterium rhizogenes stimulates production of bacopa saponins in transformed calli and plants. Plant Cell Reports, 30, 941–954.PubMedCrossRefGoogle Scholar
  79. Mano, Y., Ohkawa, H., & Yamada, Y. (1989). Production of tropane alkaloids by hairy root cultures of Duboisia leichhardtii transformed by Agrobacterium rhizogenes. Plant Science, 59(2), 191–201.CrossRefGoogle Scholar
  80. Matveeva, T. V., Sokornova, S. V., & Lutova, L. A. (2015). Influence of Agrobacterium oncogenes on secondary metabolism of plants. Phytochemistry Reviews, 14(3), 541–554.CrossRefGoogle Scholar
  81. Mauro, M. L., Trovato, M., De Paolis, A., et al. (1996). The plant oncogene rolD stimulates flowering in transgenic tobacco plants. Developmental Biology, 180(2), 693–700.PubMedCrossRefGoogle Scholar
  82. Mitra, A., Mukherjee, C., & Sircar, D. (2017). Metabolic phytochemistry-based approaches for studying secondary metabolism using transformed root culture systems. In S. Jha (Ed.), Transgenesis and secondary metabolism, Reference series in phytochemistry (pp. 513–537). Cham: Springer.CrossRefGoogle Scholar
  83. Nilsson, O., & Olsson, O. (1997). Getting to the root: The role of the Agrobacterium rhizogenes rol genes in the formation of hairy roots. Physiologia Plantarum, 100(3), 463–473.CrossRefGoogle Scholar
  84. Odegaard, E., Nielsen, K. M., Beisvag, T., et al. (1997). Agravitropic behaviour of roots of rapeseed (Brassica napus L.) transformed by Agrobacterium rhizogenes. Journal of Gravitational Physiology, 4(3), 5–14.PubMedGoogle Scholar
  85. Ohara, A., Akasaka, Y., Daimon, H., et al. (2000). Plant regeneration from hairy roots induced by infection with Agrobacterium rhizogenes in Crotalaria juncea L. Plant Cell Reports, 19, 563–568.CrossRefGoogle Scholar
  86. Oono, Y., Suzuki, T., Toki, S., et al. (1993). Effects of the over-expression of the rolC gene on leaf development in transgenic periclinal chimeric plants. Plant & Cell Physiology, 34(5), 745–752.CrossRefGoogle Scholar
  87. Palazón, J., Cusidó, R. M., Roig, C., et al. (1997). Effect of rol genes from Agrobacterium rhizogenes TL-DNA on nicotine production in tobacco root cultures. Plant Physiology and Biochemistry, 35(2), 155–162.Google Scholar
  88. Palazón, J., Cusidó, R. M., Roig, C., et al. (1998). Expression of the rolC gene and nicotine production in transgenic roots and their regenerated plants. Plant Cell Reports, 17(5), 384–390.CrossRefGoogle Scholar
  89. Park, S. U., & Facchini, P. J. (2000). Agrobacterium rhizogenes -mediated transformation of opium poppy, Papaver somniferum L., and California poppy, Eschscholzia californica Cham., root cultures. Journal of Experimental Botany, 51(347), 1005–1016.PubMedCrossRefGoogle Scholar
  90. Parr, A. J. (2017). Secondary products from plant cell cultures–early experiences with Agrobacterium rhizogenes-transformed hairy roots. In S. Jha (Ed.), Transgenesis and secondary metabolism, Reference series in phytochemistry (pp. 1–13). Cham: Springer.Google Scholar
  91. Paul, P., Sarkar, S., & Jha, S. (2015). Effects associated with insertion of cryptogein gene utilizing Ri and Ti plasmids on morphology and secondary metabolites are stable in Bacopa monnieri-transformed plants grown in vitro and ex vitro. Plant Biotechnology Reports, 9(4), 231–245.CrossRefGoogle Scholar
  92. Peres, L. E. P., Morgante, P. G., Vecchi, C., et al. (2001). Shoot regeneration capacity from roots and transgenic hairy roots of tomato cultivars and wild related species. Plant Cell Tissue and Organ Culture, 65(1), 37–44.CrossRefGoogle Scholar
  93. Pistelli, L., Giovannini, A., Ruffoni, B., et al. (2010). Hairy root cultures for secondary metabolites production. In M. T. Giardi, G. Rea, & B. Berra (Eds.), Bio-farms for nutraceuticals, Advances in experimental medicine and biology (Vol. 698, pp. 167–184). Boston: Springer.CrossRefGoogle Scholar
  94. Rao, S. R., & Ravishankar, G. A. (2002). Plant cell cultures: Chemical factories of secondary metabolites. Biotechnology Advances, 20(2), 101–153.PubMedCrossRefGoogle Scholar
  95. Ray, S., & Jha, S. (1999). Withanolide synthesis in cultures of Withania somnifera transformed with Agrobacterium tumefaciens. Plant Science, 146(1), 1–7.CrossRefGoogle Scholar
  96. Ray, S., Ghosh, B., Sen, S., et al. (1996). Withanolide production by root cultures of Withania somnifera transformed with Agrobacterium rhizogenes. Planta Medica, 62(06), 571–573.PubMedCrossRefGoogle Scholar
  97. Ray, S., Majumder, A., Bandyopadhyay, M., et al. (2014). Genetic transformation of sarpagandha (Rauvolfia serpentina) with Agrobacterium rhizogenes for identification of high alkaloid yielding lines. Acta Physiologiae Plantarum, 36(6), 1599–1605.CrossRefGoogle Scholar
  98. Robins, R. J., Parr, A. J., & Walton, N. J. (1991). Studies on the biosynthesis of tropane alkaloids in Datura stramonium L. transformed root cultures. Planta, 183(2), 196–201.PubMedCrossRefGoogle Scholar
  99. Roychowdhury, D., Ghosh, B., Chaubey, B., et al. (2013a). Genetic and morphological stability of six-year-old transgenic Tylophora indica plants. The Nucleus, 56(2), 81–89.CrossRefGoogle Scholar
  100. Roychowdhury, D., Majumder, A., & Jha, S. (2013b). Agrobacterium rhizogenes-mediated transformation in medicinal plants: Prospects and challenges. In S. Chandra, H. Lata, & A. Varma (Eds.), Biotechnology for medicinal plants: Micropropagation and improvement (pp. 29–68). Berlin/Heidelberg: Springer.CrossRefGoogle Scholar
  101. Roychowdhury, D., Basu, A., & Jha, S. (2015a). Morphological and molecular variation in Ri-transformed root lines are stable in long term cultures of Tylophora indica. Plant Growth Regulation, 75(2), 443–453.CrossRefGoogle Scholar
  102. Roychowdhury, D., Chaubey, B., & Jha, S. (2015b). The fate of integrated Ri T-DNA rol genes during regeneration via somatic embryogenesis in Tylophora indica. Journal of Botany, 2015, 1–16.CrossRefGoogle Scholar
  103. Roychowdhury, D., Halder, M., & Jha, S. (2017). Agrobacterium rhizogenes-mediated transformation in medicinal plants: Genetic stability in long-term culture. In S. Jha (Ed.), Transgenesis and secondary metabolism, Reference series in phytochemistry (pp. 323–345). Cham: Springer.CrossRefGoogle Scholar
  104. Rugini, E., Pellegrineschi, A., Mencuccini, M., et al. (1991). Increase of rooting ability in the woody species kiwi (Actinidia deliciosa A. Chev.) by transformation with Agrobacterium rhizogenes rol genes. Plant Cell Reports, 10(6–7), 291–295.PubMedGoogle Scholar
  105. Sarkar, S., & Jha, S. (2017). Morpho-histological characterization and direct shoot organogenesis in two types of explants from Bacopa monnieri on unsupplemented basal medium. Plant Cell Tissue and Organ culture, 130(2), 435–441.CrossRefGoogle Scholar
  106. Satheeshkumar, K., Jose, B., Soniya, E. V., et al. (2009). Isolation of morphovariants through plant regeneration in Agrobacterium rhizogenes induced hairy root cultures of Plumbago rosea L. Indian Journal of Biotechnology, 8(4), 435–441.Google Scholar
  107. Schmülling, T., Schell, J., & Spena, A. (1988). Single genes from Agrobacterium rhizogenes influence plant development. The EMBO Journal, 7(9), 2621–2629.PubMedPubMedCentralCrossRefGoogle Scholar
  108. Sedira, M., Holefors, A., & Welander, M. (2001). Protocol for transformation of the apple rootstock Jork 9 with the rolB gene and its influence on rooting. Plant Cell Reports, 20(6), 517–524.CrossRefGoogle Scholar
  109. Sharma, P., Padh, H., & Shrivastava, N. (2013). Hairy root cultures: A suitable biological system for studying secondary metabolic pathways in plants. Engineering in Life Sciences, 13(1), 62–75.CrossRefGoogle Scholar
  110. Shkryl, Y. N., Veremeichik, G. N., Bulgakov, V. P., et al. (2007). Individual and combined effects of the rolA, B and C genes on anthraquinone production in Rubia cordifolia transformed calli. Biotechnology and Bioengineering, 100(1), 118–125.CrossRefGoogle Scholar
  111. Simic, S. G., Tusevski, O., Maury, S., et al. (2014). Effects of polysaccharide elicitors on secondary metabolite production and antioxidant response in Hypericum perforatum L. shoot cultures. The Scientific World Journal.
  112. Sinkar, P. V., Pythoud, F., White, F. F., et al. (1988). rolA locus of the Ri plasmid directs developmental abnormalities in transgenic tobacco plants. Genes and Development, 2(6), 688–697.PubMedCrossRefGoogle Scholar
  113. Sivanandhan, G., Selvaraj, N., Ganapathi, A., et al. (2016). Elicitation approaches for withanolide production in hairy root culture of Withania somnifera (L.) Dunal. In A. Fett-Neto (Ed.), Biotechnology of plant secondary metabolism, Methods in molecular biology (Vol. 1405, pp. 1–18). New York: Humana Press.CrossRefGoogle Scholar
  114. Skoog, F., & Miller, C. O. (1957). Chemical regulation of growth and organ formation in plant tissue cultured in vitro. Symposia of the Society for Experimental Biology, 11, 118–131.PubMedGoogle Scholar
  115. Slightom, J. L., Durand-Tardif, M., Jouanin, L., et al. (1986). Nucleotide sequence analysis of TL-DNA of Agrobacterium rhizogenes agropine type plasmid. Identification of open reading frames. The Journal of Biological Chemistry, 261, 108–121.PubMedGoogle Scholar
  116. Spena, A., Schmülling, T., Koncz, C., et al. (1987). Independent and synergistic activity of rolA, B and C loci in stimulating abnormal growth in plants. The EMBO Journal, 6(13), 3891–3899.PubMedPubMedCentralCrossRefGoogle Scholar
  117. Srivastava, S., & Srivastava, A. K. (2007). Hairy root culture for mass-production of high-value secondary metabolites. Critical Reviews in Biotechnology, 27(1), 29–43.PubMedCrossRefGoogle Scholar
  118. Taneja, J., Jaggi, M., Wankhede, D. P., et al. (2010). Effect of loss of T-DNA genes on MIA biosynthetic pathway gene regulation and alkaloid accumulation in Catharanthus roseus hairy roots. Plant Cell Reports, 29(10), 1119–1129.PubMedCrossRefGoogle Scholar
  119. Tepfer, D. (1984). Genetic transformation of several species of higher plants by Agrobacterium rhizogenes: Phenotypic consequences and sexual transmission of the transformed genotype and phenotype. Cell, 37, 959–967.PubMedCrossRefGoogle Scholar
  120. Tepfer, D. (1990). Genetic transformation using Agrobacterium rhizogenes. Physiologia Plantarum, 79(1), 140–146.CrossRefGoogle Scholar
  121. Tepfer, D. (2017). DNA transfer to plants by Agrobacterium rhizogenes: A model for genetic communication between species and biospheres. In S. Jha (Ed.), Transgenesis and secondary metabolism, Reference series in phytochemistry (pp. 3–43). Cham: Springer.CrossRefGoogle Scholar
  122. Tepfer, D., & Tempé, J. (1981). Production of d’agropine par des racines transformes sous I’action d’Agrobacterium rhizogenes souche A4. Comptes Rendus Académie des Sciences, 292, 153–156.Google Scholar
  123. Thwe, A., Valan Arasu, M., Li, X., et al. (2016). Effect of different Agrobacterium rhizogenes strains on hairy root induction and phenylpropanoid biosynthesis in tartary buckwheat (Fagopyrum tataricum Gaertn). Frontiers in Microbiology, 7, 318.PubMedPubMedCentralCrossRefGoogle Scholar
  124. Toivonen, L. (1993). Utilization of hairy root cultures for production of secondary metabolites. Biotechnology Progress, 9(1), 12–20.CrossRefGoogle Scholar
  125. Trovato, M., Maras, B., Linhares, F., et al. (2001). The plant oncogene rolD encodes a functional ornithine cyclodeaminase. Proceedings of the National Academy of Sciences of the United States of America, 98(23), 13449–13453.PubMedPubMedCentralCrossRefGoogle Scholar
  126. Trulson, A. J., Simpson, R. B., & Shahin, E. A. (1986). Transformation of cucumber (Cucumis sativus L.) plants with Agrobacterium rhizogenes. Theoretical and Applied Genetics, 73, 11–15.PubMedCrossRefGoogle Scholar
  127. van Altvorst, A. C., Bino, R. J., van Dijk, A. J., et al. (1992). Effects of the introduction of Agrobacterium rhizogenes rol genes on tomato plant and flower development. Plant Science, 83(1), 77–85.CrossRefGoogle Scholar
  128. Vanhala, L., Hiltunen, R., & Oksman-Caldentey, K. M. (1995). Virulence of different Agrobacterium strains on hairy root formation of Hyoscyamus muticus. Plant Cell Reports, 14(4), 236–240.PubMedCrossRefGoogle Scholar
  129. Vereshchagina, Y. V., Bulgakov, V. P., Grigorchuk, V. P., et al. (2014). The rolC gene increases caffeoylquinic acid production in transformed artichoke cells. Applied Microbiology and Biotechnology, 98(18), 7773–7780.PubMedCrossRefGoogle Scholar
  130. Verpoorte, R., Contin, A., & Memelink, J. (2002). Biotechnology for the production of plant secondary metabolites. Phytochemistry Reviews, 1(1), 13–25.CrossRefGoogle Scholar
  131. Welander, M., Pawlicki, N., Holefors, A., et al. (1998). Genetic transformation of the apple rootstock M26 with the rolB gene and its influence on rooting. Journal of Plant Physiology, 153(3–4), 371–380.CrossRefGoogle Scholar
  132. White, F. F., Taylor, B. H., Huffman, G. A., et al. (1985). Molecular and genetic analysis of the transferred DNA regions of the root-inducing plasmid of Agrobacterium rhizogenes. Journal of Bacteriology, 164, 33–44.PubMedPubMedCentralGoogle Scholar
  133. Yang, D. C., & Choi, Y. E. (2000). Production of transgenic plants via Agrobacterium rhizogenes mediated transformation of Panax ginseng. Plant Cell Reports, 19, 491–496.CrossRefGoogle Scholar
  134. Zhang, Z., Sun, A., Cong, Y., et al. (2006). Agrobacterium-mediated transformation of the apple rootstock Malus micromalus Makino with the RolC gene. In Vitro Cellular & Developmental Biology Plant, 42(6), 491–497.CrossRefGoogle Scholar
  135. Zhu, L. H., Ahlman, A., Li, X. Y., et al. (2001a). Integration of the rolA gene into the genome of the vigorous apple rootstock A2 reduced plant height and shortened internodes. The Journal of Horticultural Science and Biotechnology, 76(6), 758–763.CrossRefGoogle Scholar
  136. Zhu, L. H., Holefors, A., Ahlman, A., et al. (2001b). Transformation of the apple rootstock M.9/29 with the rolB gene and its influence on rooting and growth. Plant Science, 160(3), 433–439.PubMedCrossRefGoogle Scholar
  137. Zhu, L. H., Li, X. Y., Ahlman, A., et al. (2003). The rooting ability of the dwarfing pear rootstock BP10030 (Pyrus communis) was significantly increased by introduction of the rolB gene. Plant Science, 165(4), 829–835.CrossRefGoogle Scholar
  138. Zia, M., Mirza, B., Malik, S. A., et al. (2010). Expression of rol genes in transgenic soybean (Glycine max L.) leads to changes in plant phenotype, leaf morphology, and flowering time. Plant Cell Tissue and Organ Culture, 103(2), 227–236.CrossRefGoogle Scholar
  139. Zuker, A., Tzfira, T., Scovel, G., et al. (2001). rolC-transgenic carnation with improved agronomic traits: Quantitative and qualitative analyses of greenhouse-grown plants. Journal of the American Society for Horticultural Science, 126(1), 13–18.Google Scholar

Copyright information

© Springer Nature Singapore Pte Ltd. 2018

Authors and Affiliations

  • Sayantika Sarkar
    • 1
  • Ipshita Ghosh
    • 1
  • Dipasree Roychowdhury
    • 2
  • Sumita Jha
    • 1
    Email author
  1. 1.Centre of Advanced Study, Department of BotanyUniversity of CalcuttaKolkataIndia
  2. 2.Department of BotanySurendranath CollegeKolkataIndia

Personalised recommendations