Identification and genome organization of saponin pathway genes from a wild crucifer, and their use for transient production of saponins in Nicotiana benthamiana

Plant Journal

Volumn 84, Issue 3, 2015, Pages 478-490

  Khakimov, Bekzod ^a   Kuzina, Vera ^a,f   Erthmann, Pernille Ø ^a   Fukushima, Ery Odette ^b   Augustin, Jörg M ^a   Olsen, Carl Erik ^a   Scholtalbers, Jelle ^c,d   Volpin, Hanne ^d,e   Andersen, Sven Bode ^a   Hauser, Thure P ^a   Muranaka, Toshiya ^b   Bak, Søren ^a  

^a UNIVERSITY OF COPENHAGEN   (Denmark)

^b OSAKA UNIVERSITY   (Japan)

^c EUROPEAN MOLECULAR BIOLOGY LABORATORY   (Germany)

^d KEYGENE N V   (Netherlands)

^e Danziger Innovations Limited   (Israel)

^f NONE   (Denmark)

Author keywords

Barbarea vulgaris; evolution; metabolic engineering; Nicotiana benthamiana; oxidosqualene cyclases; P450; synthetic biology; UDP glycosyltransferases

Indexed keywords

BIOCHEMISTRY; BIOSYNTHESIS; GENES; METABOLIC ENGINEERING; METABOLITES; SYNTHETIC BIOLOGY;

BARBAREA VULGARIS; EVOLUTION; GLYCOSYLTRANSFERASES; NICOTIANA BENTHAMIANA; OXIDOSQUALENE CYCLASES; P450;

PLANTS (BOTANY);

2,3-OXIDOSQUALENE-BETA-AMYRIN-CYCLASE; 3-O-OLEANOLIC ACID MONOGLUCOSIDE; AMYRIN; CYTOCHROME P450; LUPEOL; MUTASE; OLEANOLIC ACID; PENTACYCLIC TRITERPENE; SAPOGENIN; SAPONIN; TRITERPENE; VEGETABLE PROTEIN;

ANALOGS AND DERIVATIVES; BARBAREA; GENE EXPRESSION REGULATION; GENETICS; HERBIVORY; METABOLISM; PHYLOGENY; PLANT GENOME; QUANTITATIVE TRAIT LOCUS; TOBACCO; TRANSGENIC PLANT;

BARBAREA; CYTOCHROME P-450 ENZYME SYSTEM; GENE EXPRESSION REGULATION, PLANT; GENOME, PLANT; HERBIVORY; INTRAMOLECULAR TRANSFERASES; OLEANOLIC ACID; PENTACYCLIC TRITERPENES; PHYLOGENY; PLANT PROTEINS; PLANTS, GENETICALLY MODIFIED; QUANTITATIVE TRAIT LOCI; SAPOGENINS; SAPONINS; TOBACCO; TRITERPENES;

EID: 84944936836     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/tpj.13012     Document Type: Article

References (51)

1. Agerbirk, N., Olsen, C.E., Bibby, B.M., Frandsen, H.O., Brown, L.D., Nielsen, J.K., and, Renwick, J.A.A., (2003a) A saponin correlated with variable resistance of Barbarea vulgaris to the diamondback moth Plutella xylostella. J. Chem. Ecol. 29, 1417-1433.
2. Agerbirk, N., Ørgaard, M., and, Nielsen, J.K., (2003b) Glucosinolates, flea beetle resistance, and leaf pubescence as taxonomic characters in the genus Barbarea (Brassicaceae). Phytochemistry, 63, 69-80.
3. Augustin, J.M., Kuzina, V., Andersen, S.B., and, Bak, S., (2011) Molecular activities, biosynthesis and evolution of triterpenoid saponins. Phytochemistry, 72, 435-457.
4. Augustin, J.M., Drok, S., Shinoda, T., et al. (2012) UDP-glycosyltransferases from the UGT73C subfamily in Barbarea vulgaris catalyze sapogenin 3-O-glucosylation in saponin-mediated insect resistance. Plant Physiol. 160, 1881-1895.
5. Badenes-Perez, F.R., Gershenzon, J., and, Heckel, D.G., (2014) Insect attraction versus plant defense: young leaves high in glucosinolates stimulate oviposition by a specialist herbivore despite poor larval survival due to high saponin content. PLoS One, 9, e95766.
6. Bak, S., Beisson, F., Bishop, G., Hamberger, B., Höfer, R., Paquette, S., and, Werck-Reichhart, D., (2011) Cytochromes P450. Arabidopsis Book, 9, e0144. doi: 10.1199/tab.0144.
7. Blomstedt, C.K., Gleadow, R.M., O'Donnell, N., Naur, P., Jensen, K., Laursen, T., Olsen, C.E., Stuart, P., Hamill, J.D., and, Møller, B.L., (2012) A combined biochemical screen and TILLING approach identifies mutations in Sorghum bicolor L. Moench resulting in acyanogenic forage production. Plant Biotechnol. J. 10, 54-66.
8. Bowles, D., Isayenkova, J., Lim, E.K., and, Poppenberger, B., (2005) Glycosyltransferases: managers of small molecules. Curr. Opin. Plant Biol. 8, 254-263.
9. Carelli, M., Biazzi, E., Panara, F., Tava, A., Scaramelli, L., Porceddu, A., Graham, N., Odoardi, M., Piano, E., and, Arcioni, S., (2011) Medicago truncatula CYP716A12 is a multifunctional oxidase involved in the biosynthesis of hemolytic saponins. Plant Cell, 23, 3070-3081.
10. Christensen, S., Heimes, C., Agerbirk, N., Kuzina, V., Olsen, C.E., and, Hauser, T.P., (2014) Different geographical distributions of two chemotypes of Barbarea vulgaris that differ in resistance to insects and a pathogen. J. Chem. Ecol. 40, 491-501.
11. Chu, H.Y., Wegel, E., and, Osbourn, A., (2011) From hormones to secondary metabolism: the emergence of metabolic gene clusters in plants. Plant J. 66, 66-79.
12. Field, B., and, Osbourn, A.E., (2008) Metabolic diversification-independent assembly of operon-like gene clusters in different plants. Science, 320, 543-547.
13. Field, B., Fiston-Lavier, A.-S., Kemen, A., Geisler, K., Quesneville, H., and, Osbourn, A.E., (2011) Formation of plant metabolic gene clusters within dynamic chromosomal regions. Proc. Natl Acad. Sci. USA, 108, 16116-16121.
14. Frey, M., Chomet, P., Glawischnig, E., Stettner, C., Grün, S., Winklmair, A., Eisenreich, W., Bacher, A., Meeley, R.B., and, Briggs, S.P., (1997) Analysis of a chemical plant defense mechanism in grasses. Science, 277, 696-699.
15. Fukushima, E.O., Seki, H., Ohyama, K., Ono, E., Umemoto, N., Mizutani, M., Saito, K., and, Muranaka, T., (2011) CYP716A subfamily members are multifunctional oxidases in triterpenoid biosynthesis. Plant Cell Physiol. 52, 2050-2061.
16. Hamberger, B., and, Bak, S., (2013) Plant P450s as versatile drivers for evolution of species-specific chemical diversity. Philos. Trans. R. Soc. Lond. B Biol. Sci. 368, 20120426.
17. Hanada, K., Zou, C., Lehti-Shiu, M.D., Shinozaki, K., and, Shiu, S.-H., (2008) Importance of lineage-specific expansion of plant tandem duplicates in the adaptive response to environmental stimuli. Plant Physiol. 148, 993-1003.
18. Khakimov, B., Amigo, J.M., Bak, S., and, Engelsen, S.B., (2012) Plant metabolomics: resolution and quantification of elusive peaks in liquid chromatography-mass spectrometry profiles of complex plant extracts using multi-way decomposition methods. J. Chromatogr. 1266, 84-94.
19. Khakimov, B., Motawia, M.S., Bak, S., and, Engelsen, S.B., (2013) The use of trimethylsilyl cyanide derivatization for robust and broad-spectrum high-throughput gas chromatography-mass spectrometry based metabolomics. Anal. Bioanal. Chem. 405, 9193-9205.
20. Kliebenstein, D.J., and, Osbourn, A., (2012) Making new molecules-evolution of pathways for novel metabolites in plants. Curr. Opin. Plant Biol. 15, 415-423.
21. Kondrashov, F.A., (2012) Gene duplication as a mechanism of genomic adaptation to a changing environment. Proc. Biol. Sci. 279, 5048-5057.
22. Kristensen, C., Morant, M., Olsen, C.E., Ekstrøm, C.T., Galbraith, D.W., Lindberg Møller, B., and, Bak, S., (2005) Metabolic engineering of dhurrin in transgenic Arabidopsis plants with marginal inadvertent effects on the metabolome and transcriptome. Proc. Natl Acad. Sci. USA, 102, 1779-1784.
23. Kuzina, V., Ekstrom, C.T., Andersen, S.B., Nielsen, J.K., Olsen, C.E., and, Bak, S., (2009) Identification of defense compounds in Barbarea vulgaris against the herbivore Phyllotreta nemorum by an ecometabolomic approach. Plant Physiol. 151, 1977-1990.
24. Kuzina, V., Nielsen, J.K., Augustin, J.M., Torp, A.M., Bak, S., and, Andersen, S.B., (2011) Barbarea vulgaris linkage map and quantitative trait loci for saponins, glucosinolates, hairiness and resistance to the herbivore Phyllotreta nemorum. Phytochemistry, 72, 188-198.
25. McCullagh, P., Nelder, J.A., and, McCullagh, P., (1989) Generalized Linear Models. London: Chapman and Hall London.
26. Moses, T., Pollier, J., Almagro, L., Buyst, D., Van Montagu, M., Pedreno, M.A., Martins, J.C., Thevelein, J.M., and, Goossens, A., (2014) 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.
27. Moses, T., Pollier, J., Faizal, A., Apers, S., Pieters, L., Thevelein, J.M., Geelen, D., and, Goossens, A., (2015) Unraveling the triterpenoid saponin biosynthesis of the African shrub Maesa lanceolata. Mol. Plant, 8, 122-135.
28. Mugford, S.T., Louveau, T., Melton, R., Qi, X., Bakht, S., Hill, L., Tsurushima, T., Honkanen, S., Rosser, S.J., and, Lomonossoff, G.P., (2013) Modularity of plant metabolic gene clusters: a trio of linked genes that are collectively required for acylation of triterpenes in oat. Plant Cell, 25, 1078-1092.
29. Nielsen, J., Nagao, T., Okabe, H., and, Shinoda, T., (2010a) Resistance in the plant, Barbarea vulgaris, and counter-adaptations in flea beetles mediated by saponins. J. Chem. Ecol. 36, 277-285.
30. Nielsen, N.J., Nielsen, J., and, Staerk, D., (2010b) New resistance-correlated saponins from the insect-resistant crucifer Barbarea vulgaris. J. Agric. Food Chem. 58, 5509-5514.
31. Nützmann, H.W., and, Osbourn, A., (2014) Gene clustering in plant specialized metabolism. Curr Opin Biotechnol., 26, 91-99. Review. Erratum in: Curr Opin Biotechnol. 2014 Apr;26:199. PubMed PMID: 24679264.
32. Ørgaard, M., and, Linde-Laursen, I.B., (2007) Cytogenetics of Danish species of Barbarea (Brassicaceae): chromocentres, chromosomes and rDNA sites. Hereditas, 144, 159-170.
33. Osbourn, A., (1996) Saponins and plant defence-a soap story. Trends Plant Sci. 1, 4-9.
34. Osbourn, A., (2010) Gene clusters for secondary metabolic pathways: an emerging theme in plant biology. Plant Physiol. 154, 531-535.
35. Paquette, S.M., Bak, S., and, Feyereisen, R., (2000) Intron-exon organization and phylogeny in a large superfamily, the paralogous cytochrome P450 genes of Arabidopsis thaliana. DNA Cell Biol. 19, 307-317.
36. Phillips, D.R., Rasbery, J.M., Bartel, B., and, Matsuda, S.P., (2006) Biosynthetic diversity in plant triterpene cyclization. Curr. Opin. Plant Biol. 9, 305-314.
37. Pollier, J., Moses, T., Gonzalez-Guzman, M., et al. (2013) The protein quality control system manages plant defence compound synthesis. Nature, 504, 148-152.
38. Qi, X., Bakht, S., Leggett, M., Maxwell, C., Melton, R., and, Osbourn, A., (2004) A gene cluster for secondary metabolism in oat: implications for the evolution of metabolic diversity in plants. Proc. Natl Acad. Sci. USA, 101, 8233-8238.
39. Renwick, J.A.A., (2002) The chemical world of crucivores: lures, treats and traps. Entomol. Exp. Appl. 104, 35-42.
40. Sainsbury, F., and, Lomonossoff, G.P., (2008) Extremely high-level and rapid transient protein production in plants without the use of viral replication. Plant Physiol. 148, 1212-1218.
41. Sainsbury, F., Saxena, P., Geisler, K., Osbourn, A., and, Lomonossoff, G.P., (2012) Using a virus-derived system to manipulate plant natural product biosynthetic pathways. Methods Enzymol. 517, 185-202.
42. Seki, H., Ohyama, K., Sawai, S., Mizutani, M., Ohnishi, T., Sudo, H., Akashi, T., Aoki, T., Saito, K., and, Muranaka, T., (2008) Licorice β-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.
43. Seki, H., Sawai, S., Ohyama, K., Mizutani, M., Ohnishi, T., Sudo, H., Fukushima, E.O., Akashi, T., Aoki, T., and, Saito, K., (2011) Triterpene functional genomics in licorice for identification of CYP72A154 involved in the biosynthesis of glycyrrhizin. Plant Cell, 23, 4112-4123.
44. Seki, H., Tamura, K., and, Muranaka, T., (2015) P450s and UGTs: key players in the structural diversity of triterpenoid saponins. Plant Cell Physiol. 56, 1463-1471.
45. Shinoda, T., Nagao, T., Nakayama, M., Serizawa, H., Koshioka, M., Okabe, H., and, Kawai, A., (2002) Identification of a triterpenoid saponin from a crucifer, Barbarea vulgaris, as a feeding deterrent to the diamondback moth, Plutella xylostella. J. Chem. Ecol. 28, 587-599.
46. Takos, A.M., and, Rook, F., (2012) Why biosynthetic genes for chemical defense compounds cluster. Trends Plant Sci. 17, 383-388.
47. Tamura, K., Stecher, G., Peterson, D., Filipski, A., and, Kumar, S., (2013) MEGA6: Molecular Evolutionary Genetics Analysis version 6.0. Mol. Biol. Evol. 30, 2725-2729.
48. Thimmappa, R., Geisler, K., Louveau, T., O'Maille, P., and, Osbourn, A., (2014) Triterpene biosynthesis in plants. Annu. Rev. Plant Biol. 65, 225-257.
49. Wei, X., Zhang, X., Shen, D., Wang, H., Wu, Q., Lu, P., Qiu, Y., Song, J., Zhang, Y., and, Li, X., (2013) Transcriptome analysis of Barbarea vulgaris infested with Diamondback Moth (Plutella xylostella) larvae. PLoS One, 8, e64481.
50. Xue, Z., Duan, L., Liu, D., Guo, J., Ge, S., Dicks, J., ÓMáille, P., Osbourn, A., and, Qi, X., (2012) Divergent evolution of oxidosqualene cyclases in plants. New Phytol. 193, 1022-1038.
51. Yang, Z., (2007) PAML 4: phylogenetic analysis by maximum likelihood. Mol. Biol. Evol. 24, 1586-1591.