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Modulation of Triterpene Saponin Production: In Vitro Cultures, Elicitation, and Metabolic Engineering

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Abstract

Saponins are secondary metabolites that are widely distributed in the plant kingdom and are often the active components in medicinal herbs. Hence, saponins have a potential for the pharmaceutical industry as antibacterial, virucidal, anti-inflammatory, and anti-leishmanial drugs. However, their commercial application is often hindered because of practical problems, such as low and variable yields and limited availability of natural resources. In vitro cultures provide an alternative to avoid problems associated with field production; they offer a system in which plants are clonally propagated and yield is not affected by environmental changes. Additionally, treatment of in vitro cultures with elicitors such as methyl jasmonate may increase the production of saponins up to six times. In vitro cultures are amenable to metabolic engineering by targeting specific genes to enhance saponin production or drive production towards one specific class of saponins. Hitherto, this approach is not yet fully explored because only a limited number of saponin biosynthesis genes are identified. In this paper, we review recent studies on in vitro cultures of saponin-producing plants. The effect of elicitation on saponin production and saponin biosynthesis genes is discussed. Finally, recent research efforts on metabolic engineering of saponins will also be presented.

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References

  1. Vincken, J. P., Heng, L., de Groot, A., & Gruppen, H. (2007). Phytochemistry, 68, 275–297.

    Article  CAS  Google Scholar 

  2. Liu, J. K., & Henkel, T. (2002). Current Medicinal Chemistry, 9, 1483–1485.

    CAS  Google Scholar 

  3. Wu, J. Y., & Zhong, J. J. (1999). Journal of Biotechnology, 68, 89–99.

    Article  CAS  Google Scholar 

  4. Liang, Y., & Zhao, S. (2008). Plant Biology, 10, 415–421.

    Article  CAS  Google Scholar 

  5. Dang, H. X., Chen, Y., Liu, X. M., Wang, Q., Wang, L. W., Jia, W., et al. (2009). Progress in Neuro-Psychopharmacology & Biological Psychiatry, 33, 1417–1424.

    Article  CAS  Google Scholar 

  6. Luo, J. Z., & Luo, L. G. (2009). Evidence-Based Complementary and Alternative Medicine, 6, 423–427.

    Article  Google Scholar 

  7. Jia, L., & Zhao, Y. Q. (2009). Current Medicinal Chemistry, 16, 2475–2484.

    Article  CAS  Google Scholar 

  8. Jia, L., Zhao, Y. Q., & Liang, X. J. (2009). Current Medicinal Chemistry, 16, 2924–2942.

    Article  CAS  Google Scholar 

  9. Lu, J. M., Yao, Q. Z., & Chen, C. Y. (2009). Current Vascular Pharmacology, 7, 293–302.

    Article  CAS  Google Scholar 

  10. Francis, G., Kerem, Z., Makkar, H. P., & Becker, K. (2002). The British Journal of Nutrition, 88, 587–605.

    Article  CAS  Google Scholar 

  11. Morrissey, J. P., & Osbourn, A. E. (1999). Microbiology and Molecular Biology Reviews, 63, 708.

    CAS  Google Scholar 

  12. Gonzalez-Lamothe, R., Mitchell, G., Gattuso, M., Diarra, M. S., Malouin, F., & Bouarab, K. (2009). International Journal of Molecular Sciences, 10, 3400–3419.

    Article  CAS  Google Scholar 

  13. Papadopoulou, K., Melton, R. E., Leggett, M., Daniels, M. J., & Osbourn, A. E. (1999). Proceedings of the National Academy of Sciences of the United States of America, 96, 12923–12928.

    Article  CAS  Google Scholar 

  14. Trojanowska, M. R., Osbourn, A. E., Daniels, M. J., & Threlfall, D. R. (2001). Phytochemistry, 56, 121–129.

    Article  CAS  Google Scholar 

  15. Mylona, P., Owatworakit, A., Papadopoulou, K., Jenner, H., Qin, B., Findlay, K., et al. (2008). The Plant Cell, 20, 201–212.

    Article  CAS  Google Scholar 

  16. Bowyer, P., Clarke, B. R., Lunness, P., Daniels, M. J., & Osbourn, A. E. (1995). Science, 267, 371–374.

    Article  CAS  Google Scholar 

  17. Sacchettini, J. C., & Poulter, C. D. (1997). Science, 277, 1788–1789.

    Article  CAS  Google Scholar 

  18. Eisenreich, W., Schwarz, M., Cartayrade, A., Arigoni, D., Zenk, M. H., & Bacher, A. (1998). Chemistry & Biology, 5, R221–233.

    Article  CAS  Google Scholar 

  19. Dubey, V. S., Bhalla, R., & Luthra, R. (2003). Journal of Biosciences, 28, 637–646.

    Article  CAS  Google Scholar 

  20. Shibuya, M., Katsube, Y., Otsuka, M., Zhang, H., Tansakul, P., Xiang, T., et al. (2009). Plant Physiology and Biochemistry, 47, 26–30.

    Article  CAS  Google Scholar 

  21. Punja, Z. K., Feeney, M., Schluter, C., & Tautorus, T. (2004). In Vitro Cellular & Developmental Biology-Plant, 40, 329–338.

    Article  CAS  Google Scholar 

  22. Choi, Y. E., Jeong, J. H., & Shin, C. K. (2003). Plant Cell, Tissue and Organ Culture, 72, 229–235.

    Article  CAS  Google Scholar 

  23. Okrslar, V., Plaper, I., Kovac, M., Erjavec, A., Obermajer, T., Rebec, A., et al. (2007). In Vitro Cellular & Developmental Biology-Plant, 43, 644–651.

    Article  CAS  Google Scholar 

  24. Paek, K. Y., Murthy, H. N., Hahn, E. J., & Zhong, J. J. (2009). Biotechnology in China I, 113, 151–176.

    Article  CAS  Google Scholar 

  25. Langhansova, L., Marsik, P., & Vanek, T. (2005). Biologia Plantarum, 49, 463–465.

    Article  CAS  Google Scholar 

  26. Mangas, S., Moyano, E., Osuna, L., Cusido, R. M., Bonfill, M., & Palazon, J. (2008). Biotechnological Letters, 30, 1853–1859.

    Article  CAS  Google Scholar 

  27. Herold, M. C., & Henry, M. (2001). Biotechnology Letters, 23, 335–337.

    Article  CAS  Google Scholar 

  28. Arroo, R. R. J., Develi, A., Meijers, H., Vandewesterlo, E., Kemp, A. K., Croes, A. F., et al. (1995). Physiologia Plantarum, 93, 233–240.

    Article  CAS  Google Scholar 

  29. Choi, Y. E., Yang, D. C., Yoon, E. S., & Choi, K. T. (1999). Plant Cell Reports, 18, 493–499.

    Article  CAS  Google Scholar 

  30. Choi, Y. E., Yang, D. C., Park, J. C., Soh, W. Y., & Choi, K. T. (1998). Plant Cell Reports, 17, 544–551.

    Article  CAS  Google Scholar 

  31. Vasconsuelo, A., & Boland, R. (2007). Plant Science, 172, 861–875.

    Article  CAS  Google Scholar 

  32. Creelman, R. A., & Mullet, J. E. (1997). Annual Review of Plant Physiology and Plant Molecular Biology, 48, 355–381.

    Article  CAS  Google Scholar 

  33. Hu, F. X., & Zhong, J. J. (2008). Process Biochemistry, 43, 113–118.

    Article  CAS  Google Scholar 

  34. Raskin, I. (1992). Annual Review of Plant Physiology and Plant Molecular Biology, 43, 439–463.

    Article  CAS  Google Scholar 

  35. Ali, M. B., Yu, K. W., Hahn, E. J., & Paek, K. Y. (2006). Plant Cell Reports, 25, 613–620.

    Article  CAS  Google Scholar 

  36. Zhong, J. J., & Zhang, Z. Y. (2005). Engineering in Life Sciences, 5, 471–474.

    Article  CAS  Google Scholar 

  37. Wang, W., Zhang, Z. Y., & Zhong, J. J. (2005). Applied Microbiology and Biotechnology, 67, 752–758.

    Article  CAS  Google Scholar 

  38. Hu, F. X., & Zhong, J. J. (2007). Journal of Bioscience and Bioengineering, 104, 513–516.

    Article  CAS  Google Scholar 

  39. Shabani, L., Ehsanpour, A. A., Asghari, G., & Emami, J. (2009). Russian Journal of Plant Physiology, 56, 621–626.

    Article  CAS  Google Scholar 

  40. Pereira, P. S., Ticli, F. K., Franca, S. D. C., de Souza Breves, C. M., & Lourenco, M. V. (2007). Quimica Nova, 30, 1849–1852.

    CAS  Google Scholar 

  41. Kim, O. T., Kim, M. Y., Hong, M. H., Ahn, J. C., & Hwang, B. (2004). Plant Cell Reports, 23, 339–344.

    Article  CAS  Google Scholar 

  42. Suzuki, H., Achnine, L., Xu, R., Matsuda, S. P. T., & Dixon, R. A. (2002). The Plant Journal, 32, 1033–1048.

    Article  CAS  Google Scholar 

  43. Suzuki, H., Reddy, M. S. S., Naoumkina, M., Aziz, N., May, G. D., Huhman, D. V., et al. (2005). Planta, 220, 696–707.

    Article  CAS  Google Scholar 

  44. Kuzuyama, T. (2002). Bioscience, Biotechnology, and Biochemistry, 66, 1619–1627.

    Article  CAS  Google Scholar 

  45. Kim, Y. S., Han, J. Y., Lim, S., & Choi, Y. E. (2009). Journal of Medicinal Plants Research, 3, 1270–1276.

    CAS  Google Scholar 

  46. Kim, O. T., Kim, S. H., Ohyama, K., Muranaka, T., Choi, Y. E., Lee, H. Y., et al. (2010). Plant Cell Reports, 29, 403–411.

    Article  CAS  Google Scholar 

  47. Abe, I., Rohmer, M., & Prestwich, G. D. (1993). Chemical Reviews, 93, 2189–2206.

    Article  CAS  Google Scholar 

  48. Hayashi, H., Hirota, A., Hiraoka, N., & Ikeshiro, Y. (1999). Biological & Pharmaceutical Bulletin, 22, 947–950.

    CAS  Google Scholar 

  49. Devarenne, T. P., Ghosh, A., & Chappell, J. (2002). Plant Physiology, 129, 1095–1106.

    Article  CAS  Google Scholar 

  50. Lee, M. H., Jeong, J. H., Seo, J. W., Shin, C. G., Kim, Y. S., In, J. G., et al. (2004). Plant & Cell Physiology, 45, 976–984.

    Article  CAS  Google Scholar 

  51. Kim, O. T., Seong, N. S., Kim, M. Y., & Hwang, B. (2005). Journal of Plant Biology, 48, 263–269.

    Article  CAS  Google Scholar 

  52. Akamine, S., Nakamori, K., Chechetka, S. A., Banba, M., Umehara, Y., Kouchi, H., et al. (2003). Biochimica Et Biophysica Acta-Gene Structure and Expression, 1626, 97–101.

    Article  CAS  Google Scholar 

  53. Seo, J. W., Jeong, J. H., Shin, C. G., Lo, S. C., Han, S. S., Yu, K. W., et al. (2005). Phytochemistry, 66, 869–877.

    Article  CAS  Google Scholar 

  54. Uchida, H., Yamashita, H., Kajikawa, M., Ohyama, K., Nakayachi, O., Sugiyama, R., et al. (2009). Planta, 229, 1243–1252.

    Article  CAS  Google Scholar 

  55. Rasbery, J. M., Shan, H., LeClair, R. J., Norman, M., Matsuda, S. P. T., & Bartel, B. (2007). The Journal of Biological Chemistry, 282, 17002–17013.

    Article  CAS  Google Scholar 

  56. Han, J. Y., In, J. G., Kwon, Y. S., & Choi, Y. E. (2010). Phytochemistry, 71, 36–46.

    Article  CAS  Google Scholar 

  57. Kushiro, T., Shibuya, M., & Ebizuka, Y. (1998). Towards Natural Medicine Research in the 21st Century, 1157, 421–427.

    CAS  Google Scholar 

  58. Morita, M., Shibuya, M., Kushiro, T., Masuda, K., & Ebizuka, Y. (2000). European Journal of Biochemistry, 267, 3453–3460.

    Article  CAS  Google Scholar 

  59. Hayashi, H., Huang, P. Y., Kirakosyan, A., Inoue, K., Hiraoka, N., Ikeshiro, Y., et al. (2001). Biological & Pharmaceutical Bulletin, 24, 912–916.

    Article  CAS  Google Scholar 

  60. Haralampidis, K., Bryan, G., Qi, X., Papadopoulou, K., Bakht, S., Melton, R., et al. (2001). Proceedings of the National Academy of Sciences of the United States of America, 98, 13431–13436.

    Article  CAS  Google Scholar 

  61. Iturbe-Ormaetxe, I., Haralampidis, K., Papadopoulou, K., & Osbourn, A. E. (2003). Plant Molecular Biology, 51, 731–743.

    Article  CAS  Google Scholar 

  62. Zhang, H., Shibuya, M., Yokota, S., & Ebizuka, Y. (2003). Biological & Pharmaceutical Bulletin, 26, 642–650.

    Article  CAS  Google Scholar 

  63. Kajikawa, M., Yamato, K. T., Fukuzawa, H., Sakai, Y., Uchida, H., & Ohyama, K. (2005). Phytochemistry, 66, 1759–1766.

    Article  CAS  Google Scholar 

  64. Meesapyodsuk, D., Balsevich, J., Reed, D. W., & Covello, P. S. (2007). Plant Physiology, 143, 959–969.

    Article  CAS  Google Scholar 

  65. Cammareri, M., Consiglio, M. F., Pecchia, P., Corea, G., Lanzotti, V., Ibeas, J. I., et al. (2008). Plant Science, 175, 255–261.

    Article  CAS  Google Scholar 

  66. Scholz, M., Lipinski, M., Leupold, M., Luftmann, H., Harig, L., Ofir, R., et al. (2009). Phytochemistry, 70, 517–522.

    Article  CAS  Google Scholar 

  67. Liu, Y. L., Cai, Y. F., Zhao, Z. J., Wang, J. F., Li, J., Xin, W., et al. (2009). Biological & Pharmaceutical Bulletin, 32, 818–824.

    Article  CAS  Google Scholar 

  68. Confalonieri, M., Cammareri, M., Biazzi, E., Pecchia, P., Fevereiro, M. P. S., Balestrazzi, A., et al. (2009). Plant Biotechnology Journal, 7, 172–182.

    Article  CAS  Google Scholar 

  69. Hayashi, H., Huang, P., Takada, S., Obinata, M., Inoue, K., Shibuya, M., et al. (2004). Biological & Pharmaceutical Bulletin, 27, 1086–1092.

    Article  CAS  Google Scholar 

  70. Ohnishi, T., Yokota, T., & Mizutani, M. (2009). Phytochemistry, 70, 1918–1929.

    Article  CAS  Google Scholar 

  71. Shibuya, M., Hoshino, M., Katusbe, Y., Hayashi, H., Kushiro, T., & Ebizuka, Y. (2006). The FEBS Journal, 273, 948–959.

    Article  CAS  Google Scholar 

  72. Seki, H., Ohyama, K., Sawai, S., Mizutani, M., Ohnishi, T., Sudo, H., et al. (2008). Proceedings of the National Academy of Sciences of the United States of America, 105, 14204–14209.

    Article  CAS  Google Scholar 

  73. Qi, X., Bakht, S., Qin, B., Leggett, M., Hemmings, A., Mellon, F., et al. (2006). Proceedings of the National Academy of Sciences of the United States of America, 103, 18848–18853.

    Article  CAS  Google Scholar 

  74. Mizutani, M., & Ohta, D. (2010). Annual Review of Plant Biology, 61, 291–315.

    Article  CAS  Google Scholar 

  75. Phillips, D. R., Rasbery, J. M., Bartel, B., & Matsuda, S. P. T. (2006). Current Opinion in Plant Biology, 9, 305–314.

    Article  CAS  Google Scholar 

  76. Xu, R., Fazio, G. C., & Matsuda, S. P. T. (2004). Phytochemistry, 65, 261–291.

    Article  CAS  Google Scholar 

  77. Achnine, L., Huhman, D. V., Farag, M. A., Sumner, L. W., Blount, J. W., & Dixon, R. A. (2005). The Plant Journal, 41, 875–887.

    Article  CAS  Google Scholar 

  78. Naoumkina, M. A., Modolo, L. V., Huhman, D. V., Urbanczyk-Wochniak, E., Tang, Y. H., Sumner, L. W., et al. (2010). The Plant Cell, 22, 850–866.

    Article  CAS  Google Scholar 

  79. Shibuya, M., Nishimura, K., Yasuyama, N., & Ebizuka, Y. (2010). FEBS Letters, 584, 2258–2264.

    Article  CAS  Google Scholar 

  80. Vogt, T., & Jones, P. (2000). Trends in Plant Science, 5, 380–386.

    Article  CAS  Google Scholar 

  81. Modolo, L. V., Blount, J. W., Achnine, L., Naoumkina, M. A., Wang, X. Q., & Dixon, R. A. (2007). Plant Molecular Biology, 64, 499–518.

    Article  CAS  Google Scholar 

  82. Zhang, W. J., & Tang, Y. (2008). Journal of Medicinal Chemistry, 51, 2629–2633.

    Article  CAS  Google Scholar 

  83. Floss, H. G. (2006). Journal of Biotechnology, 124, 242–257.

    Article  CAS  Google Scholar 

  84. Julsing, M. K., Koulman, A., Woerdenbag, H. J., Quax, W. J., & Kayser, O. (2006). Biomolecular Engineering, 23, 265–279.

    Article  CAS  Google Scholar 

  85. Menzella, H. G., & Reeves, C. D. (2007). Current Opinion in Microbiology, 10, 238–245.

    Article  CAS  Google Scholar 

  86. Horinouchi, S. (2009). Current Opinion in Chemical Biology, 13, 197–204.

    Article  CAS  Google Scholar 

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Acknowledgments

This research was funded by FWO-Flanders (project No. G.0014.08) and the Directorate General of Higher Education, Ministry of National Education, Republic of Indonesia.

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  1. Department of Plant Production, Faculty of Bioscience Engineering, University of Ghent, Coupure Links 653, 9000, Ghent, Belgium

    Ellen Lambert, Ahmad Faizal & Danny Geelen

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  1. Ellen Lambert
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  2. Ahmad Faizal
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  3. Danny Geelen
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Correspondence to Danny Geelen.

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Lambert, E., Faizal, A. & Geelen, D. Modulation of Triterpene Saponin Production: In Vitro Cultures, Elicitation, and Metabolic Engineering. Appl Biochem Biotechnol 164, 220–237 (2011). https://doi.org/10.1007/s12010-010-9129-3

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