Biosynthesis of Triterpenoid Saponins in Plants

  • Kosmas Haralampidis
  • Miranda Trojanowska
  • Anne E. Osbourn
Chapter
Part of the Advances in Biochemical Engineering/Biotechnology book series (ABE, volume 75)

Abstract

Many different plant species synthesise triterpenoid saponins as part of their normal programme of growth and development. Examples include plants that are exploited as sources of drugs, such as liquorice and ginseng, and also crop plants such as legumes and oats. Interest in these molecules stems from their medicinal properties, antimicrobial activity, and their likely role as determinants of plant disease resistance. Triterpenoid saponins are synthesised via the isoprenoid pathway by cyclization of 2,3-oxidosqualene to give primarily oleanane (β-amyrin) or dammarane triterpenoid skeletons. The triterpenoid backbone then undergoes various modifications (oxidation, substitution and glycosylation), mediated by cytochrome P450-dependent monooxygenases, glycosyltransferases and other enzymes. In general very little is known about the enzymes and biochemical pathways involved in saponin biosynthesis. The genetic machinery required for the elaboration of this important family of plant secondary metabolites is as yet largely uncharacterised, despite the considerable commercial interest in this important group of natural products. This is likely to be due in part to the complexity of the molecules and the lack of pathway intermediates for biochemical studies. Considerable advances have recently been made, however, in the area of 2,3-oxidosqualene cyclisation, and a number of genes encoding the enzymes that give rise to the diverse array of plant triterpenoid skeletons have been cloned. Progress has also been made in the characterisation of saponin glucosyltransferases. This review outlines these developments, with particular emphasis on triterpenoid saponins.

Keywords

Saponins Triterpenoids Sterols 2,3-Oxidosqualene cyclases Glycosyltransferases 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. 1.
    Wink M (1999) Functions of plant secondary metabolites and their exploitation in biotechnology, Sheffield Academic Press, SheffieldGoogle Scholar
  2. 2.
    Tschesche R (1971) Advances in the chemistry of antibiotic substances from higher plants. In: Wagner H, Hörhammer L (eds) Pharmacognosy and phytochemistry. Springer, Berlin Heidelberg New York, p 274Google Scholar
  3. 3.
    Schönbeck F, Schlösser E (1976) Preformed substances as potential phytoprotectants. In: Heitefuss R, Williams PH (eds) Physiological plant pathology. Springer, Berlin Heidelberg New York, p 653Google Scholar
  4. 4.
    Osbourn AE (1996) Plant Cell 8:1821CrossRefGoogle Scholar
  5. 5.
    Morrissey JP, Osbourn AE (1999) Microbiol Mol Biol Revs 63:708Google Scholar
  6. 6.
    Price KR, Johnson IT, Fenwick GR (1987) CRC Crit Rev Food Sci Nutr 26:27Google Scholar
  7. 7.
    Hostettmann K, Hostettmann M, Marston M ( 1991) Methods Plant Biochem 7:434Google Scholar
  8. 8.
    Fenwick GR, Price KR, Tsukamota C, Okubo K ( 1992) Saponins. In: D’Mello JP, Duffus CM, Duffus JH (eds) Toxic substances in crop plants. The Royal Society of Chemistry, Cambridge, UK, p 284Google Scholar
  9. 9.
    Hostettmann KA, Marston A (1995) Saponins. Chemistry and pharmacology of natural products. Cambridge University Press, Cambridge, UKGoogle Scholar
  10. 10.
    Roddick JG (1974) Phytochemistry 13:9CrossRefGoogle Scholar
  11. 11.
    Osbourn AE (1996) Trends Plant Sci 1:4CrossRefGoogle Scholar
  12. 12.
    Kushiro T, Shibuya M, Ebizuka Y (1998) Eur J Biochem 256:238CrossRefGoogle Scholar
  13. 13.
    Kushiro T, Ohno Y, Shibuya M, Ebizuka Y (1997) Biol Pharm Bull 20:292Google Scholar
  14. 14.
    Kushiro T, Shibuya M, Ebizuka Y (1998) Molecular cloning of oxidosqualene cyclase cDNA from Panax ginseng: the isogene that encodes β-amyrin synthase. In: Ageta H, Aimi N, Ebizuka Y, Fujita T, Honda G (eds) Towards natural medicine research in the 21st century. Elsevier Science, Amsterdam, p 421Google Scholar
  15. 15.
    Kushiro T, Shibuya M, Ebizuka Y (1999) J Am Chem Soc 121:1208CrossRefGoogle Scholar
  16. 16.
    Papadopoulou K, Melton RE, Leggett M, Daniels MJ, Osbourn AE (1999) Proc Natl Acad Sci USA 96:12,923CrossRefGoogle Scholar
  17. 17.
    Ruzicka L, Eschenmoser A, Heusser H (1953) Experientia 357Google Scholar
  18. 18.
    Eschenmoser A, Ruzicka L, Jeger O, Arigoni D (1955) Helv Chem Acta 38:1890CrossRefGoogle Scholar
  19. 19.
    Nes WR, McKean ML (1977) Biochemistry of steroids and other isoprenoids. University Park Press, BaltimoreGoogle Scholar
  20. 20.
    Abe I, Rohmer M, Prestwich GD (1993) Chem Rev 93:2189CrossRefGoogle Scholar
  21. 21.
    Jolidon S, Polak AM, Guerry P, Hartmann PG (1990) Biochem Soc Trans 18:47Google Scholar
  22. 22.
    Cattel L, Ceruti M, Viola F, Delprino L, Balliano G, Duriatti A, Bouvier-Navé P ( 1986) Lipids 21:31CrossRefGoogle Scholar
  23. 23.
    Baisted DJ (1971) Biochem J 124:375Google Scholar
  24. 24.
    Threlfall DR, Whitehead IM (1990) Redirection of terpenoid biosynthesis in elicitor-treated plant cell suspension cultures. In: Quinn PJ, Harwood JL (eds) Plant lipid biochemistry. Portland Press, London, p 344Google Scholar
  25. 25.
    Van der Deijden R, Threlfall DR, Verpoorte R, Whitehead IM (1989) Phytochemistry 28:2981CrossRefGoogle Scholar
  26. 26.
    Henry M, Rahier A, Taton M (1992) Phytochemistry 31:3855CrossRefGoogle Scholar
  27. 27.
    Abe I, Sankawa U, Ebizuka Y ( 1992) Chem Pharm Bull 40:1755Google Scholar
  28. 28.
    Goad LJ (1983) Biochem Soc Trans 548Google Scholar
  29. 29.
    Palmer MA, Bowden BN (1977) Phytochemistry 16:459CrossRefGoogle Scholar
  30. 30.
    Abe I, Ebizuka Y, Sankawa U (1988) Chem Pharm Bull 36:5031Google Scholar
  31. 31.
    Abe I, Sankawa U, Ebizuka Y ( 1989) Chem Pharm Bull 37:536Google Scholar
  32. 32.
    Abe I, Ebizuka Y, Seo S, Sankawa U ( 1989) FEBS Letts 249:100CrossRefGoogle Scholar
  33. 33.
    Buntel CJ, Griffin JH (1994) ACS Sym Ser 562:44CrossRefGoogle Scholar
  34. 34.
    Abe I, Prestwich GD (1995) Proc Natl Acad Sci 92:9274CrossRefGoogle Scholar
  35. 35.
    Kusano M, Shibuya M, Sankawa U, Ebizuka Y (1995) Biol Pharm Bull 18:195Google Scholar
  36. 36.
    Shi Z, Buntel CJ, Griffin JH (1994) Proc Natl Acad Sci 91:7370CrossRefGoogle Scholar
  37. 37.
    Kelly R, Miller SM, Lai MH, Kirsch DR (1990) Gene 87:177CrossRefGoogle Scholar
  38. 38.
    Roessner CA, Min C, Hardin SH, Harris-Haller LW, McCollum JC, Scott AL (1993) Gene 127:149CrossRefGoogle Scholar
  39. 39.
    Corey EJ, Matsuda SPT, Bartel B ( 1993) Proc Natl Acad Sci 90:11,628CrossRefGoogle Scholar
  40. 40.
    Sung CK, Shibuya M, Sankawa U, Ebizuka Y (1995) Biol Pharm Bull 18:1459Google Scholar
  41. 41.
    Corey EJ, Matsuda SPT, Bartel B ( 1994) Proc Natl Acad Sci USA 91:2211CrossRefGoogle Scholar
  42. 42.
    Morita M, Shibuya M, Lee M-S, Sankawa U, Ebizuka Y ( 1997) Biol Pharm Bull 20:770Google Scholar
  43. 43.
    Venkatramesh M, Nes WD (1995) Arch Biochem Biophys 324:189CrossRefGoogle Scholar
  44. 44.
    Morita M, Shibuya M, Kushiro T, Masuda K, Ebizuka Y (2000) Eur J Biochem 267:3453CrossRefGoogle Scholar
  45. 45.
    Shibuya M, Zhang H, Endo A, Shishikura K, Kushiro T, Ebizuka Y (1999) Eur J Biochem 266:302CrossRefGoogle Scholar
  46. 46.
    Herrera JBR, Bartel B, Wilson WK, Matsuda SPT (1998) Phytochemistry 49:1905CrossRefGoogle Scholar
  47. 47.
    Husselstein-Muller T, Schaller H, Benveniste P (2001) Plant Mol Biol 45:63CrossRefGoogle Scholar
  48. 48.
    Kushiro T, Shibuya M, Masuda K, Ebizuka Y (2000) Tetrahedron Letts 41:7705CrossRefGoogle Scholar
  49. 49.
    Segura MJR, Meyer MM, Matsuda SPT (2000) Org Letts 2:2257CrossRefGoogle Scholar
  50. 50.
    Felsenstein J (1996) Methods Enzymol 266:418CrossRefGoogle Scholar
  51. 51.
    Ourisson G, Rohmer M, Poralla K (1987) Ann Rev Microbiol 41:301CrossRefGoogle Scholar
  52. 52.
    Perzl M, Müller P, Poralla K, Kannenberg EL (1997) Microbiology 143:1235CrossRefGoogle Scholar
  53. 53.
    Reipen IG, Poralla K, Sahm H, Sprenger GA (1995) Microbiology 141:155Google Scholar
  54. 54.
    Ochs D, Kaletta C, Entian K-D, Beck-Sickinger A, Poralla K (1992) J Bact 174:298Google Scholar
  55. 55.
    Wendt KU, Poralla K, Schultz GE (1997) Science 277:1811CrossRefGoogle Scholar
  56. 56.
    Wendt KU, Lenhart A, Schulz GE (1999) J Mol Biol 286:175CrossRefGoogle Scholar
  57. 57.
    Abe I, Prestwich GD (1994) J Biol Chem 269:802Google Scholar
  58. 58.
    Abe I, Prestwich GD (1995) Lipids 30:231CrossRefGoogle Scholar
  59. 59.
    Feil C, Sussmuth R, Jung G, Poralla K (1996) Eur J Biochem 242:51CrossRefGoogle Scholar
  60. 60.
    Corey EJ, Cheng H, Baker H, Matsuda SPT, Li D, Song X ( 1997) J Am Chem Soc 119:1277CrossRefGoogle Scholar
  61. 61.
    Dang T, Prestwich GD (2000) Chem Biol 7:643CrossRefGoogle Scholar
  62. 62.
    Poralla K, Hewelt A, Prestwich GD, Abe I, Reipen I, Sprenger G ( 1994) TIBS 19:157Google Scholar
  63. 63.
    Sato T, Kanai Y, Hoshino T (1998) Biosci Biotech Biochem 62:407CrossRefGoogle Scholar
  64. 64.
    Poralla K ( 1994) Bioorg Med Chem Lett 4:285CrossRefGoogle Scholar
  65. 65.
    Corey EJ, Matsuda SPT (1991) J Am Chem Soc 113:8172CrossRefGoogle Scholar
  66. 66.
    Hayashi H, Hiraoka N, Ikeshiro Y, Kushiro T, Morita M, Shibuya M, Ebizuka Y (2000) Biol Pharm Bull 23:231Google Scholar
  67. 67.
    Hart EA, Hua L, Darr LB, Wilson WK, Pang J, Matsuda SPT (1999) J Am Chem Soc 121:9887CrossRefGoogle Scholar
  68. 68.
    Herrera JBR, Wilson WK, Matsuda SPT (2000) J Am Chem Soc 122:6765CrossRefGoogle Scholar
  69. 69.
    Meyer MM, Segura MJR, Wilson WK, Matsuda SPT (2000) Angew Chem Int Ed 39:4090CrossRefGoogle Scholar
  70. 70.
    Kushiro T, Shibuya M, Ebizuka Y (1999) Tet Lett 40:5553CrossRefGoogle Scholar
  71. 71.
    Kushiro T, Shibuya M, Masuda K, Ebizuka Y (2000) J Am Chem Soc 122:6816CrossRefGoogle Scholar
  72. 72.
    Matsuda SPT (1998) In: Steinbüchel A (ed) Biochemical principles and mechanisms of biosynthesis and degradation of polymers. Wiley-VCH, Weinheim, p 300Google Scholar
  73. 73.
    Taton M, Benveniste P, Rahier A (1992) Biochemistry 31:7892CrossRefGoogle Scholar
  74. 74.
    Taton M, Benveniste P, Rahier A (1986) Biochem Biophys Res Comm 138:764CrossRefGoogle Scholar
  75. 75.
    Cattel L, Ceruti M ( 1992) 2,3-Oxidosqualene cyclase and squalene epoxidase: enzymology, mechanism and inhibitors. In: Patterson GW, Nes WD (eds) Physiology and biochemistry of sterols. American Oil Chemists’ Society, Champaign, p 50Google Scholar
  76. 76.
    Taton M, Ceruti M, Cattel L, Rahier A (1996) Phytochemistry 43:75CrossRefGoogle Scholar
  77. 77.
    Paczkowski C, Wojciechowski ZA ( 1994) Phytochemistry 35:1429CrossRefGoogle Scholar
  78. 78.
    Kintia PK, Wojciechowski Z, Kasprzyk Z (1974) Bulletin de L’Académie Polonaise des Sciences 22:73Google Scholar
  79. 79.
    Wojciechowski ZA (1975) Phytochemistry 14:1749CrossRefGoogle Scholar
  80. 80.
    Bergenstråhle A, Tillberg E, Jonsson L (1992) Plant Sci 84:35CrossRefGoogle Scholar
  81. 81.
    Kalinowska M, Wojciechowski ZA (1986) Phytochemistry 25:2525CrossRefGoogle Scholar
  82. 82.
    Kalinowska M, Wojciechowski ZA (1987) Phytochemistry 26:353CrossRefGoogle Scholar
  83. 83.
    Kalinowska M, Wojciechowski ZA (1988) Plant Science 55:239CrossRefGoogle Scholar
  84. 84.
    Paczkowski C, Wojciechowski ZA (1988) Phytochemistry 27:2743CrossRefGoogle Scholar
  85. 85.
    Paczkowski C, Zimowski J, Krawczyk D, Wojciechowski ZA ( 1990) Phytochemistry 29:63CrossRefGoogle Scholar
  86. 86.
    Paczkowski C, Kalinowska M, Wojciechowski ZA (1997) Acta Biochimica Polonica 44:43Google Scholar
  87. 87.
    Paczkowski C, Kalinowska M, Wojciechowski ZA ( 1998) Phytochemistry 48:1151CrossRefGoogle Scholar
  88. 88.
    Stapleton A, Allen PV, Friedman M, Belknap WR ( 1991 ) J Agric Food Chem 39:1187CrossRefGoogle Scholar
  89. 89.
    Zimowski J (1991) Phytochemistry 30:1827CrossRefGoogle Scholar
  90. 90.
    Zimowski J (1992) Phytochemistry 31:2977CrossRefGoogle Scholar
  91. 91.
    Zimowski J (1996) Enzymatic glycosylation of tomatidine in tomato plants. In: Waller GR, Yamasaki K (eds) Saponins used in traditional and modern medicine. Plenum Press, New York, p 71Google Scholar
  92. 92.
    Kalinowska M (1994) Phytochemistry 36:617CrossRefGoogle Scholar
  93. 93.
    Zimowski J (1994) Acta Biochimica Polonica 41:202Google Scholar
  94. 94.
    Zimowski J (1998) Plant Sci 136:139CrossRefGoogle Scholar
  95. 95.
    Moehs CP, Allen PV, Friedman M, Belknap WR (1997) Plant J 11:227CrossRefGoogle Scholar
  96. 96.
    Vogt T, Jones P (2000) Trends Plant Sci 5:380CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2002

Authors and Affiliations

  • Kosmas Haralampidis
    • 1
  • Miranda Trojanowska
    • 1
  • Anne E. Osbourn
    • 1
  1. 1.Sainsbury LaboratoryJohn Innes CentreNorwichUK

Personalised recommendations