Transcript profiling of jasmonate-elicited Taxus cells reveals a β-phenylalanine-CoA ligase

Plant Biotechnology Journal

Volumn 14, Issue 1, 2016, Pages 85-96

  Ramírez Estrada, Karla ^a   Altabella, Teresa ^a,b   Onrubia, Miriam ^c   Moyano, Elisabeth ^c   Notredame, Cedric ^c,d   Osuna, Lidia ^e   Vanden Bossche, Robin ^f,g   Goossens, Alain ^f,g   Cusido, Rosa M ^a   Palazon, Javier ^a  

^a UNIVERSITY OF BARCELONA   (Spain)

^b UNIVERSITAT AUTÒNOMA DE BARCELONA   (Spain)

^c UNIVERSITAT POMPEU FABRA   (Spain)

^d CENTRE FOR GENOMIC REGULATION CRG   (Spain)

^e INSTITUTO MEXICANO DEL SEGURO SOCIAL   (Mexico)

^f DEPARTMENT OF PLANT SYSTEMS BIOLOGY   (Belgium)

^g GHENT UNIVERSITY   (Belgium)

Author keywords

Taxus baccata; cDNA AFLP; Cell cultures; CoA ligase; Methyl jasmonate; Taxol; phenylalanine

Indexed keywords

BRIDGED COMPOUND; COMPLEMENTARY DNA; CYCLOPENTANE DERIVATIVE; JASMONIC ACID; LIGASE; MESSENGER RNA; OXYLIPIN; PACLITAXEL; PHENYLALANINE; PLANT PROTEIN; TAXANE; TAXOID;

AMINO ACID SEQUENCE; AMPLIFIED FRAGMENT LENGTH POLYMORPHISM; BIOSYNTHESIS; CHEMISTRY; COMPUTER SIMULATION; CYTOLOGY; CYTOSOL; DRUG EFFECTS; ENZYMOLOGY; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETIC ASSOCIATION STUDY; GENETICS; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; METABOLISM; MOLECULAR MODEL; PLANT GENE; SEQUENCE ALIGNMENT; TANDEM MASS SPECTROMETRY; TAXUS;

AMINO ACID SEQUENCE; AMPLIFIED FRAGMENT LENGTH POLYMORPHISM ANALYSIS; BRIDGED-RING COMPOUNDS; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; COMPUTER SIMULATION; CYCLOPENTANES; CYTOSOL; DNA, COMPLEMENTARY; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, PLANT; GENES, PLANT; GENETIC ASSOCIATION STUDIES; LIGASES; MODELS, MOLECULAR; OXYLIPINS; PACLITAXEL; PHENYLALANINE; PLANT PROTEINS; RNA, MESSENGER; SEQUENCE ALIGNMENT; TANDEM MASS SPECTROMETRY; TAXOIDS; TAXUS;

EID: 84955204304     PISSN: 14677644     EISSN: 14677652     Source Type: Journal    
DOI: 10.1111/pbi.12359     Document Type: Article

References (52)

1. Allina, S.M., Pri-Hadash, A., Theilmann, D.A., Ellis, B.E. and Douglas, C.J. (1998) 4-Coumarate: coenzyme a ligase in hybrid poplar. Plant Physiol. 116, 743-775.
2. Bentebibel, S., Moyano, E., Palazon, J., Cusidó, R.M., Bonfill, M., Eibl, R. and Piñol, M.T. (2005) Effects of immobilization by entrapment in alginate and scale-up on paclitaxel and baccatin III production in ell suspension cultures of Taxus baccata. Biotechnol. Bioeng. 89, 647-655.
3. Breyne, P. and Zabeau, M. (2001) Genome-wide expression analysis of plant cell cycle modulated genes. Curr. Opin. Plant Biol. 4, 136-142.
4. Colling, J., Pollier, J., Makunga, N.P. and Goossens, A. (2013) cDNA-AFLP-based transcript profiling for genome-wide expression analysis of jasmonate-treated plants and plant cultures. Methods Mol. Biol. 1011, 287-303.
5. Croteau, R., Ketchum, R.E.B., Long, R.B., Kaspera, R. and Wildung, M.R. (2006) Taxol biosynthesis and molecular genetics. Phytochem. Rev. 5, 75-97.
6. Cusido, R.M., Palazón, J., Bonfill, M., Navia-Osorio, A., Morales, C. and Piñol, M.T. (2002) Improved paclitaxel and baccatin III production in suspension cultures of Taxus media. Biotechnol. Prog. 18, 418-423.
7. Cusido, R.M., Onrubia, M., Sabater-Jara, A.B., Moyano, E., Bonfill, M., Goossens, A., Pedreño, M.A. and Palazon, J. (2014) A rational approach to improving the biotechnological production of taxanes in plant cell cultures of Taxus spp. Biotechnol. Adv. 32, 1157-1167.
8. De Geyter, N., Gholami, A., Goormachtig, S. and Goossens, A. (2012) Transcriptional machineries in jasmonate-elicited plant secondary metabolism. Trends Plant Sci. 17, 349-359.
9. Deblaere, R., Bytebier, B., DeGreve, H., Deboeck, F., Schell, J., Van Montagu, M. and Leemans, J. (1985) Efficient octopine Ti plasmid-derived vectors for Agrobacterium-mediated gene transfer to plants. Nucleic Acids Res. 13, 4777-4788.
10. Dickerson, D.P., Pascholati, S.F., Hagerman, A.E., Butler, L.G. and Nicholson, R.L. (1984) Phenylalanine ammonia-lyase and hydroxycinnamate:CoA ligase in maize mesocotyls inoculated with Helminthosporium maydis or Helminthosporium carbonum. Physiol. Plant Pathol. 25, 111-123.
11. Docimo, T., Conssoni, R., Coraggio, I. and Mattana, M. (2013) Early phenylpropanoid biosynthetic steps in Cannabis sativa: link between genes and metabolites. Int. J. Mol. Sci. 14, 13626-13644.
12. Earley, K.W., Haag, J.R., Pontes, O., Opper, K., Juehne, T., Song, K. and Pikaard, C.S. (2006) Gateway-compatible vectors for plant functional genomics and proteomics. Plant J. 45, 616-629.
13. Ehlting, J., Büttner, D., Wang, Q., Douglas, C.J., Somssich, I.E. and Kombrink, E. (1999) Three 4-coumarate: coenzyme A ligases in Arabidopsis thaliana represent two evolutionarily divergent classes in angiosperms. Plant J. 19, 9-20.
14. Ernst, O. and Zor, T. (2010) Linearization of the Bradford protein assay. J. Vis. Exp. 38, 1918.
15. Expósito, O., Bonfill, M., Moyano, E., Onrubia, M., Mirjalili, H., Cusidó, R.M. and Palazon, J. (2009) Biotechnological production of taxol and related taxoids: current state and prospects. Anticancer Agents Med. Chem. 9, 109-121.
16. Floss, H.G. and Mocek, U. (1995) Biosynthesis of taxol. In Taxol: Science and Applications (Suffness, M., ed.), pp. 191-208. Boca Raton: CRC Press.
17. Frense, D. (2007) Taxanes: perspectives for biotechnological production. Appl. Microbiol. Biotechnol. 73, 1233-1240.
18. Goossens, A. (2015) It is easy to get huge candidate gene lists for plant metabolism now, but how to get beyond? Mol. Plant. 8, 2-5.
19. Goossens, A., Hakkinen, S.T., Laakso, I., Seppanen-Laakso, T., Biondi, S., De Sutter, V., Lammertyn, F., Nuutila, A.M., Söderlund, H., Zabeau, M., Inze, D. and Oksman-Caldentey, K.M. (2003) A functional genomics approach toward the understanding of secondary metabolism in plant cells. Proc. Natl Acad. Sci. USA, 100, 8595-8600.
20. Goytia, E., Fernández-Clavino, L., Martínez-Garcia, B., López-Abella, D. and López-Moya, J.J. (2006) Production of plum pox virus HC-Pro functionally active for aphid transmission in a transient expression system. J. Gen. Virol. 87, 3413-3423.
21. Guo, B.H., Kai, G.Y., Jin, H.B. and Tang, K.X. (2006) Taxol synthesis. A. J. Biotechnol. 5, 15-20.
22. Hamberger, B. and Hahlbrock, K. (2004) The 4-coumarate:CoA ligase gene family in Arabidopsis thaliana comprises one rare, sinapate-activating and three commonly occurring isoenzymes. Proc. Natl Acad. Sci. USA, 101, 2209-2214.
23. Held, M.A., Boulaflous, A. and Brandizzi, F. (2008) Advances in fluorescent protein-based imaging for the analysis of plant endomembranes. Plant Physiol. 147, 1469-1481.
24. Hezari, M., Ketchum, R.E.B., Gibson, D.M. and Croteau, R. (1997) Taxol production and taxadiene synthase activity in Taxus canadensis cell suspension cultures. Arch. Biochem. Biophys. 337, 185-190.
25. Hu, Y., Gai, Y., Yin, L., Wang, X., Feng, C., Feng, L., Li, D., Jiang, X. and N. Wang, D.C. (2010) Crystal structures of Populus tomentosa 4-Coumarate: CoA ligase shed light on its enzymatic mechanisms. Plant Cell, 22, 3093-3140.
26. Jalalpour, Z., Shabani, L., Afghani, L., Sharifi-Tehrani, M. and Amini, S.A. (2014) Stimulatory effect of methyl jasmonate and squalestatin on phenolic metabolism through induction of LOX activity in cell suspension culture of yew. Turk. J. Biol. 38, 76-82.
27. Keeling, C.I. and Bohlmann, J. (2006) Diterpene resin acids in conifers. Phytochemistry, 67, 2415-2423.
28. Kelley, L.A. and Sternberg, M.J.E. (2009) Protein structure prediction on the web: a case study using the Phyre server. Nat. Protoc. 4, 363-371.
29. Kingston, D.G.I. (2000) Recent advances in the chemistry of taxol. J. Nat. Prod. 63, 726-734.
30. Koepp, A.E., Hezari, M., Zajicek, J., Stofer, V.B., LaFever, R.E., Lewis, N.G. and Croteau, R.B. (1995) Cyclization of geranylgeranyl diphosphate to taxa-4(5), 11(12)-diene is the committed step of Taxol biosynthesis in Pacific yew. J. Biol. Chem. 270, 8686-8690.
31. Koetsier, M.J., Jekel, P.A., Vandenberg, M.A., Bovenberg, R.A. and Jansen, D.B. (2009) Characterization of a phenylacetate-CoA ligase from Penicillium chrysogenum. Biochem. J. 417, 467-476.
32. Lange, B.M. and Ahkami, A. (2013) Metabolic engineering of plant monoterpenes, sesquiterpenes and diterpenes - current status and future opportunities. Plant Biotechnol. J. 11, 169-196.
33. Li, S.T., Zhang, P., Zhang, M., Fu, Ch.H., Zhao, Ch.F., Dong, Y.S., Guo, A.Y. and Yu, L.J. (2012) Transcriptional profile of Taxus chinensis cells in response to methyl jasmonate. BMC Genom. 13, 295.
34. Lindermayr, Ch., Möllers, B., Fliegmann, J., Uhlmann, A., Lottspeich, F., Meimberg, H. and Ebel, J. (2002) Divergent members of a soybean (Glycine max L.) 4-coumarate:coenzyme A ligase gene family. Primary structures, catalytic properties and differential expression. Eur. J. Biochem. 269, 1304-1315.
35. Malik, S., Cusido, R.M., Mirjalili, M.H., Moyano, E., Palazon, J. and Bonfill, M. (2011) Production of the anticancer drug taxol in Taxus baccata suspension cultures: a review. Proc. Biochem. 46, 23-34.
36. Marchler-Bauer, A., Anderson, J.B., Chitsaz, F., Derbyshire, M.K., DeWeese-Scott, C., Fong, J.H., Geer, L.Y., Geer, R.C., Gonzales, N.R., Gwadz, M., He, S., Hurwitz, D.I., Jackson, J.D., Ke, Z., Lanczycki, C.J., Liebert, C.A., Liu, C., Lu, F., Lu, S., Marchler, G.H., Mullokandov, M., Song, J.S., Tasneem, A., Thanki, N., Yamashita, R.A., Zhang, D., Zhang, N. and Bryant, S.H. (2009) CDD: specific functional annotation with the conserved domain database. Nucleic Acids Res. 37, D205-D210.
37. Marchler-Bauer, A., Lu, S., Anderson, J.B., Chitsaz, F., Derbyshire, M.K., DeWeese-Scott, C., Fong, J.H., Geer, L.Y., Geer, R.C., Gonzales, N.R., Gwadz, M., Hurwitz, D.I., Jackson, J.D., Ke, Z., Lanczycki, C.J., Lu, F., Marchle, R.G.H., Mullokandov, M., Omelchenko, M.V., Robertson, C.L., Song, J.S., Thanki, N., Yamashita, R.A., Zhang, D., Zhang, N., Zheng, C. and Bryant, S.H. (2011) CDD: a conserved domain database for the functional annotation of proteins. Nucleic Acids Res. 39, D225-D229.
38. Muchiri, R. and Walker, K.D. (2012) Taxol biosynthesis: tyrocidine synthetase A catalyzes the production of phenylisoserinyl CoA and other amino phenylpropanoyl thioesters. Chem. Biol. 19, 679-685.
39. Nims, E., Dubois, C.P., Roberts, S.C. and Walker, E.L. (2006) Expression profiling of genes involved in paclitaxel biosynthesis for targeted metabolic engineering. Metab. Eng. 8, 385-394.
40. Onrubia, M., Moyano, E., Bonfill, M., Expósito, O., Palazón, J. and Cusidó, R.M. (2010) An approach to the molecular mechanism of methyl jasmonate and vanadyl sulphate elicitation in Taxus baccata cell cultures: the role of txs and bapt gene expression. Biochem. Eng. J. 53, 104-111.
41. Onrubia, M., Cusido, R.M., Ramirez, K., Hernández-Vázquez, L., Moyano, E., Bonfill, M. and Palazon, J. (2013a) Bioprocessing of plant in vitro systems for the mass production of pharmaceutically important metabolites: Paclitaxel and its derivatives. Curr. Med. Chem. 20, 880-891.
42. Onrubia, M., Moyano, E., Bonfill, M., Cusidó, R.M., Goossens, A. and Palazón, J. (2013b) Coronatine, a more powerful elicitor for inducing taxane biosynthesis in Taxus media cell cultures than methyl jasmonate. J. Plant Physiol. 170, 211-219.
43. Onrubia, M., Pollie, r.J., Vanden Bossche, R., Goethals, M., Gevaert, K., Moyano, E., Vidal-Limon, H., Cusidó, R.M., Palazón, J. and Goossens, A. (2014) Taximin, a conserved plant-specific peptide modulates secondary metabolism in Taxus baccata and Nicotiana tabacum. Plant Biotechnol. J. 12, 971-983.
44. Palazon, J., Cusido, R.M., Bonfill, M., Morales, C. and Piñol, M.T. (2003) Inhibition of paclitaxel and baccatin III accumulation by mevinolin and fosmidomycin in suspension cultures of Taxus baccata. J. Biotechnol. 101, 157-163.
45. Pauwels, L., Inzé, D. and Goossens, A. (2009) Jasmonate-inducible gene: what does it mean? Trends Plant Sci. 14, 87-91.
46. Petersen, T.N., Brunak, S., von Heijne, G. and Nielsen, H. (2011) SignalP 4.0: discriminating signal peptides from transmembrane regions. Nat. Methods, 8, 785-786.
47. Sabater-Jara, A.B., Onrubia, M., Moyano, E., Bonfill, M., Palazón, J., Pedreño, M.A. and Cusidó, R.M. (2014) Synergistic effect of cyclodextrins and methyl jasmonate on taxane production in Taxus x media cell cultures. Plant Biotechnol. J. 12, 1075-1084.
48. Voinnet, O., Rivas, S., Mestre, P. and Baulcombe, D. (2003) An enhanced transient expression system in plants based on suppression of gene silencing by the p19 protein of tomato bushy stunt virus. Plant J. 33, 949-956.
49. Vongpaseuth, K. and Roberts, S.C. (2007) Advancements in the understanding of Paclitaxel metabolism in tissue culture. Curr. Pharm. Biotechnol. 8, 219-236.
50. Walker, K. and Croteau, R. (2001) Taxol biosynthetic genes. Phytochemistry, 58, 1-7.
51. Wasternack, C. (2007) Jasmonates: an update on biosynthesis, signal transduction and action in plant stress response, growth and development. Ann. Bot. 100, 681-697.
52. Wu, Y., Masison, D.C., Eisenberg, E. and Green, L.E. (2006) Application of photobleaching for measuring diffusion of prion proteins in cytosol of yeast cells. Methods, 39, 43-49.