Expression of tabersonine 16-hydroxylase and 16-hydroxytabersonine-O-methyltransferase in Catharanthus roseus hairy roots

Biotechnology and Bioengineering

Volumn 115, Issue 3, 2018, Pages 673-683

  Sun, Jiayi ^a   Zhao, Le ^b   Shao, Zengyi ^b   Shanks, Jacqueline ^b   Peebles, Christie A M ^a  

^a Engineering Research Center and Hydraulics Laboratory   (United States)

^b IOWA STATE UNIVERSITY   (United States)

Author keywords

Madagascar periwinkle; metabolic engineering; plant secondary metabolites; terpenoid indole alkaloid; vindoline pathway

Indexed keywords

BIOCHEMISTRY; BIOMOLECULES; CHEMICAL STABILITY; DRUG PRODUCTS; GENES; GENETIC ENGINEERING; LIPIDS; METABOLIC ENGINEERING; METABOLITES; MONOTERPENES; PLANT EXTRACTS; POLYCYCLIC AROMATIC HYDROCARBONS; POLYMERASE CHAIN REACTION;

CATHARANTHUS ROSEUS; MADAGASCAR PERIWINKLES; MONOTERPENE INDOLE ALKALOIDS; PLANT SECONDARY METABOLITES; TERPENOID INDOLE ALKALOIDS; TRANSCRIPTIONAL CHANGES; TRANSGENIC HAIRY ROOTS; VINDOLINE;

ALKALOIDS;

16 HYDROXYTABERSONINE; 16 HYDROXYTABERSONINE O METHYLTRANSFERASE; 16 METHOXYTABERSONINE; 19 HYDROXYTABERSONINE; AJMALICINE; CATHARANTHINE; DRUG METABOLITE; EPOXIDIZED 16 HYDROXYTABERSONINE; HORHAMMERICINE; INDOLE ALKALOID; LOCHNERICINE; LOCHNERININE; PLANT PROTEIN; TABERSONINE; TABERSONINE 16 HYDROXYLASE; UNCLASSIFIED DRUG; VINDOLINE; ZINC FINGER PROTEIN; CYP71D12 PROTEIN, CATHARANTHUS ROSEUS; CYTOCHROME P450; QUINOLINE DERIVATIVE;

16OMT GENE; ARTICLE; CATHARANTHUS ROSEUS; CONTROLLED STUDY; DRUG SYNTHESIS; GENE OVEREXPRESSION; GENETIC ENGINEERING; HAIRY ROOT CULTURE; MAT GENE; NONHUMAN; ORCA GENE; PLANT GENE; PLANT ROOT; PROMOTER REGION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SGD GENE; STR GENE; T16H GENE; T19H GENE; BIOSYNTHESIS; CATHARANTHUS; ENZYMOLOGY; GENE EXPRESSION; GENETICS; METABOLISM; TRANSGENIC PLANT;

CATHARANTHUS; CYTOCHROME P-450 ENZYME SYSTEM; GENE EXPRESSION; INDOLE ALKALOIDS; PLANT PROTEINS; PLANT ROOTS; PLANTS, GENETICALLY MODIFIED; QUINOLINES;

EID: 85034781756     PISSN: 00063592     EISSN: 10970290     Source Type: Journal    
DOI: 10.1002/bit.26487     Document Type: Article

References (38)

1. Aoyama, T., & Chua, N. H. (1997). A glucocorticoid-mediated transcriptional induction system in transgenic plants. Plant Journal, 11, 605–612.
2. Bhadra, R., Vani, S., & Shanks, J. V. (1993). Production of indole alkaloids by selected hairy root lines of Catharanthus roseus. Biotechnology and Bioengineering, 41, 581–592.
3. Brown, S., Clastre, M., Courdavault, V., & O'Connor, S. E. (2015). De novo production of the plant-derived alkaloid strictosidine in yeast. Proceedings of the National Academy of Sciences of the United States of America, 112, 3205–3210.
4. Chi, S. M., Xie, W., Zhang, J. W., & Xu, S. C. (2015). Theoretical insight into the structural mechanism for the binding of vinblastine with tubulin. Journal of Biomolecular Structure and Dynamics, 33, 2234–2254.
5. Costa, M. M., Hilliou, F., Duarte, P., Pereira, L. G., Almeida, I., Leech, M., … Sottomayor, M. (2008). Molecular cloning and characterization of a vacuolar class III peroxidase involved in the metabolism of anticancer alkaloids in Catharanthus roseus. Plant Physiology, 146, 403–417.
6. Courdavault, V., Papon, N., Clastre, M., Giglioli-Guivarc'h, N., St-Pierre, B., & Burlat, V. (2014). A look inside an alkaloid multisite plant: The catharanthus logistics. Current Opinion in Plant Biology, 19, 43–50.
7. Georgiev, M. I., Pavlov, A. I., & Bley, T. (2007). Hairy root type plant in vitro systems as sources of bioactive substances. Applied Microbiology & Biotechnology, 74, 1175–1185.
8. Giddings, L. A., Liscombe, D. K., Hamilton, J. P., Childs, K. L., DellaPenna, D., Buell, C. R., & O'Connor, S. E. (2011). A stereoselective hydroxylation step of alkaloid biosynthesis by a unique cytochrome P450 in Catharanthus roseus. The Journal of Biological Chemistry, 286, 16751–16757.
9. Goklany, S., Rizvi, N. F., Loring, R. H., Cram, E. J., & Lee-Parsons, C. W. T. (2013). Jasmonate-dependent alkaloid biosynthesis in Catharanthus roseus hairy root cultures is correlated with the relative expression of ORCA and ZCT transcription factors. Biotechnology Progress, 29, 1367–1376.
10. Hong, S. B., Peebles, C. A. M., Shanks, J. V., San, K. Y., & Gibson, S. I. (2006). Expression of the Arabidopsis feedback-insensitive anthranilate synthase holoenzyme and tryptophan decarboxylase genes in Catharanthus roseus hairy roots. Journal of Biotechnology, 122, 28–38.
11. Hughes, E. H., Hong, S. B., Gibson, S. I., Shanks, J. V., & San, K. Y. (2004). Metabolic engineering of the indole pathway in Catharanthus roseus hairy roots and increased accumulation of tryptamine and serpentine. Metabolic Engineering, 6, 268–276.
12. Hughes, E. H., Hong, S. B., Shanks, J. V., San, K. Y., & Gibson, S. I. (2002). Characterization of an inducible promoter system in Catharanthus roseus hairy roots. Biotechnology Progress, 18, 1183–1186.
13. Kellner, F., Kim, J., Clavijo, B. J., Jamilton, J. P., Childs, K. L., Vaillancourt, B., … O'Connor, S. E. (2015). Genome-guided investigation of plant natural product. Plant Journal, 82, 680–692.
14. Laflamme, P., St-Pierre, B., & De Luca, V. (2001). Molecular and biochemical analysis of a madagascar periwinkle root-specific minovincinine-19-hydroxy-o-acetyltransferase. Plant Physiology, 125, 189–198.
15. Li, C. Y., Leopold, A. L., Sander, G. W., Shanks, J. V., Zhao, L., & Gibson, S. I. (2013). The ORCA2 transcription factor plays a key role in regulation of the terpenoid indole alkaloid pathway. BMC Plant Biology, 13, 155.
16. Li, C. Y., Leopold, A. L., Sander, G. W., Shanks, J. V., Zhao, L., & Gibson, S. I. (2015). CrBPF1 overexpression alters transcript levels of terpenoid indole alkaloid biosynthetic and regulatory genes. Frontiers in Plant Science, 6, 818.
17. Liu, Y. P., Li, Y., Cai, X. H., Li, X. Y., Kong, L. M., Cheng, G. G., & Luo, X. D. (2012). Melodinines M-U, cytotoxic alkaloids from Melodinus suaveolens. Journal of Natural Products, 75, 220–224.
18. Luijendijk, T. J. C., Stevens, L. H., & Verpoorte, R. (1998). Purification and characterisation of strictosidine beta-d-glucosidase from Catharanthus roseus cell suspension cultures. Plant Physiology and Biochemistry, 36, 419–425.
19. Magnotta, M., Murata, J., Chen, J. X., & De Luca, V. (2007). Expression of deacetylvindoline-4-o-acetyltransferase in Catharanthus roseus hairy roots. Phytochemistry, 68, 1922–1931.
20. McKnight, T. D., Roessner, C. A., Devagupta, R., Scott, A. I., & Nessler, C. L. (1990). Nucleotide sequence of a cDNA encoding the vacuolar protein strictosidine synthase from Catharanthus roseus. Nucleic Acids Research, 18, 4939.
21. Menke, F. L., Parchmann, S., Mueller, M. J., Kijne, J. W., & Memelink, J. (1999). Involvement of the octadecanoid pathway and protein phosphorylation in fungal elicitor-induced expression of terpenoid indole alkaloid biosynthetic genes in Catharanthus roseus. Plant Physiology, 119, 1289–1296.
22. Morgan, J. A., Barney, C. S., Penn, A. H., & Shanks, J. V. (2000). Effects of buffered media upon growth and alkaloid production of Catharanthus roseus hairy roots. Applied Microbiology & Biotechnology, 53, 262–265.
23. Murata, J., & De Luca, V. (2005). Localization of tabersonine 16-hydroxylase and 16-OH tabersonine-16-O-methyltransferase to leaf epidermal cells defines them as a major site of precursor biosynthesis in the vindoline pathway in Catharanthus roseus. Plant Journal, 44, 581–594.
24. Nobili, S., Lippi, D., Witort, E., Donnini, M., Bausi, L., Mini, E., & Capaccioli, S. (2009). Natural compounds for cancer treatment and prevention. Pharmacological Research, 59, 365–378.
25. O'Connor, S. E., & Maresh, J. J. (2006). Chemistry and biology of monoterpene indole alkaloid biosynthesis. Natural Product Reports, 23, 532–547.
26. Pasquali, G., Porto, D. D., & Fett-Neto, A. G. (2006). Metabolic engineering of cell cultures versus whole plant complexity in production of bioactive monoterpene indole alkaloids: Recent progress related to old dilemma. Journal of Bioscience and Bioengineering, 101, 287–296.
27. Peebles, C. A., Hughes, E. H., Shanks, J. V., & San, K. Y. (2009). Transcriptional response of the terpenoid indole alkaloid pathway to the overexpression of ORCA3 along with jasmonic acid elicitation of Catharanthus roseus hairy roots over time. Metabolic Engineering, 11, 76–86.
28. Peebles, C. A. M., Hong, S. B., Gibson, S. I., Shanks, J. V., & San, K. Y. (2005). Transient effects of overexpressing anthranilate synthase alpha and beta subunits in Catharanthus roseus hairy roots. Biotechnology Progress, 21, 1572–1576.
29. Pompon, D., Louerat, B., Bronine, A., & Urban, P. (1996). Yeast expression of animal and plant P450s in optimized redox environments. Methods in Enzymology, 272, 51–64.
30. Qu, Y., MLAE, E., Froese, J., Simionescu, R., Hudlicky, T., & De Luca, V. (2015). Completion of the seven-step pathway from tabersonine to the anticancer drug precursor vindoline and its assembly in yeast. Proceedings of the National Academy of Sciences United States of America, 112, 6224–6229.
31. Rodriguez, S., Compagnon, V., Crouch, N. P., St-Pierre, B., & De Luca, V. (2003). Jasmonate-induced epoxidation of tabersonine by a cytochrome P450 in hairy root cultures of Catharanthus roseus. Phytochemistry, 64, 401–409.
32. Roepke, J., Salim, V., Wu, M., Thamm, A. M. K., Murata, J., Ploss, K., … De Luca, V. (2010). Vinca drug components accumulate exclusively in leaf exudates of Madagascar Periwinkle. Proceedings of the National Academy of Sciences United States of America, 107, 15287–15292.
33. Sears, J. E., & Boger, D. L. (2015). Total synthesis of vinblastine, related natural products, and key analogues and development of inspired methodology suitable for the systematic study of their structure-function properties. Accounts Chemical Research, 48, 653–662.
34. Shalel-Levanon, S., San, K. Y., & Bennett, G. N. (2005). Effect of oxygen, and arca and fnr regulators on the expression of genes related to the electron transfer chain and the TCA cycle in Escherichia coli. Metabolic Engineering, 7, 364–374.
35. Shanks, J. V., Bhadra, R., Morgan, J., Rijhwani, S., & Vani, S. (1998). Quantification of metabolites in the indole alkaloid pathways of Catharanthus roseus: Implications for metabolic engineering. Biotechnology and Bioengineering, 58, 333–338.
36. Sun J., & Peebles C. A. 2015. Engineering overexpression of ORCA3 and strictosidine glucosidase in Catharanthus roseus hairy roots increases alkaloid production. Protoplasma, 253, 1255–1264
37. Sun, J., Ma, L., San, K. Y., & Peebles, C. A. (2017). Still stable after 11 years: A Catharanthus roseus hairy root line maintains inducible expression of anthranilate synthase. Biotechnology Progress, 33, 66–69.
38. Sun, J., Manmathan, H., Sun, C., & Peebles, C. A. (2016). Examining the transcriptional response of overexpressing anthranilate synthase in the hairy roots of an important medicinal plant Catharanthus roseus by RNA-s eq. BMC Plant Biology, 16, 108.