Skip to main content
SpringerLink
Log in

Differential Secretion and Accumulation of Terpene Indole Alkaloids in Hairy Roots of Catharanthus roseus Treated with Methyl Jasmonate

  • Research
  • Published:
Molecular Biotechnology Aims and scope Submit manuscript

Abstract

The induction of several secondary metabolites in plants is one of the most commonly observed effects after the external addition of methyl jasmonate (MeJA). After the elicitation of Catharanthus roseus hairy roots with different concentrations of MeJA, changes in the accumulation of alkaloids such as ajmalicine, serpentine, ajmaline and catharanthine were observed. In addition to the increased accumulation of alkaloids in the tissues, the root exudation of phytochemicals increased compared to that of the non-treated control hairy roots. Moreover, MeJA induced differential secretion of several C. roseus hairy root metabolites.

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

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  1. Vick, B. A., & Zimmerman, D. C. (1984). The biosynthesis of jasmonic acid by several plant species. Plant Physiology, 75, 458–461.

    Article  CAS  Google Scholar 

  2. Feussner, I., & Wasternack, C. (2002). The lipoxygenase pathway. Annual Review of Plant Biology, 53, 275–297. doi:10.1146/annurev.arplant.53.100301.135248.

    Article  CAS  Google Scholar 

  3. Wasternack, C. (2007). Jasmonates: an update on biosynthesis, signal transduction and action in plant stress response, growth and development. Annals of Botany, 100, 681–697. doi:10.1093/aob/mcm079.

    Article  CAS  Google Scholar 

  4. Creelman, R. A., & Mullet, J. E. (1997). Biosynthesis and action of jasmonates in plants. Annual Review of Plant Physiology and Plant Molecular Biology, 48, 355–381. doi:10.1146/annurev.arplant.48.1.355.

    Article  CAS  Google Scholar 

  5. Farmer, E. E., Almeras, E., & Krishnamurthy, V. (2003). Jasmonates and related oxylipins in plant responses to pathogenesis and herbivory. Current Opinion in Plant Biology, 6, 372–378. doi:10.1016/S1369-5266(03)00045-1.

    Article  CAS  Google Scholar 

  6. Creelman, R. A., & Mullet, J. E. (1995). Jasmonic acid distribution and action in plants: Regulation during development and response to biotic and abiotic stress. Proceedings of the National Academy of Sciences of the United States of America, 92, 4114–4119. doi:10.1073/pnas.92.10.4114.

    Article  CAS  Google Scholar 

  7. Badri, D. V., Loyola-Vargas, V. M., Du, J., Stermitz, F. R., Broeckling, C. D., Iglesias-Andreu, L. G., et al. (2008). Increase in the secretion of phytochemicals by roots of Arabidopsis thaliana under the effect of several growth regulators. The New Phytologist, 179, 209–223. doi:10.1111/j.1469-8137.2008.02458.x.

    Article  CAS  Google Scholar 

  8. Vázquez-Flota, F., Moreno-Valenzuela, O. A., Miranda-Ham, M. L., Coello-Coello, J., & Loyola-Vargas, V. M. (1994). Catharanthine and ajmalicine synthesis in Catharanthus roseus hairy root cultures. Medium optimization and elicitation. Plant Cell, Tissue and Organ Culture, 38, 273–279. doi:10.1007/BF00033887.

    Article  Google Scholar 

  9. Aerts, R. J., Gisi, D., De Carolis, E., De Luca, V., & Baumann, T. W. (1994). Methyl jasmonate vapor increases the developmentally controlled synthesis of alkaloid in Catharanthus and Cinchona seedling. The Plant Journal, 5, 635–643. doi:10.1111/j.1365-313X.1994.00635.x.

    Article  CAS  Google Scholar 

  10. Gantet, P., Imbault, N., Thiersault, M., & Doireau, P. (1998). Necessity of a functional octadecanoic pathway for indole alkaloid synthesis by Catharanthus roseus cell suspensions cultured in an auxin-starved medium. Plant & Cell Physiology, 39, 220–225.

    CAS  Google Scholar 

  11. Lee-Parsons, C. W. T., & Ertük, S. (2005). Ajmalicine production in methyl jasmonate-induced Catharanthus roseus cell cultures depends on Ca2+ level. Plant Cell Reports, 24, 677–682. doi:10.1007/s00299-005-0026-0.

    Article  CAS  Google Scholar 

  12. Lee-Parsons, C. W. T., Ertük, S., & Tengtrakool, J. (2004). Enhancement of ajmalicine production in Catharanthus roseus cell cultures with methyl jasmonate is dependent on timing and dosage of elicitation. Biotechnology Letters, 26, 1595–1599. doi:10.1023/B:BILE.0000045825.37395.94.

    Article  CAS  Google Scholar 

  13. Van der Fits, L., Zhang, H., Menke, F. L. H., Deneka, M., & Memelink, J. (2000). A Catharanthus roseus BPF-1 homologue interacts with an elicitor-responsive region of the secondary metabolite biosynthetic gene Str and is induced by elicitor via a JA-independent signal transduction pathway. Plant Molecular Biology, 44, 675–685. doi:10.1023/A:1026526522555.

    Article  Google Scholar 

  14. Menke, F. L. H., Champion, A., Kijne, J. W., & Memelink, J. (1999). A novel jasmonate- and elicitor-responsive element in the periwinkle secondary metabolite biosynthetic gene Str interacts with a jasmonate- and elicitor-inducible AP2-domain transcription factor, ORCA2. The EMBO Journal, 18, 4455–4463. doi:10.1093/emboj/18.16.4455.

    Article  CAS  Google Scholar 

  15. Van der Fits, L., & Memelink, J. (2000). ORCA3, a jasmonate-responsive transcriptional regulator of plant primary and secondary metabolism. Science, 289, 295–297. doi:10.1126/science.289.5477.295.

    Article  Google Scholar 

  16. Zhang, Z.-P., & Baldwin, I. T. (1997). Transport of [2–14C] jasmonic acid from leaves to roots mimics wound-induced changes in endogenous jasmonic acid pools in Nicotiana sylvestris. Planta, 203, 436–441. doi:10.1007/s004250050211.

    Article  CAS  Google Scholar 

  17. Parchmann, S., Gundlach, H., & Mueller, M. J. (1997). Induction of 12-oxo-phytodienoic acid in wounded plants and elicited plant cell cultures. Plant Physiology, 115, 1057–1064. doi:10.1104/pp.115.3.1057.

    Article  CAS  Google Scholar 

  18. De Luca, V., & St Pierre, B. (2000). The cell and developmental biology of alkaloid biosynthesis. Trends in Plant Science, 5, 168–173. doi:10.1016/S1360-1385(00)01575-2.

    Article  Google Scholar 

  19. Loyola-Vargas, V. M., Broeckling, C. D., Badri, D. V., & Vivanco, J. M. (2007). Effect of transporters on the secretion of phytochemicals by the roots of Arabidopsis thaliana. Planta, 225, 301–310. doi:10.1007/s00425-006-0349-2.

    Article  CAS  Google Scholar 

  20. Bais, H. P., Weir, T. L., Perry, L. G., Gilroy, S., & Vivanco, J. M. (2006). The role of root exudates in rhizosphere interactions with pand other organisms. Annual Review of Plant Biology, 57, 233–266. doi:10.1146/annurev.arplant.57.032905.105159.

    Article  CAS  Google Scholar 

  21. Ciau-Uitz, R., Miranda-Ham, M. L., Coello-Coello, J., Chí, B., Pacheco, L. M., & Loyola-Vargas, V. M. (1994). Indole alkaloid production by transformed and non-transformed root cultures of Catharanthus roseus. In Vitro Cell Developmental Biology-Plant, 30, 84–88.

    Article  Google Scholar 

  22. Gamborg, O. L., Miller, R. A., & Ojima, K. (1968). Nutrient requirements of suspension cultures of soybean root cells. Experimental Cell Research, 50, 151–158. doi:10.1016/0014-4827(68)90403-5.

    Article  CAS  Google Scholar 

  23. Monforte-González, M., Ayora-Talavera, T., Maldonado-Mendoza, I. E., & Loyola-Vargas, V. M. (1992). Quantitative analysis of serpentine and ajmalicine in plant tissues of Catharanthus roseus and hyoscyamine and scopolamine in root tissues of Datura stramonium by densitometry in thin layer chromatography. Phytochemical Analysis, 3, 117–121. doi:10.1002/pca.2800030305.

    Article  Google Scholar 

  24. Matsumoto, T., Ikeda, T., Okimura, C., Obi, Y., Kisaki, T., Noguchi, M. (1982). Production of ubiquinone 10 (UQ-10) by UQ highly producing strains selected by a cell cloning technique. In A. Fujiwara (Ed.), Plant tissue culture (pp. 275–276). Tokyo: Japanese Association for Plant Tissue Culture.

  25. Loyola-Vargas, V. M., Galaz-Avalos, R. M., & Rodríguez-Ku, J. R. (2007). Catharanthus biosynthetic enzymes: The road ahead. Phytochemistry Reviews, 6, 307–339. doi:10.1007/s11101-007-9064-2.

    Article  CAS  Google Scholar 

  26. Spollansky, T. C., Pitta-Alvarez, S. I., & Giulietti, A. M. (2000). Effect of jasmonic acid and aluminum on production of tropane alkaloids in hairy root cultures of Brugmansia candida. Electronic Journal of Biotechnology, 3, 72–75.

    Google Scholar 

  27. Colque, R., Viladomat, F., Bastida, J., & Codina, C. (2004). Improved production of galanthamine and related alkaloids by methyl jasmonate in Narcissus confusus shoot-clumps. Planta Medica, 70, 1180–1188. doi:10.1055/s-2004-835849.

    Article  CAS  Google Scholar 

  28. Zhao, J., Davis, L. C., & Verpoorte, R. (2005). Elicitor signal transduction leading to production of plant secondary metabolites. Biotechnology Advances, 23, 283–333. doi:10.1016/j.biotechadv.2005.01.003.

    Article  CAS  Google Scholar 

  29. Bonfill, M., Bentebibel, S., Moyano, E., Palazón, J., Cusidó, R. M., Eibl, R., et al. (2007). Paclitaxel and baccatin III production induced by methyl jasmonate in free and immobilized cells of Taxus baccata. Biologia Plantarum, 51, 647–652. doi:10.1007/s10535-007-0137-2.

    Article  CAS  Google Scholar 

  30. Gadzovska, S., Maury, S., Delaunay, A., Spasenoski, M., Joseph, C., & Hagège, D. (2007). Jasmonic acid elicitation of Hypericum perforatum L. cell suspensions and effects on the production of phenylpropanoids and naphtodianthrones. Plant Cell, Tissue and Organ Culture, 89, 1–13. doi:10.1007/s11240-007-9203-x.

    Article  CAS  Google Scholar 

  31. Baldwin, I. T. (1996). Methyl jasmonate-induced nicotine production in Nicotiana attenuata: inducing defenses in the field without wounding. Entomologia Experimentalis et Applicata, 80, 213–220. doi:10.1007/BF00194760.

    Article  CAS  Google Scholar 

  32. Staswick, P. E., Su, W., & Howell, S. H. (1992). Methyl jasmonate inhibition of root growth and induction of a leaf protein are decreased in an Arabidopsis thaliana mutant. Proceedings of the National Academy of Sciences of the United States of America, 89, 6837–6840. doi:10.1073/pnas.89.15.6837.

    Article  CAS  Google Scholar 

  33. Goossens, A., Hakkinen, S. T., Laakso, I., Seppanen-Laakso, T., Biondi, S., De Sutter, V., et al. (2003). A functional genomics approach toward the understanding of secondary metabolism in plant cells. Proceedings of the National Academy of Sciences of the United States of America, 100, 8595–8600. doi:10.1073/pnas.1032967100.

    Article  CAS  Google Scholar 

  34. El-Sayed, M., & Verpoorte, R. (2005). Methyljasmonate accelerates catabolism of monoterpenoid indole alkaloids in Catharanthus roseus during leaf processing. Fitoterapia, 76, 83–90. doi:10.1016/j.fitote.2004.10.019.

    Article  CAS  Google Scholar 

  35. Eichhorn, H., Klinghammer, M., Becht, P., & Tenhaken, R. (2006). Isolation of a novel ABC-transporter gene from soybean induced by salicylic acid. Journal of Experimental Botany, 57, 2193–2201. doi:10.1093/jxb/erj179.

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We are grateful to Emily Wortman-Wunder and Clelia De-la-Peña for editorial assistance.

Author information

Authors and Affiliations

  1. Unidad de Bioquímica y Biología Molecular de Plantas, Centro de Investigación Científica de Yucatán, Calle 43 No. 130, Col. Chuburná de Hidalgo, Merida, Yucatán, Mexico

    Eliel Ruiz-May, Rosa M. Galaz-Ávalos & Víctor M. Loyola-Vargas

Authors
  1. Eliel Ruiz-May
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Rosa M. Galaz-Ávalos
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Víctor M. Loyola-Vargas
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Víctor M. Loyola-Vargas.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Ruiz-May, E., Galaz-Ávalos, R.M. & Loyola-Vargas, V.M. Differential Secretion and Accumulation of Terpene Indole Alkaloids in Hairy Roots of Catharanthus roseus Treated with Methyl Jasmonate. Mol Biotechnol 41, 278–285 (2009). https://doi.org/10.1007/s12033-008-9111-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12033-008-9111-2

Keywords

Search

Navigation