Unraveling the triterpenoid saponin biosynthesis of the african shrub maesa lanceolata

Molecular Plant

Volumn 8, Issue 1, 2015, Pages 122-135

  Moses, Tessa ^a,b,c   Pollier, Jacob ^a,b   Faizal, Ahmad ^b   Apers, Sandra ^d   Pieters, Luc ^d   Thevelein, Johan M ^a,c   Geelen, Danny ^b   Goossens, Alain ^a,b  

^a DEPARTMENT OF PLANT SYSTEMS BIOLOGY   (Belgium)

^b GHENT UNIVERSITY   (Belgium)

^c UNIVERSITY OF LEUVEN   (Belgium)

^d UNIVERSITY OF ANTWERP   (Belgium)

Author keywords

C 16a oxidase; C 28 oxidase; cytochrome P450; Maesa lanceolata; oxidosqualene cyclase; triterpenoid saponin

Indexed keywords

MAESA LANCEOLATA; MEDICAGO TRUNCATULA; SACCHAROMYCES CEREVISIAE;

CYTOCHROME P450; LANOSTEROL SYNTHASE; MUTASE; OXIDOREDUCTASE; SAPONIN; TRITERPENE;

BIOSYNTHESIS; ENZYMOLOGY; METABOLISM; MOLECULAR GENETICS; PRIMULACEAE;

CYTOCHROME P-450 ENZYME SYSTEM; INTRAMOLECULAR TRANSFERASES; MOLECULAR SEQUENCE DATA; MYRSINACEAE; OXIDOREDUCTASES; SAPONINS; TRITERPENES;

EID: 84922980653     PISSN: 16742052     EISSN: 17529867     Source Type: Journal    
DOI: 10.1016/j.molp.2014.11.004     Document Type: Article

References (52)

1. S. Alberti, A.D. Gitler, and S. Lindquist A suite of Gateway cloning vectors for high-throughput genetic analysis in Saccharomyces cerevisiae Yeast 24 2007 913 919
2. S. Apers, A. Foriers, J.B. Sindambiwe, A. Vlietinck, and L. Pieters Separation of a triterpenoid saponin mixture from Maesa lanceolata: semipreparative reversed-phase wide pore high performance liquid chromatography with temperature control J. Pharm. Biomed. Anal. 18 1998 737 743
3. J.M. Augustin, V. Kuzina, S.B. Andersen, and S. Bak Molecular activities, biosynthesis and evolution of triterpenoid saponins Phytochemistry 72 2011 435 457
4. S. Bak, F. Beisson, G. Bishop, B. Hamberger, R. Höfer, S. Paquette, and D. Werck-Reichhart Cytochromes P450 Arabidopsis Book 2011 e0144
5. M. Carelli, E. Biazzi, F. Panara, A. Tava, L. Scaramelli, A. Porceddu, N. Graham, M. Odoardi, E. Piano, and S. Arcioni Medicago truncatula CYP716A12 is a multifunctional oxidase involved in the biosynthesis of hemolytic saponins Plant Cell 23 2011 3070 3081
6. C. Chaban, F. Waller, M. Furuya, and P. Nick Auxin responsiveness of a novel cytochrome p450 in rice coleoptiles Plant Physiol. 133 2003 2000 2009
7. P. De Felipe, G.A. Luke, L.E. Hughes, D. Gani, C. Halpin, and M.D. Ryan E unum pluribus: multiple proteins from a self-processing polyprotein Trends Biotechnol. 24 2006 68 75
8. N. De Geyter, A. Gholami, S. Goormachtig, and A. Goossens Transcriptional machineries in jasmonate-elicited plant secondary metabolism Trends Plant Sci. 17 2012 349 359
9. A. Faizal Modulation of saponin production in medicinal Maesa spp PhD thesis 2013 Ghent University Belgium Available online at http://lib.ugent.be/catalog/pug01:3191661
10. A. Faizal, and D. Geelen Agroinfiltration of intact leaves as a method for the transient and stable transformation of saponin producing Maesa lanceolata Plant Cell Rep. 31 2012 1517 1526
11. A. Faizal, E. Lambert, K. Foubert, S. Apers, and D. Geelen In vitro propagation of four saponin producing Maesa species Plant Cell Tiss. Org. Cult. 106 2011 215 223
12. K. Foubert, F. Cuyckens, K. Vleeschouwer, M. Theunis, A. Vlietinck, L. Pieters, and S. Apers Rapid quantification of 14 saponins of Maesa lanceolata by UPLC-MS/MS Talanta 81 2010 1258 1263
13. E.O. Fukushima, H. Seki, K. Ohyama, E. Ono, N. Umemoto, M. Mizutani, K. Saito, and T. Muranaka CYP716A subfamily members are multifunctional oxidases in triterpenoid biosynthesis Plant Cell Physiol. 52 2011 2050 2061
14. E.O. Fukushima, H. Seki, S. Sawai, M. Suzuki, K. Ohyama, K. Saito, and T. Muranaka Combinatorial biosynthesis of legume natural and rare triterpenoids in engineered yeast Plant Cell Physiol. 54 2013 740 749
15. K. Geisler, R.K. Hughes, F. Sainsbury, G.P. Lomonossoff, M. Rejzek, S. Fairhurst, C.E. Olsen, M.S. Motawia, R.E. Melton, and A.M. Hemmings Biochemical analysis of a multifunctional cytochrome P450 (CYP51) enzyme required for synthesis of antimicrobial triterpenes in plants Proc. Natl. Acad. Sci. U S A 110 2013 E3360 3367
16. S.K. Guttikonda, J. Trupti, N.C. Bisht, H. Chen, Y.Q. An, S. Pandey, D. Xu, and O. Yu Whole genome co-expression analysis of soybean cytochrome P450 genes identifies nodulation-specific P450 monooxygenases BMC Plant Biol. 10 2010 243
17. J.Y. Han, M.J. Kim, Y.W. Ban, H.S. Hwang, and Y.E. Choi The involvement of β-amyrin 28-oxidase (CYP716A52v2) in oleanane-type ginsenoside biosynthesis in Panax ginseng Plant Cell Physiol. 54 2013 2034 2046
18. H. Hayashi, P. Huang, A. Kirakosyan, K. Inoue, N. Hiraoka, Y. Ikeshiro, T. Kushiro, M. Shibuya, and Y. Ebizuka Cloning and characterization of a cDNA encoding beta-amyrin synthase involved in glycyrrhizin and soyasaponin biosyntheses in licorice Biol. Pharm. Bull. 24 2001 912 916
19. L. Huang, J. Li, H. Ye, C. Li, H. Wang, B. Liu, and Y. Zhang Molecular characterization of the pentacyclic triterpenoid biosynthetic pathway in Catharanthus roseus Planta 236 2012 1571 1581
20. M. Karimi, A. Bleys, R. Vanderhaeghen, and P. Hilson Building blocks for plant gene assembly Plant Physiol. 145 2007 1183 1191
21. M. Karimi, D. Inzé, and A. Depicker GATEWAY vectors for Agrobacterium-mediated plant transformation Trends Plant Sci. 7 2002 193 195
22. J. Kirby, D.W. Romanini, E.M. Paradise, and J.D. Keasling Engineering triterpene production in Saccharomyces cerevisiae-beta-amyrin synthase from Artemisia annua FEBS J. 275 2008 1852 1859
23. M. Kunii, Y. Kitahama, E.O. Fukushima, H. Seki, T. Muranaka, Y. Yoshida, and Y. Aoyama β-Amyrin oxidation by oat CYP51H10 expressed heterologously in yeast cells: the first example of CYP51-dependent metabolism other than the 14-demethylation of sterol precursors Biol. Pharm. Bull. 35 2012 801 804
24. T. Kushiro, M. Shibuya, K. Masuda, and Y. Ebizuka Mutational studies on triterpene synthases: engineering lupeol synthase into β-amyrin synthase J. Am. Chem. Soc. 122 2000 6816 6824
25. M.A. Larkin, G. Blackshields, N.P. Brown, R. Chenna, P.A. McGettigan, H. McWilliam, F. Valentin, I.M. Wallace, A. Wilm, and R. Lopez Clustal W and Clustal X version 2.0 Bioinformatics 23 2007 2947 2948
26. L.O.A. Manguro, J.O. Midiwo, L.F. Tietze, and P. Hao Triterpene saponins of Maesa lanceolata leaves ARKIVOC ii 2011 172 198
27. D. Meesapyodsuk, J. Balsevich, D.W. Reed, and P.S. Covello Saponin biosynthesis in Saponaria vaccaria. CDNAs encoding beta-amyrin synthase and a triterpene carboxylic acid glucosyltransferase Plant Physiol. 143 2007 959 969
28. T. Moses, K.K. Papadopoulou, and A. Osbourn Metabolic and functional diversity of saponins, biosynthetic intermediates and semi-synthetic derivatives Crit. Rev. Biochem. Mol. Biol. 49 2014 439 462
29. T. Moses, J. Pollier, L. Almagro, D. Buyst, M. Van Montagu, M.A. Pedreño, J.C. Martins, J.M. Thevelein, and A. Goossens Combinatorial biosynthesis of sapogenins and saponins in Saccharomyces cerevisiae using a C-16α hydroxylase from Bupleurum falcatum Proc. Natl. Acad. Sci. U S A 111 2014 1634 1639
30. T. Moses, J. Pollier, J.M. Thevelein, and A. Goossens Bioengineering of plant terpenoids: from metabolic engineering of plants to synthetic biology in vivo and in vitro New Phytol. 200 2013 27 43
31. D. Nelson, and D. Werck-Reichhart A P450-centric view of plant evolution Plant J. 66 2011 194 211
32. D.R. Nelson, R. Ming, M. Alam, and M.A. Schuler Comparison of cytochrome P450 genes from six plant genomes Trop. Plant Biol. 1 2008 216 235
33. A. Osbourn, R.J.M. Goss, and R.A. Field The saponins - polar isoprenoids with important and diverse biological activities Nat. Prod. Rep. 28 2011 1261 1268
34. L. Pauwels, D. Inzé, and A. Goossens Jasmonate-inducible gene: what does it mean? Trends Plant Sci. 14 2009 87 91
35. J. Pollier, M. González-Guzmán, W. Ardiles-Diaz, D. Geelen, and A. Goossens An integrated PCR colony hybridization approach to screen cDNA libraries for full-length coding sequences PLoS ONE 6 2011 e24978
36. J. Pollier, K. Morreel, D. Geelen, and A. Goossens Metabolite profiling of triterpene saponins in Medicago truncatula hairy roots by liquid chromatography Fourier transform ion cyclotron resonance mass spectrometry J. Nat. Prod. 74 2011 1462 1476
37. J. Pollier, T. Moses, and A. Goossens Combinatorial biosynthesis in plants: a (p)review on its potential and future exploitation Nat. Prod. Rep. 28 2011 1897 1916
38. K. Poralla The possible role of a repetitive amino acid motif in evolution of triterpenoid cyclases Bioorg. Med. Chem. Lett. 4 1994 285 290
39. H. Rischer, M. Orešič, T. Seppänen-Laakso, M. Katajamaa, F. Lammertyn, W. Ardiles-Diaz, M.C. Van Montagu, D. Inzé, K.M. Oksman-Caldentey, and A. Goossens Gene-to-metabolite networks for terpenoid indole alkaloid biosynthesis in Catharanthus roseus cells Proc. Natl. Acad. Sci. U S A 103 2006 5614 5619
40. M.A. Schuler, and D. Werck-Reichhart Functional genomics of P450s Annu. Rev. Plant Biol. 54 2003 629 667
41. H. Seki, S. Sawai, K. Ohyama, M. Mizutani, T. Ohnishi, H. Sudo, E.O. Fukushima, T. Akashi, T. Aoki, and K. Saito Triterpene functional genomics in licorice for identification of CYP72A154 involved in the biosynthesis of glycyrrhizin Plant Cell 23 2011 4112 4123
42. J.B. Sindambiwe, M. Calomme, S. Geerts, L. Pieters, A.J. Vlietinck, and D.A. Vanden Berghe Evaluation of biological activities of triterpenoid saponins from Maesa lanceolata J. Nat. Prod. 61 1998 585 590
43. C.A. Smith, E.J. Want, G. O'Maille, R. Abagyan, and G. Siuzdak XCMS: processing mass spectrometry data for metabolite profiling using nonlinear peak alignment, matching, and identification Anal. Chem. 78 2006 779 787
44. S.G. Sparg, M.E. Light, and J. van Staden Biological activities and distribution of plant saponins J. Ethnopharmacol. 94 2004 219 243
45. H. Suzuki, L. Achnine, R. Xu, S.P. Matsuda, and R.A. Dixon A genomics approach to the early stages of triterpene saponin biosynthesis in Medicago truncatula Plant J. 32 2002 1033 1048
46. K. Tamura, D. Peterson, N. Peterson, G. Stecher, M. Nei, and S. Kumar MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods Mol. Biol. Evol. 28 2011 2731 2739
47. M.H. Theunis, K. Foubert, J. Pollier, M. Gonzalez-Guzman, A. Goossens, A.J. Vlietinck, L.A. Pieters, and S. Apers Determination of saponins in Maesa lanceolata by LC-UV: development and validation Phytochemistry 68 2007 2825 2830
48. R. Thimmappa, K. Geisler, T. Louveau, P. O'Maille, and A. Osbourn Triterpene biosynthesis in plants Annu. Rev. Plant Biol. 65 2014 16.1 16.33
49. J.P. Vincken, L. Heng, A. De Groot, and H. Gruppen Saponins, classification and occurrence in the plant kingdom Phytochemistry 68 2007 275 297
50. M. Vuylsteke, J.D. Peleman, and M.J. van Eijk AFLP-based transcript profiling (cDNA-AFLP) for genome-wide expression analysis Nat. Protoc. 2 2007 1399 1413
51. R. Xu, G.C. Fazio, and S.P. Matsuda On the origins of triterpenoid skeletal diversity Phytochemistry 65 2004 261 291
52. Z. Xue, L. Duan, D. Liu, J. Guo, S. Ge, J. Dicks, P. ÓMáille, A. Osbourn, and X. Qi Divergent evolution of oxidosqualene cyclases in plants New Phytol. 193 2012 1022 1038