The ancient CYP716 family is a major contributor to the diversification of eudicot triterpenoid biosynthesis

Nature Communications

Volumn 8, Issue , 2017, Pages

  Miettinen, Karel ^a,b   Pollier, Jacob ^a,b   Buyst, Dieter ^b   Arendt, Philipp ^a,b,c   Csuk, René ^d   Sommerwerk, Sven ^d   Moses, Tessa ^a,b   Mertens, Jan ^a,b   Sonawane, Prashant D ^e   Pauwels, Laurens ^a,b   Aharoni, Asaph ^e   Martins, José ^b   Nelson, David R ^f   Goossens, Alain ^a,b  

^a Department of Plant Systems Biology ^*  (Belgium)

^b GHENT UNIVERSITY   (Belgium)

^c DEPARTMENT OF PLANT SYSTEMS BIOLOGY   (Belgium)

^d MARTIN LUTHER UNIVERSITY HALLE WITTENBERG   (Germany)

^e WEIZMANN INSTITUTE OF SCIENCE   (Israel)

^f UNIVERSITY OF TENNESSEE HEALTH SCIENCE CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOCHROME P450; CYTOCHROME P450 716; TRITERPENOID; UNCLASSIFIED DRUG; PLANT PROTEIN; TRITERPENE;

BIOACTIVITY; DICOTYLEDON; ENZYME ACTIVITY; GENE EXPRESSION; MEDICINAL PLANT; OXIDATION; PHYLOGENETICS; PLANT DEFENSE; PROTEIN; TERPENE; YEAST;

ARTICLE; BIOSYNTHESIS; CYCLIZATION; EUDICOT; HETEROLOGOUS EXPRESSION; MOLECULAR EVOLUTION; NONHUMAN; OXIDATION; PHYLOGENY; PROTEIN FAMILY; SYNTHETIC BIOLOGY; YEAST; BIODIVERSITY; GENETICS; METABOLISM; PLANT PHYSIOLOGY;

BIODIVERSITY; CYTOCHROME P-450 ENZYME SYSTEM; EVOLUTION, MOLECULAR; PHYLOGENY; PLANT PHYSIOLOGICAL PHENOMENA; PLANT PROTEINS; TRITERPENES;

EID: 85011693539     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms14153     Document Type: Article

References (56)

1. Thimmappa, R., Geisler, K., Louveau, T., O'Maille, P., Osbourn, A. Triterpene biosynthesis in plants. Annu. Rev. Plant Biol. 65, 225-257 (2014).
2. Moses, T., Papadopoulou, K. K., Osbourn, A. Metabolic and functional diversity of saponins, biosynthetic intermediates and semi-synthetic derivatives. Crit. Rev. Biochem. Mol. Biol. 49, 439-462 (2014).
3. Seki, H., Tamura, K., Muranaka, T. P450s and UGTs: key players in the structural diversity of triterpenoid saponins. Plant Cell Physiol. 56, 1463-1471 (2015).
4. Vincken, J. P., Heng, L., de Groot, A., Gruppen, H. Saponins, classification and occurrence in the plant kingdom. Phytochemistry 68, 275-297 (2007).
5. Moses, T., Pollier, J., Thevelein, J. M., Goossens, A. Bioengineering of plant (tri)terpenoids: from metabolic engineering of plants to synthetic biology in vivo and in vitro. New Phytol. 200, 27-43 (2013).
6. Shang, Y., et al. Plant science. Biosynthesis, regulation, and domestication of bitterness in cucumber. Science 346, 1084-1088 (2014).
7. Biazzi, E., et al. CYP72A67 catalyzes a key oxidative step in Medicago truncatula hemolytic saponin biosynthesis. Mol. Plant 8, 1493-1506 (2015).
8. Boutanaev, A. M., et al. Investigation of terpene diversification across multiple sequenced plant genomes. Proc. Natl Acad. Sci. USA 112, E81-E88 (2015).
9. Khakimov, B., et al. Identification and genome organization of saponin pathway genes from a wild crucifer, and their use for transient production of saponins in Nicotiana benthamiana. Plant J. 84, 478-490 (2015).
10. Moses, T., et al. Unraveling the triterpenoid saponin biosynthesis of the African shrub Maesa lanceolata. Mol. Plant 8, 122-135 (2015).
11. Moses, T., et al. OSC2 and CYP716A14v2 catalyze the biosynthesis of triterpenoids for the cuticle of aerial organs of Artemisia annua. Plant Cell 27, 286-301 (2015).
12. Yasumoto, S., Fukushima, E. O., Seki, H., Muranaka, T. Novel triterpene oxidizing activity of Arabidopsis thaliana CYP716A subfamily enzymes. FEBS Lett. 590, 533-540 (2016).
13. Zhang, J., et al. Oxidation of cucurbitadienol catalyzed by CYP87D18 in the biosynthesis of Mogrosides from Siraitia grosvenorii. Plant Cell Physiol. 57, 1000-1007 (2016).
14. Hamberger, B., Bak, S. Plant P450s as versatile drivers for evolution of species-specific chemical diversity. Phil. Trans. R. Soc. Lond. B Biol. Sci. 368, 20120426 (2013).
15. Nelson, D., Werck-Reichhart, D. A P450-centric view of plant evolution. Plant J. 66, 194-211 (2011).
16. Fukushima, E. O., et al. CYP716A subfamily members are multifunctional oxidases in triterpenoid biosynthesis. Plant Cell Physiol. 52, 2050-2061 (2011).
17. Han, J. Y., Hwang, H. S., Choi, S. W., Kim, H. J., Choi, Y. E. Cytochrome P450 CYP716A53v2 catalyzes the formation of protopanaxatriol from protopanaxadiol during ginsenoside biosynthesis in Panax ginseng. Plant Cell Physiol. 53, 1535-1545 (2012).
18. Han, J. Y., Kim, H. J., Kwon, Y. S., Choi, Y. E. The Cyt P450 enzyme CYP716A47 catalyzes the formation of protopanaxadiol from dammarenediol-II during ginsenoside biosynthesis in Panax ginseng. Plant Cell Physiol. 52, 2062-2073 (2011).
19. Moses, T., et al. Combinatorial biosynthesis of sapogenins and saponins in Saccharomyces cerevisiae using a C-16alpha hydroxylase from Bupleurum falcatum. Proc. Natl Acad. Sci. USA 111, 1634-1639 (2014).
20. Huang, L., et al. Molecular characterization of the pentacyclic triterpenoid biosynthetic pathway in Catharanthus roseus. Planta 236, 1571-1581 (2012).
21. The Angiosperm Phylogeny Group. An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants: APG III. Bot. J. Linnean Soc. 161, 105-121 (2009).
22. Bylka, W., Znajdek-Awizen, P., Studzinska-Sroka, E., Danczak-Pazdrowska, A., Brzezinska, M. Centella asiatica in dermatology: an overview. Phytother. Res. 28, 1117-1124 (2014).
23. James, J. T., Dubery, I. A. Pentacyclic triterpenoids from the medicinal herb, Centella asiatica (L.) Urban. Molecules 14, 3922-3941 (2009).
24. Xiao, M., et al. Transcriptome analysis based on next-generation sequencing of non-model plants producing specialized metabolites of biotechnological interest. J. Biotechnol. 166, 122-134 (2013).
25. Hayashi, H., et al. Cloning and characterization of a cDNA encoding beta-amyrin synthase involved in glycyrrhizin and soyasaponin biosyntheses in licorice. Biol. Pharm. Bull. 24, 912-916 (2001).
26. Carelli, M., et al. Medicago truncatula CYP716A12 is a multifunctional oxidase involved in the biosynthesis of hemolytic saponins. Plant Cell 23, 3070-3081 (2011).
27. Weng, X. X., et al. Two new dammarane monodesmosides from Centella asiatica. J. Asian Nat. Products Res. 13, 749-755 (2011).
28. Zhang, L., et al. Platycodon grandiflorus-an ethnopharmacological, phytochemical and pharmacological review. J. Ethnopharmacol. 164, 147-161 (2015).
29. Csuk, R., Siewert, B. A convenient separation of ursolic and oleanolic acid. Tetrahedron Lett. 52, 6616-6618 (2011).
30. Zhang, L., Liu, Z. H., Tian, J. K. Cytotoxic triterpenoid saponins from the roots of Platycodon grandiflorum. Molecules 12, 832-841 (2007).
31. Nishida, M., Yoshimitsu, H., Okawa, M., Nohara, T. Four new cycloartane glycosides from Aquilegia vulgaris. Chem. Pharm. Bull. 51, 956-959 (2003).
32. Nishida, M., Yoshimitsu, H., Okawa, M., Nohara, T. Four new cycloartane glycosides from Aquilegia vulgaris and their immunosuppressive activities in mouse allogeneic mixed lymphocyte reaction. Chem. Pharm. Bull. 51, 683-687 (2003).
33. Yoshimitsu, H., Nishida, M., Nohara, T. Two new cycloartane glycosides from the underground parts of Aquilegia vulgaris. Chem. Pharm. Bull. 56, 1625-1627 (2008).
34. Yoshimitsu, H., Nishidas, M., Hashimoto, F., Nohara, T. Cycloartane-type glycosides from Aquilegia flabellata. Phytochemistry 51, 449-452 (1999).
35. Gas-Pascual, E., Berna, A., Bach, T. J., Schaller, H. Plant oxidosqualene metabolism: cycloartenol synthase-dependent sterol biosynthesis in Nicotiana benthamiana. PLoS ONE 9, e109156 (2014).
36. Matasci, N., et al. Data access for the 1, 000 Plants (1KP) project. GigaScience 3, 17 (2014).
37. Proost, S., et al. PLAZA 3.0: an access point for plant comparative genomics. Nucleic Acids Res. 43, D974-D981 (2015).
38. Seki, H., et al. Licorice beta-amyrin 11-oxidase, a cytochrome P450 with a key role in the biosynthesis of the triterpene sweetener glycyrrhizin. Proc. Natl Acad. Sci. USA 105, 14204-14209 (2008).
39. Han, J. Y., Kim, M. J., Ban, Y. W., Hwang, H. S., Choi, Y. E. The involvement of beta-amyrin 28-oxidase (CYP716A52v2) in oleanane-type ginsenoside biosynthesis in Panax ginseng. Plant Cell Physiol. 54, 2034-2046 (2013).
40. Qi, X., et al. A different function for a member of an ancient and highly conserved cytochrome P450 family: from essential sterols to plant defense. Proc. Natl Acad. Sci. USA 103, 18848-18853 (2006).
41. Geisler, K., et al. Biochemical analysis of a multifunctional cytochrome P450 (CYP51) enzyme required for synthesis of antimicrobial triterpenes in plants. Proc. Natl Acad. Sci. USA 110, E3360-E3367 (2013).
42. Seki, H., et al. Triterpene functional genomics in licorice for identification of CYP72A154 involved in the biosynthesis of glycyrrhizin. Plant Cell 23, 4112-4123 (2011).
43. Phillips, D. R., Rasbery, J. M., Bartel, B., Matsuda, S. P. Biosynthetic diversity in plant triterpene cyclization. Curr. Opin. Plant Biol. 9, 305-314 (2006).
44. Xue, Z., et al. Divergent evolution of oxidosqualene cyclases in plants. New Phytol. 193, 1022-1038 (2012).
45. Marquina, S., Bonilla-Barbosa, J., Alvarez, L. Comparative phytochemical analysis of four Mexican Nymphaea species. Phytochemistry 66, 921-927 (2005).
46. Weng, J. K., Noel, J. P. Chemodiversity in Selaginella: a reference system for parallel and convergent metabolic evolution in terrestrial plants. Front. Plant Sci. 4, 119 (2013).
47. Otto, A., Wilde, V. Sesqui-, Di-, and triterpenoids as chemosystematic markers in extant conifers-a review. Bot. Rev. 67, 141-238 (2001).
48. Fukushima, E. O., et al. Combinatorial biosynthesis of legume natural and rare triterpenoids in engineered yeast. Plant Cell Physiol. 54, 740-749 (2013).
49. Pollier, J., Moses, T., Goossens, A. Combinatorial biosynthesis in plants: a (p)review on its potential and future exploitation. Nat. Product Rep. 28, 1897-1916 (2011).
50. Edwards, K., Johnstone, C., Thompson, C. A simple and rapid method for the preparation of plant genomic DNA for PCR analysis. Nucleic Acids Res. 19, 1349 (1991).
51. Alberti, S., Gitler, A. D., Lindquist, S. A suite of Gateway cloning vectors for high-throughput genetic analysis in Saccharomyces cerevisiae. Yeast 24, 913-919 (2007).
52. DiCarlo, J. E., et al. Genome engineering in Saccharomyces cerevisiae using CRISPR-Cas systems. Nucleic Acids Res. 41, 4336-4343 (2013).
53. Moses, T., Thevelein, J. M., Goossens, A., Pollier, J. Comparative analysis of CYP93E proteins for improved microbial synthesis of plant triterpenoids. Phytochemistry 108, 47-56 (2014).
54. Edgar, R. C. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32, 1792-1797 (2004).
55. Abascal, F., Zardoya, R., Posada, D. ProtTest: selection of best-fit models of protein evolution. Bioinformatics 21, 2104-2105 (2005).
56. Tamura, K., et al. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol. Biol. Evol. 28, 2731-2739 (2011).