Skip to main content
SpringerLink
Log in

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

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

Abstract

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.

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

Access this chapter

Log in via an institution
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

Similar content being viewed by others

References

  • 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.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    CAS  PubMed  Google Scholar 

  • 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. https://doi.org/10.1371/journal.pone.0096979.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Bourgaud, F., Gravot, A., Milesi, S., et al. (2001). Production of plant secondary metabolites: A historical perspective. Plant Science, 161(5), 839–851.

    Article  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Bulgakov, V. P. (2008). Functions of rol genes in plant secondary metabolism. Biotechnology Advances, 26(4), 318–324.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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 

  • 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.

    Chapter  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Chandra, S. (2012). Natural plant genetic engineer Agrobacterium rhizogenes: Role of T-DNA in plant secondary metabolism. Biotechnology Letters, 34(3), 407–415.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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 

  • Christey, M. C. (2001). Use of Ri-mediated transformation for production of transgenic plants. In Vitro Cellular & Developmental Biology. Plant, 37(6), 687–700.

    Article  CAS  Google Scholar 

  • Costantino, P., Capone, I., Cardarelli, M., et al. (1994). Bacterial plant oncogenes: The rol genes’ saga. Genetica, 94(2), 203–211.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  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/Heidelberg: Springer.

    Chapter  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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. https://doi.org/10.3389/fpls.2016.01486.

    Article  PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Hamill, J. D., Parr, A. J., Rhodes, M. J., et al. (1987). New routes to plant secondary products. Nature Biotechnology, 5(8), 800–804.

    Article  CAS  Google Scholar 

  • Hicks, G. S. (1994). Shoot induction and organogenesis in vitro: A developmental perspective. In Vitro Cellular & Developmental Biology, 30(1), 10–15.

    Article  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Ikeuchi, M., Ogawa, Y., Iwase, A., et al. (2016). Plant regeneration: Cellular origins and molecular mechanisms. Development, 143, 1442–1451.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    CAS  Google Scholar 

  • 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 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    CAS  Google Scholar 

  • 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 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Kumar, N., & Reddy, M. P. (2011). In vitro plant propagation: A review. Journal of Forest Science, 27, 61–72.

    Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Chapter  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Chapter  Google Scholar 

  • Rao, S. R., & Ravishankar, G. A. (2002). Plant cell cultures: Chemical factories of secondary metabolites. Biotechnology Advances, 20(2), 101–153.

    Article  PubMed  CAS  Google Scholar 

  • Ray, S., & Jha, S. (1999). Withanolide synthesis in cultures of Withania somnifera transformed with Agrobacterium tumefaciens. Plant Science, 146(1), 1–7.

    Article  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Chapter  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Chapter  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    CAS  Google Scholar 

  • Schmülling, T., Schell, J., & Spena, A. (1988). Single genes from Agrobacterium rhizogenes influence plant development. The EMBO Journal, 7(9), 2621–2629.

    Article  PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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. https://doi.org/10.1155/2014/609649.

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Chapter  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Tepfer, D. (1990). Genetic transformation using Agrobacterium rhizogenes. Physiologia Plantarum, 79(1), 140–146.

    Article  CAS  Google Scholar 

  • 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.

    Chapter  Google Scholar 

  • 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.

    CAS  Google Scholar 

  • 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.

    Article  PubMed  PubMed Central  Google Scholar 

  • Toivonen, L. (1993). Utilization of hairy root cultures for production of secondary metabolites. Biotechnology Progress, 9(1), 12–20.

    Article  CAS  Google Scholar 

  • 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.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Verpoorte, R., Contin, A., & Memelink, J. (2002). Biotechnology for the production of plant secondary metabolites. Phytochemistry Reviews, 1(1), 13–25.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    PubMed  PubMed Central  CAS  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    CAS  Google Scholar 

Download references

Acknowledgements

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.

Author information

Authors and Affiliations

  1. Centre of Advanced Study, Department of Botany, University of Calcutta, Kolkata, West Bengal, India

    Sayantika Sarkar, Ipshita Ghosh & Sumita Jha

  2. Department of Botany, Surendranath College, Kolkata, West Bengal, India

    Dipasree Roychowdhury

Authors
  1. Sayantika Sarkar
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ipshita Ghosh
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Dipasree Roychowdhury
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Sumita Jha
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Sumita Jha .

Editor information

Editors and Affiliations

  1. Department of Biotechnology, Central University of South Bihar, Panchanpur, Gaya, Bihar, India

    Nitish Kumar

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

Sarkar, S., Ghosh, I., Roychowdhury, D., Jha, S. (2018). The Effects of rol Genes of Agrobacterium rhizogenes on Morphogenesis and Secondary Metabolite Accumulation in Medicinal Plants. In: Kumar, N. (eds) Biotechnological Approaches for Medicinal and Aromatic Plants. Springer, Singapore. https://doi.org/10.1007/978-981-13-0535-1_2

Download citation

Publish with us

Policies and ethics

Search

Navigation