A genomics approach to the early stages of triterpene saponin biosynthesis in Medicago truncatula

Plant Journal

Volumn 32, Issue 6, 2002, Pages 1033-1048

  Suzuki, Hideyuki ^a   Achnine, Lahoucine ^a   Xu, Ran ^b   Matsuda, Seiichi P T ^b   Dixon, Richard A ^a  

^a PLANT BIOLOGY DIVISION   (United States)

^b RICE UNIVERSITY   (United States)

Author keywords

Elicitation; Functional expression; Methyl jasmonate; Saponin; Sterol; Triterpene

Indexed keywords

DNA; ENZYMES; PLANT CELL CULTURE; YEAST;

GENOMICS;

PLANTS (BOTANY);

ACETIC ACIDS; AMINO ACID SEQUENCE; CARBOHYDRATE SEQUENCE; CELLS, CULTURED; CYCLOPENTANES; ESCHERICHIA COLI; EXPRESSED SEQUENCE TAGS; FARNESYL-DIPHOSPHATE FARNESYLTRANSFERASE; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GENE EXPRESSION REGULATION, PLANT; GENOMICS; INTRAMOLECULAR TRANSFERASES; MEDICAGO; MOLECULAR SEQUENCE DATA; OLEANOLIC ACID; OXYGENASES; PHYLOGENY; PHYTOSTEROLS; SAPONINS; SIGNAL TRANSDUCTION; SQUALENE MONOOXYGENASE; TRITERPENES;

EMBRYOPHYTA; ESCHERICHIA COLI; EUKARYOTA; MEDICAGO; MEDICAGO TRUNCATULA;

EID: 0036959970     PISSN: 09607412     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1365-313X.2002.01497.x     Document Type: Article

References (69)

1. Abe, I. and Prestwich, G.D. (1995) Molecular cloning, characterization, and functional expression of rat oxidosqualene cyclase cDNA. Proc. Natl Acad. Sci. USA, 92, 9274-9278.
2. Abe, I., Rohmer, M. and Prestwich, G.D. (1993) Enzymatic cyclization of squalene and oxidosqualene to sterols and triterpenes. Chem. Rev. 93, 2189-2206.
3. Akalezi, C.O., Liu, S., Li, Q.S., Yu, J.T. and Zhong, J.J. (1999) Combined effects of initial sucrose concentration and inoculum size on cell growth and ginseng saponin production by suspension cultures of Panax ginseng. Process Biochem. 34, 639-664.
4. Behboudi, S., Morein, B. and VillacresEriksson, M.C. (1999) Quillaja saponin formulations that stimulate proinflammatory cytokines elicit a potent acquired cell-mediated immunity. Scand. J. Immunol. 50, 371-377.
5. Bell, C., Dixon, R.A., Farmer, A.D. et al. (2001) The Medicago genome initiative: a model legume database. Nucl Acids Res. 29, 114-117.
6. Bishop, G.J., Nomura, T., Yokota, T., Harrison, K., Noguchi, T., Fujioka, S., Takatsuto, S., Jones, J.D.G. and Kamiya, Y. (1999) The tomato DWARF enzyme catalyses C-6 oxidation in brassinosteroid biosynthesis. Proc. Natl Acad. Sci. USA, 96, 1761-1766.
7. Chapple, C. (1998) Molecular genetic analysis of plant cytochrome P450-dependent monooxygenases. Annu. Rev. Plant Physiol. Plant Mol. Biol. 49, 311-343.
8. Cheeke, P.R. (1976) Nutritional and physiological properties of saponins. Nutr. Report Int. 13, 315-324.
9. Church, G.M. and Gilbert, W. (1984) Genomic sequencing. Proc. Natl Acad. Sci. USA, 81, 1991-1995.
10. Corey, E.J., Matsuda, S.P.T., Baker, C.H., Ting, A.Y. and Cheng, H. (1996) Molecular cloning of a Schizosaccharomyces pombe cDNA encoding lanosterol synthase and investigation of conserved tryptophan residues. Biochem. Biophys. Res. Comm. 219, 327-331.
11. Corey, E.J., Matsuda, S.P.T. and Bartel, B. (1993) Isolation of an Arabidopsis thaliana gene encoding cycloartenol synthase by functional expression in a yeast mutant lacking lanosterol synthase by the use of a chromatographic screen. Proc. Natl Acad. Sci. USA, 90, 11628-11632.
12. Corey, E.J., Matsuda, S.P.T. and Bartel, B. (1994) Molecular cloning, characterization, and overexpression of ERG7, the Saccharomyces cerevisiae gene encoding lanosterol synthase. Proc. Natl Acad. Sci. USA, 91, 2211-2215.
13. Dixon, R.A. (1999) Isoflavonoids: biochemistry, molecular biology and biological functions. In Comprehensive Natural Products Chemistry, Vol. 1 (Sankawa, U., ed.). Oxford: Elsevier, pp. 773-823.
14. Dixon, R.A., Dey, P.M., Murphy, D.L. and Whitehead, I.M. (1981) Dose-responses for Colletotrichum lindemuthianum elicitor-mediated enzyme induction in French bean cell suspension cultures. Planta, 151, 272-280.
15. Fujioka, S., Noguchi, T., Watanabe, T., Takatsuto, S. and Yoshida, S. (2000) Biosynthesis of brassinosteroids in cultured cells of Catharanthus roseus. Phytochemistry, 53, 549-553.
16. Fulcheri, C., Morard, P. and Henry, M. (1998) Stimulation of the growth and the triterpenoid saponin accumulation of Saponaria officinalis cell and Gypsophila paniculata root suspension cultures by improvement of the mineral composition of the media. J. Agric. Food Chem. 46, 2055-2061.
17. Gundlach, H., Müller, M.J., Kutchan, T.M. and Zenk, M.H. (1992) Jasmonic acid is a signal transducer in elicitor-induced plant cell cultures. Proc. Natl Acad. Sci. USA, 89, 2389-2393.
18. Haralampidis, K., Bryan, G., Qi, X., Papadopoulou, K., Bakht, S., Melton, R. and Osbourn, A. (2001) A new class of oxidosqualene cyclase directs synthesis of antimicrobial phytoprotectants in monocots. Proc. Natl Acad. Sci. USA, 98, 13431-13436.
19. Haridas, V., Higuchi, M., Jayatilake, G.S., Bailey, D., Mujoo, K., Blake, M.E., Arntzen, C.J. and Gutterman, J.U. (2001) Avicins: triterpenoid saponins from Acacia victoriae (Bentham) induce apoptosis by mitochondrial perturbation. Proc. Natl Acad. Sci. USA, 98, 5821-5826.
20. Hayashi, H., Hiraoka, N., Ikeshiro, Y., Kushiro, T., Morita, M., Shibuya, M. and Ebizuka, Y. (2000) Molecular cloning and characterization of a cDNA for Glycyrrhiza glabra cycloartenol synthase. Biol. Pharm. Bull. 23, 231-234.
21. Herold, M.C. and Henry, M. (2001) UDP-glucuronosyltransferase activity is correlated to saponin production in Gypsophila paniculata root in vitro cultures. Biotechnol. Lett. 23, 335-337.
22. Herrera, J.B., Bartel, B., Wilson, W.K. and Matsuda, S.P. (1998) Cloning and characterization of the Arabidopsis thaliana lupeol synthase gene. Phytochemistry, 49, 1905-1911.
23. Huhman, D.V. and Sumner, L.W. (2002) Metabolic profiling of saponin glycosides in Medicago sativa and Medicago truncatula using HPLC coupled to an electrospray ion-trap mass spectrometer. Phytochemistry, 59, 347-360.
24. Husselstein-Muller, T., Schaller, H. and Benveniste, P. (2001) Molecular cloning and expression in yeast of 2,3-oxidosqualene-triterpenoid cyclases from Arabidopsis thaliana. Plant Mol Biol. 45, 75-92.
25. Jandrositz, A., Turnowsky, F. and Hogenauer, G. (1991) The gene encoding squalene epoxidase from Saccharomyces cerevisiae: cloning and characterization. Gene, 107, 155-160.
26. Jones, M. and Elliott, F.C. (1969) Two rapid assays for saponin in individual alfalfa plants. Crop Sci. 9, 688-691.
27. Korth, K.L. and Dixon, R.A. (1997) Evidence for chewing insect-specific molecular events distinct from a general wound response in leaves. Plant Physiol. 115, 1299-1305.
28. Kribii, R., Arro, M., Del Arco, A., Gonzalez, V., Balcells, L., Delourme, D., Ferrer, A., Karst, F. and Boronat, A. (1997) Cloning and characterization of the Arabidopsis thaliana SQS1 gene encoding squalene synthase - involvement of the C-terminal region of the enzyme in the channeling of squalene through the sterol pathway. Eur. J. Biochem. 249, 61-69.
29. Kushiro, T., Shibuya, M. and Ebizuka, Y. (1998) β-Amyrin synthase: cloning of oxidosqualene cyclase that catalyzes the formation of the most popular triterpene among higher plants. Eur. J. Biochem. 256, 238-244.
30. Kushiro, T., Shibuya, M., Masuda, K. and Ebizuka, Y. (2000) A novel multifunctional triterpene synthase from Arabidopsis thaliana. Tetrahedron Lett. 41, 7705-7710.
31. Laden, B.P., Tang, Y. and Porter, T.D. (2000) Cloning, heterologous expression, and enzymological characterization of human squalene monooxygenase. Arch. Biochem. Biophys. 374, 381-388.
32. Landl, K.M., Klosch, B. and Turnowsky, F. (1996) ERG1, encoding squalene epoxidase, is located on the right arm of chromosome VII of Saccharomyces cerevisiae. Yeast, 12, 609-613.
33. Leber, R., Landl, K., Zinser, E., Ahorn, H., Spok, A., Kohlwein, S.D., Turnowsky, F. and Daum, G. (1998) Dual locaLization of squalene epoxidase, Erg1p, in yeast reflects a relationship between the endoplasmic reticulum and lipid particles. Mol. Biol. Cell. 9, 375-386.
34. Lee, H.K., Denner-Ancona, P., Sakakibara, J., Ono, T. and Prestwich, G.D. (2000) Photoaffinity labeling and site-directed mutagenesis of rat squalene epoxidase. Arch. Biochem. Biophys. 381, 43-52.
35. Marciani, D.J., Press, J.B., Reynolds, R.C., Pathak, A.K., Pathak, V., Gundy, L.E., Farmer, J.T., Koratich, M.S. and May, R.D. (2000) Development of semisynthetic triterpenoid saponin derivatives with immune stimulating activity. Vaccine, 18, 3141-3151.
36. Massiot, G., Lavaud, C., Le Men-Olivier, L., Van Binst, G., Miller, S.P.F. and Fales, H.M. (1988) Structural elucidation of alfalfa root saponins by mass spectrometry and nuclear magnetic resonance analysis. J. Chem. Soc. Perkin Trans. 1, 3071-3079.
37. McConn, M., Creelman, R.A., Bell, E., Mullet, J.E. and Browse, J. (1997) Jasmonate is essential for insect defense in Arabidopsis. Proc. Natl Acad. Sci. USA, 94, 5473-5477.
38. Memelink, J., Verpoorte, R. and Kijne, J.W. (2001) ORCAnization of jasmonate-responsive gene expression in alkaloid metabolism. Trends Plant Sci. 6, 212-219.
39. Morita, M., Shibuya, M., Kushiro, T., Masuda, K. and Ebizuka, Y. (2000) Molecular cloning and functional expression of triterpene synthases from pea (Pisum sativum). New alpha-amyrin-producing enzyme is a multifunctional triterpene synthase. Eur. J. Biochem. 267, 3453-3460.
40. Morita, M., Shibuya, M., Lee, M.S., Sankawa, U. and Ebizuka, Y. (1997) Molecular cloning of pea cDNA encoding cycloartenol synthase and its functional expression in yeast. Biol. Pharm. Bull. 20, 770-775.
41. Nagata, T., Tsushida, T., Hamaya, E., Enoki, N., Manabe, S. and Nishino, C. (1985) Camellidins, antifugal saponins isolated from Camellia japonica. Agric. Biol. Chem. 49, 1181-1186.
42. Nakashima, T., Inoue, T., Oka, A., Nishino, T., Osumi, T. and Hata, S. (1995) Cloning, expression, and characterization of cDNAs encoding Arabidopsis thaliana squalene synthase. Proc. Natl Acad. Sci. USA, 92, 2328-2332.
43. Noguchi, T., Fujioka, S., Choe, S., Takatsuto, S., Tax, F.E., Yoshida, S. and Feldmann, K.A. (2000) Biosynthetic pathways of brassinolide in Arabidopsis. Plant Physiol. 124, 201-209.
44. Oleszek, W. (1988) Solid phase extraction-fractionation of alfalfa saponins. J. Sci. Food Agric. 44, 43-49.
45. Oleszek, W. (1997) Alfalfa saponins: structure, biological activity, and chemotaxonomy. In Saponins Used in Food and Agriculture (Waller, G. and Yamasaki, K., eds). New York: Plenum Press, pp. 155-170.
46. Oleszek, W., Junkuszew, M. and Stochmal, A. (1999) Determination and toxicity of saponins from Amaranthus cruentus seeds. J. Agric. Food Chem. 47, 3685-3687.
47. Oleszek, W. and Jurzysta, M. (1990) High-performance liquid chromatography of alfalfa root saponins. J. Chromatog. 519, 109-116.
48. Oleszek, W., Jurzysta, M., Ploszynski, M., Colquhoun, I.J., Price, K.R. and Fenwick, G.R. (1992) Zahnic acid tridesmoside and other dominant saponins from alfalfa (Medicago sativa L.) aerial parts. J. Agric. Food Chem. 40, 191-196.
49. Oleszek, W., Price, K.R., Colquhoun, I.J., Jurzysta, M., Ploszynski, M. and Fenwick, G.R. (1990) Isolation and identification of alfalfa (Medicago sativa L.) root saponins: their activity in relation to a fungal bioassay. J. Agric. Food. Chem. 38, 1810-1817.
50. Ono, T. and Bloch, K. (1975) Solubilization and partial characterization of rat liver squalene epoxidase. J. Biol. Chem. 250, 1571-1579.
51. Osbourn, A. (1996) Saponins and plant defence - a soap story. Trends Plant Sci. 1, 4-9.
52. Pandit, J., Danley, D.E., Schulte, G.K., Mazzalupo, S., Pauly, T.A., Hayward, C.M., Hamanaka, E.S., Thompson, J.F. and Harwood, H.J., Jr (2000) Crystal structure of human squalene synthase. J. Biol. Chem. 275, 30610-30617.
53. Papadopoulou, K., Melton, R.E., Leggett, M., Daniels, M.J. and Osbourn, A.E. (1999) Compromised disease resistance in saponin-deficient plants. Proc. Natl Acad. Sci. USA, 96, 12923-12928.
54. Park, H.J., Kwon, S.H., Lee, J.H., Lee, K.H., Miyamoto, K. and Lee, K.T. (2001) Kalopanaxsaponin A is a basic saponin structure for the anti-tumor activity of hederagenin monodesmosides. Planta Med. 67, 118-121.
55. Pedersen, M.W., Barnes, D.K., Sorensen, E.L. et al. (1976) Effects of low and high saponin selection in alfalfa on agronomic and pest resistance traits and the interrelationship of these traits. Crop Sci. 16, 193-199.
56. Pracros, P. (1988) Mesure de l'activité des saponins de la luzerne pas les larves du ver de farine: Tenebrio molitor L. (Coléoptère, Tenebrionidae). II. Recherche des fractions de saponins responsables des effects antinutritionnels observés. Agronomie, 8, 793-799.
57. Quackenbush, J., Liang, F., Holt, I., Pertea, G. and Upton, J. (2000) The TIGR gene indices: reconstruction and representation of expressed gene sequences. Nucl. Acids Res. 28, 141-145.
58. Sakakibara, J., Watanabe, R., Kanai, Y. and Ono, T. (1995) Molecular cloning and expression of rat squalene epoxidase. J. Biol. Chem. 270, 17-20.
59. Sambrook, J., Fritsch, E.F. and Maniatis, T. (1989) Molecular Cloning: a Laboratory Manual. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
60. Schäfer, U.A., Reed, D.W., Hunter, D.G., Yao, K., Weninger, A.M., Tsang, E.W.T., Reaney, M.J.T., MacKenzie, S.L. and Covello, P.S. (1999) An example of intron junctional sliding in the gene families encoding squalene monooxygenase homologues in Arabidopsis thaliana and Brassica napus. Plant Mol. Biol. 39, 721-728.
61. Segura, M.J.R., Meyer, M.M. and Matsuda, S.P.T. (2000) Arabidopsis thaliana LUP1 converts oxidosqualene to multiple triterpene alcohols and a triterpene diol. Org. Lett. 2, 2257-2259.
62. Shibata, N., Arita, M., Misaki, Y., Dohmae, N., Takio, K., Ono, T. and Inoue, K (2001) Supernatant protein factor, which stimulates the conversion of squalene to lanosterol, is a cytosolic squalene transfer protein and enhances cholesterol biosynthesis. Proc. Natl Acad. Sci. USA, 98, 2244-2249.
63. Small, E. (1996) Adaptations to herbivory in alfalfa (Medicago sativa). Can. J. Bot. 74, 807-822.
64. Tava, A. and Odoardi, M. (1997) Saponins from Medicago spp: chemical characterization and biological activity against insects. In Saponins Used in Food and Agriculture (Waller, G. and Yamasaki, K., eds). New York: Plenum Press, pp. 97-109.
65. Tava, A., Oleszek, W., Jurzysta, M., Berardo, N. and Odoardi, M. (1993) Alfalfa saponins and sapogenins: isolation and quantification in two different cultivars. Phytochem. Anal. 4, 269-274.
66. Vögeli, U. and Chappell, J. (1988) Induction of sesquiterpene cyclase and suppression of squalene synthetase activities in plant cell cultures treated with fungal elicitor. Plant Physiol. 88, 1291-1296.
67. Vogt, T. and Jones, P. (2000) Glycosyltransferases in plant natural product synthesis: characterization of a supergene family. Trends Plant Sci. 5, 380-386.
68. Waller, G.R., Jurzysta, M. and Thorne, R.L.Z. (1993) Allelopathic activity of root saponins from alfalfa (Medicago sativa L.) on weeds and wheat. Bot. Bull. Acad. Sin. 34, 1-11.
69. Yamamoto, S. and Bloch, K. (1970) Studies on squalene epoxidase of rat liver. J. Biol. Chem. 245, 7-16.