A rational approach to improving the biotechnological production of taxanes in plant cell cultures of Taxus spp

Biotechnology Advances

Volumn 32, Issue 6, 2014, Pages 1157-1167

  Cusido, Rosa M ^a   Onrubia, Miriam ^b   Sabater Jara, Ana B ^c   Moyano, Elisabet ^b   Bonfill, Mercedes ^a   Goossens, Alain ^d,e   Angeles Pedreno M ^c   Palazon, Javier ^a  

^a UNIVERSITY OF BARCELONA   (Spain)

^b UNIVERSITAT POMPEU FABRA   (Spain)

^c UNIVERSITY OF MURCIA   (Spain)

^d DEPARTMENT OF PLANT SYSTEMS BIOLOGY   (Belgium)

^e GHENT UNIVERSITY   (Belgium)

Author keywords

Coronatine; Cyclodextrins; Elicitation; Metabolic engineering; Methyl jasmonate; Plant cell culture; Taxanes; Taxol; Taxus spp.; Transcriptomics

Indexed keywords

BIOCHEMISTRY; BIOSYNTHESIS; BIOTECHNOLOGY; CELL CULTURE; CYCLODEXTRINS; GENE EXPRESSION; METABOLIC ENGINEERING; METABOLISM; PLANT CELL CULTURE; PLANTS (BOTANY);

CORONATINE; ELICITATION; METHYL JASMONATE; TAXANES; TAXOL; TAXUS SPP; TRANSCRIPTOMICS;

CELL ENGINEERING;

TAXUS;

TAXOID;

BIOTECHNOLOGY; CELL CULTURE; CHEMISTRY; CYTOLOGY; METABOLIC ENGINEERING; METABOLISM; PROCEDURES; TAXUS;

BIOTECHNOLOGY; CELLS, CULTURED; METABOLIC ENGINEERING; TAXOIDS; TAXUS;

EID: 84926259256     PISSN: 07349750     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.biotechadv.2014.03.002     Document Type: Review

References (112)

1. Abal M., Andreu J.M., Barasoain I. Taxanes: microtubule and centrosome targets, and cell cycle dependent mechanism of action. Curr Cancer Drug Targets 2003, 3:193-203.
2. Ajikumar P.K., Xiao W.H., Tyo K.E., Wang Y., Simeon F., Leonard E., et al. Isoprenoid pathway optimization for taxol precursor overproduction in Escherichia coli. Science 2010, 330(6000):70-74.
3. Almagro L., López-Pérez A.J., Pedreño M.A. New method to enhance ajmalicine production in Catharanthus roseus cell cultures based on the use of cyclodextrins. Biotechnol Lett 2011, 33:381-385.
4. Baebler S., Camloh M., Kovac M., Ravnikar M., Zel J. Jasmonic acid stimulates taxane production in cell suspension culture of yew (Taxus×media). Planta Med 2002, 68(5):475-476.
5. Belchí-Navarro S., Almagro L., Lijavetzky D., Bru R., Pedreño M.A. Enhanced extracellular production of trans-resveratrol in Vitis vinifera suspension cultured cells by using cyclodextrins and methyljasmonate. Plant Cell Rep 2012, 31:81-89.
6. Belchí-Navarro S., Almagro L., Sabater-Jara A.B.., Fernández-Pérez F., Bru R., Pedreño M.A. Early signaling events in grapevine cells elicited with cyclodextrins and methyl jasmonate. Plant Physiol Biochem 2013, 62:107-110.
7. Belchí-Navarro S., Almagro L., Sabater-Jara A.B., Fernández-Pérez F., Bru R., Pedreño M.A. Induction of trans-resveratrol and extracellular pathogenesis-related proteins in elicited suspension cultured cells of Vitis vinifera cv Monastrell. J Plant Physiol 2013, 170:258-264.
8. Belchí-Navarro S., Pedreño M.A., Corchete P. Methyl jasmonate increases silymarin production in Silybum marianum (L.) Gaernt cell cultures treated with β-cyclodextrins. Biotechnol Lett 2013, 3:179-184.
9. Bonfill M., Palazón J., Cusidó R.M., Joly S., Morales C., Piñol M.T. Influence of elicitors on taxane production and 3-hydroxy-3-methylglutaryl coenzyme A reductase activity in Taxus media cells. Plant Physiol Biochem 2003, 41:91-96.
10. Briceño Z., Almagro L., Sabater-Jara A.B.., Calderón A.A., Pedreño M.A., Ferrer M.A. Enhancement of phytosterols, taraxasterol and induction of extracellular pathogenesis-related proteins in cell cultures of Solanum lycopersicum cv Micro-Tom elicited with cyclodextrins and methyl jasmonate. J Plant Physiol 2012, 169:1050-1058.
11. Bru R, Pedreño MA. Method for the production of resveratrol in cell cultures. PCT Patent WO/2003/062406 2003.
12. Bru R., Sellés S., Casado-Vela J., Belchí-Navarro S., Pedreño M.A. Modified cyclodextrins are chemically defined glucan inducers of defense responses in grapevine cell cultures. J Agric Food Chem 2006, 54:65-71.
13. Capell T., Christou P. Progress in plant metabolic engineering. Curr Opin Biotechnol 2004, 15(2):148-154.
14. Cha M., Shim S.H., Kim S.H., Kim O.T., Lee S.W., Kwon S.Y., et al. Production of taxadiene from cultured ginseng roots transformed with taxadiene synthase gene. BMB Rep 2012, 45(10):589-594.
15. Collins-Pavao M., Chin C.K., Pedersen H. Taxol partitioning in two-phase plant cell cultures of Taxus brevifolia. J Biotechnol 1996, 49:95-100.
16. Croteau R., Ketchum R.E., Long R.M., Kaspera R., Wildung M.R. Taxol biosynthesis and molecular genetics. Phytochem Rev 2006, 5:75-97.
17. Cusido R.M., Palazón J., Bonfill M., Navia-Osorio A., Morales C., Piñol M.T. Improved paclitaxel and baccatin III production in suspension cultures of Taxus media. Biotechnol Prog 2002, 18(3):418-423.
18. Dai Y., Qin Q., Dai D., Kong L., Li W., Zha X., et al. Isolation and characterization of a novel cDNA encoding methyl jasmonate-responsive transcription factor TcAP2 from Taxus cuspidata. Biotechnol Lett 2009, 31:1801-1809.
19. De Geyter N., Gholami A., Goormachtig S., Goossens A. Transcriptional machineries in jasmonate-elicited plant secondary metabolism. Trends Plant Sci 2012, 17:349-359.
20. Dean A., Voss D. Design and analysis of experiments 1999, 506-514. Springer, New York.
21. Denis J.N., Greene A., Guenard D., Gueritte-Voegelein F., Mangatal L., Potier P. Highly efficient, practical approach to natural taxol. J Am Chem Soc 1988, 110:5917-5919.
22. Ehrlich A., Booher S., Becerra Y., Borris D.L., Figg D., Turner M.L., et al. Micellar paclitaxel improves severe psoriasis in a prospective phase II pilot study. J Am Acad Dermatol 2004, 50:533-540.
23. Expósito O., Bonfill M., Moyano E., Onrubia M., Mirjalili M.H., Cusidó R.M., et al. Biotechnological production of taxol and related taxoids: current state and prospects. Anticancer Agents Med Chem 2009, 9:109-121.
24. Exposito O., Bonfill M., Onrubia M., Jané A., Moyano E., Cusidó Rosa M., et al. Effect of taxol feeding on taxol and related taxane production in Taxus baccata suspension cultures. N Biotechnol 2009, 25:252-259.
25. Expósito O., Syklowska-Baranek K., Moyano E., Onrubia M., Bonfill M., Palazón J., et al. Metabolic responses of Taxus media transformed cell cultures to the addition of methyl jasmonate. Biotechnol Prog 2010, 26:1145-1153.
26. Feng S., Ma L., Wang X., Xie D., Dinesh-Kumar S.P., Wei N., et al. The COP9 signalosome interacts physically with SCFCOI1 and modulates jasmonate responses. Plant Cell 2003, 15:1083-1094.
27. Fett-Neto A.G., Pennington J.J., DiCosmo F. Effect of white light on taxol and baccatin iii accumulation in cell cultures of Taxus cuspidata Sieb and Zucc. J Plant Physiol 1995, 146:584-590.
28. Fliegmann J., Schüler G., Boland W., Ebel J., Mithöfer A. The role of octadecanoids and functional mimics in soybean defense responses. Biol Chem 2003, 384:437-446.
29. Fornale S., Esposti D.D., Navia-Osorio A., Cusido R.M., Palazon J., Piñol M.T., et al. Taxol transport in Taxus baccata cell suspension cultures. Plant Physiol Biochem 2002, 40:81-88.
30. Fu C., Li L., Wu W., Li M., Yu X., Yu L. Assessment of genetic and epigenetic variation during long-term Taxus cell culture. Plant Cell Rep 2012, 31(7):1321-1331.
31. Furmanowa M., Syklowska-Baranek K. Hairy root cultures of Taxus×media var. Hicksii Rehd. as a new source of paclitaxel and 10-deacetylbaccatin III. Biotechnol Lett 2000, 22:683-686.
32. Gamborg O.L., Miller R.A., Ojima K. Nutrient requirements of suspension cultures of soybean root cells. Exp Cell Res 1968, 50:151-158.
33. Geng X., Cheng J., Gangadharan A., Mackey D. The coronatine toxin of Pseudomonas syringae is a multifunctional suppressor of Arabidopsis defense. Plant Cell 2012, 24:4763-4774.
34. Guo S., Huang L. Nanoparticles containing insoluble drug for cancer therapy. Biotechnol Adv 2014, 32:778-788.
35. Haider G., von Schrader T., FüBlein M., Blechert S., Kutchan T.M. Structure-activity relationships of synthetic analogs of jasmonic acid and coronatine on induction of benzo[c]phenanthridine alkaloid accumulation in Eschscholzia californica cell cultures. Biol Chem 2000, 381:741-748.
36. Häkkinen S.T., Tilleman S., Swiatek A., De Sutter V., Rischer H., Vanhoutte I., et al. Functional characterisation of genes involved in pyridine alkaloid biosynthesis in tobacco. Phytochemistry 2007, 68:2773-2785.
37. Hampel D., Mau C.J., Croteau R.B. Taxol biosynthesis: identification and characterization of two acetyl CoA:taxoid-O-acetyl transferases that divert pathway flux away from Taxol production. Arch Biochem Biophys 2009, 487:91-97.
38. Han K.H., Fleming P., Walker K., Loper M., Chilton W.S., Mocek U., et al. Genetic transformation of mature Taxus: an approach to genetically control the in vitro production of the anticancer drug, taxol. Plant Sci 1994, 95:187-196.
39. Hao D.C., Ge G., Xiao P., Zhang Y., Yang L. The first insight into the tissue specific Taxus transcriptome via Illumina second generation sequencing. PLoS One 2011, 6:e21220.
40. Hao D., Yang L., Xiao P. The first insight into the Taxus genome via fosmid library construction and end sequencing. Mol Genet Genomics 2011, 285:197-205.
41. Hao D.C., Xiao P.G., Ge G.B., Ming M. Biological, chemical, and omics research of Taxus. Med Resour Drug Dev Res 2012, 73:477-486.
42. Hao D.C., Yang L., Xiao P.G., Liu M. Identification of Taxus microRNAs and their targets with high-throughput sequencing and degradome analysis. Physiol Plant 2012, 146:388-403.
43. Ho C.K., Chang S.H., Lung J., Tsai C.J., Chen K.P. The strategies to increase taxol production by using Taxus mairei cells transformed with TS and DBAT genes. Int J Appl Sci Eng 2005, 3:179-185.
44. Holton R.A., Kim H.B., Somoza C., Liang F., Biediger R.J., Boatman P.D., et al. First total synthesis of taxol. 2. Completion of the C and D rings. J Am Chem Soc 1994, 116:1599-1600.
45. Holton R.A., Somoza C., Kim H.B., Liang F., Biediger R.J., Boatman P.D., et al. First total synthesis of taxol. 1. Functionalization of the B ring. J Am Chem Soc 1994, 116:1597-1598.
46. Hu F., Huang J., Xu Y., Qian X., Zhong J.J. Responses of defense signals, biosynthetic gene transcription and taxoid biosynthesis to elicitation by a novel synthetic jasmonate in cell cultures of Taxus chinensis. Biotechnol Bioeng 2006, 94:1064-1071.
47. Jennewein S., Wildung M.R., Chau M., Walker K., Croteau R. Random sequencing of an induced Taxus cell cDNA library for identification of clones involved in Taxol biosynthesis. Proc Natl Acad Sci U S A 2004, 101:9149-9154.
48. Katsir L., Schilmiller A.L., Staswick P.E., He S.Y., Howe G.A. COI1 is a critical component of a receptor for jasmonate and the bacterial virulence factor coronatine. Proc Natl Acad Sci U S A 2008, 105:7100-7105.
49. Kim B.J., Gibson D.M., Shuler M.L. Effect of subculture and elicitation on instability of taxol production in Taxus sp. suspension cultures. Biotechnol Prog 2004, 20(6):1666-1673.
50. Kim B.J., Gibson D.M., Shuler M.L. Effect of the plant peptide regulator, phytosulfokine-alpha on the growth and taxol production from Taxus sp suspension cultures. Biotechnol Bioeng 2006, 95:8-14.
51. Kim J.A., Baek K.H., Son Y.M., Son S.H., Shin H. Hairy root cultures of Taxus cuspidata for enhanced production of paclitaxel. J Korean Soc Appl Biol Chem 2009, 52(2):144-150.
52. Kombrink E. Chemical and genetic exploration of jasmonate biosynthesis and signalling paths. Planta 2012, 236:1351-1366.
53. Lackman P., González-Guzmán M., Tilleman S., Carqueijeiro I., Pérez A.C., Moses T., et al. Jasmonate signaling involves the abscisic acid receptor PYL4 to regulate metabolic reprogramming in Arabidopsis and tobacco. Proc Natl Acad Sci U S A 2011, 108:5891-5896.
54. Lauchli R., Schüler G., Boland W. Selective induction of secondary metabolism in Phaseolus lunatus by 6-substituted indanoyl isoleucine conjugates. Phytochemistry 2002, 61:807-817.
55. Law R.D., Suttle J.C. Chromatin remodeling in plant cell culture: patterns of DNA methylation and histone H3 and H4 acetylation vary during growth of asynchronous potato cell suspensions. Plant Physiol Biochem 2005, 43:527-534.
56. Lee E.K., Jin Y.W., Park J.H., Yoo Y.M., Hong S.M., Amir R., et al. Cultured cambial meristematic cells as a source of plant natural products. Nat Biotechnol 2010, 28:1213-1217.
57. Lee S., Yang D.S., Uppalapati S.R., Sumner L.W., Mysore K.S. Suppression of plant defense responses by extracellular metabolites from Pseudomonas syringae pv Tabaci in Nicotiana benthamiana. BMC Plant Biol 2013, 13:65.
58. Lenka S.K., Boutaoui N., Paulose B., Vongpaseuth K., Normanly J., Roberts S.C., et al. Identification and expression analysis of methyl jasmonate responsive ESTs in paclitaxel producing Taxus cuspidata suspension culture cells. BMC Genomics 2012, 13:148.
59. Leone L.M., Roberts S.C. Accessing anti-cancer natural products by plant cell culture. Natural products and cancer drug discovery 2013, 193-213. Humana Press. Springer, New York, Heidelberg, Dordrecht, London. F.E. Koehn (Ed.).
60. Li Y.C., Tao W.Y. Paclitaxel-producing fungal endophyte stimulates the accumulation of taxoids in suspension cultures of Taxus cuspidate. Sci Hortic 2009, 121:97-102.
61. Li F.L., Ma X.J., Hu X.L., Hoffman A., Dai J.G., Qiu D.Y. Antisense-induced suppression of taxoid 14β-hydroxylase gene expression in transgenic Taxus×media cells. Afr J Biotechnol 2011, 10:8720-8728.
62. Li S.T., Fu C.H., Zhang M., Zhang Y., Xie S., Yu L.J. Enhancing taxol biosynthesis by overexpressing a 9-cis-epoxycarotenoid dioxygenase gene in transgenic cell lines of Taxus chinensis. Plant Mol Biol Report 2012, 30:1125-1130.
63. Li S.T., Zhang P., Zhang M., Fu C.-H., Zhao C.-F., Dong Y.-S., et al. Transcriptional profile of Taxus chinensis cells in response to methyl jasmonate. BMC Genomics 2012, 13:295.
64. Li L.Q., Li X.L., Fu C.H., Zhao C.F., Yu L.J. Sustainable use of Taxus media cell cultures through minimal growth conservation and manipulation of genome methylation. Process Biochem 2013, 48:525-531.
65. Li S., Zhang P., Zhang M., Fu C., Yu L. Functional analysis of a WRKY transcription factor involved in transcriptional activation of the DBAT gene in Taxus chinensis. Plant Biol 2013, 15:19-26.
66. Lijavetzky D., Almagro L., Belchí-Navarro S., Martínez-Zapater J.M., Bru R., Pedreño M.A. Synergistic effect of methyljasmonate and cyclodextrin on stilbene biosynthesis pathway gene expression and resveratrol production in Monastrell grapevine cell cultures. BMC Res Notes 2008, 1:132-140.
67. Lloyd G., McCown B.H. Commercially feasible micropropagation of mountain laurel, (Kalmia latifolia) by use of shoot tip culture. Int Plant Prop Soc Comb Proc 1980, 30:421-427.
68. Luan E.C., Allen S.E., Bolyard M.G. Transient GUS expression in zygotic embryos of Taxus brevifolia. In Vitro Cell Dev Biol Plant 1996, 32:81-85.
69. Luo J., He G.Y. Optimization of elicitors and precursors for paclitaxel production in cell suspension culture of Taxus chinensis in the presence of nutrient feeding. Process Biochem 2004, 39(9):1073-1079.
70. Malik S., Cusido R.M., Mirjalili M.H., Moyano E., Palazon J., Bonfill M. Production of the anticancer drug taxol in Taxus baccata suspension cultures: a review. Process Biochem 2011, 46:23-34.
71. Miele M., Mumot A.M., Zappa A., Romano P., Ottaggio L. Hazel and other sources of paclitaxel and related compounds. Phytochem Rev 2012, 11:211-225.
72. Murashige T., Skoog F. A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiol Plant 1962, 15:473-497.
73. Naill M.C., Kolewe M.E., Roberts S.C. Paclitaxel uptake and transport in Taxus cell suspension cultures. Biochem Eng J 2012, 63:50-56.
74. Nicolaou K.C., Yang Z., Liu J.J., Ueno H., Nantermet P.G., Guy R.K., et al. Total synthesis of taxol. Nature 1994, 367:630-634.
75. Nystedt B., Street N.R., Wetterbom A., Zuccolo A., Lin Y.C., Scofield D.G., et al. The Norway spruce genome sequence and conifer genome evolution. Nature 2013, 497:579-584.
76. Onrubia M. A molecular approach to taxol biosynthesis 2012, [PhD dissertation], University Pompeu Fabra, [http://hdl.handle.net/10803/83344].
77. Onrubia M., Moyano E., Bonfill M., Expósito O., Palazón J., Cusidó R.M. 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 2010, 53:104-111.
78. Onrubia M., Cusidó R.M., Ramirez K., Hernández-Vázquez L., Moyano E., Bonfill M., et al. Bioprocessing of plant in vitro systems for the mass production of pharmaceutically important metabolites: paclitaxel and its derivatives. Curr Med Chem 2013, 20(7):880-891.
79. Onrubia M., Moyano E., Bonfill M., Cusidó R.M., Goossens A., Palazón J. Coronatine, a more powerful elicitor for inducing taxane biosynthesis in Taxus media cell cultures than methyl jasmonate. J Plant Physiol 2013, 170(2):211-219. [15].
80. Patel H., Krishnamurthy R. Elicitors in plant tissue culture. J Pharm Phytochem 2013, 2:60-65.
81. Pauwels L., Inzé D., Goossens A. Jasmonate-inducible gene: what does it mean?. Trends Plant Sci 2009, 14:87-91.
82. Pollier J., Moses T., González-Guzmán M., De Geyter N., Lippens S., Bossche R.V., et al. The protein quality control system manages plant defense compound synthesis. Nature 2013, 10.1038/nature12685.
83. Qian Z.G., Zhao Z.J., Xu Y., Qian X., Zhong J.J. With a newly synthesized jasmonate in fed-batch cultivation of Taxus chinensis cells. Biotechnol Bioeng 2005, 90:516-521.
84. Qiu D., Pan X., Wilson I.W., Li F., Liu M., Teng W., Zhang B. High throughput sequencing technology reveals that the taxoid elicitor methyl jasmonate regulates microRNA expression in Chinese yew (Taxus chinensis). Gene. 2009, 436:37-44.
85. Ramachandra-Raoa S., Ravishankar G.A. Plant cell cultures: chemical factories of secondary metabolites. Biotechnol Adv 2002, 20:101-153.
86. Roberts S.C., Shuler M.L. Large-scale plant cell culture. Curr Opin Biotechnol 1997, 8:154-159.
87. Sabater-Jara A.B.. Estudio de las respuestas de defensa inducidas por elicitores en cultivos de células vegetales 2013, [PhD dissertation], University of Murcia, [http://hdl.handle.net/10201/35414].
88. Sabater-Jara A.B.., Pedreño M.A. Use of β-cyclodextrins to enhance phytosterol production in cell suspension cultures of carrot (Daucus carota L.). Plant Cell Tiss Org 2013, 114:249-258.
89. Sabater-Jara A.B.., Almagro L., Belchí-Navarro S., Ferrer M.A., Ros Barceló A., Pedreño M.A. Induction of sesquiterpenes, phytoesterols and extracellular pathogenesis-related proteins in elicited cell cultures of Capsicum annuum. J Plant Physiol 2010, 167:1273-1281.
90. Sabater-Jara A.B.., Tudela L.R., López-Pérez A.J. In vitro culture of Taxus sp.: strategies to increase cell growth and taxoid production. Phytochem Rev 2010, 9:343-356.
91. Saenger W. Cyclodextrin inclusion compounds in research and industry. Angew Chem Int Ed 1980, 19:344-362.
92. Sun G., Yang Y., Xie F., Wen J.F., Wu J., Wilson I.W., et al. Deep sequencing reveals transcriptome re-programming of Taxus×media cells to the elicitation with methyl jasmonate. PLoS One 2013, 8:e62865.
93. Syklowska-Baranek K., Pietrosiuk A., Kokoszka A., Furmanowa M. Enhancement of taxane production in hairy root culture of Taxus×media var. Hicksii. J Plant Physiol 2009, 166:1950-1954.
94. Szejtli J. Utilization of cyclodextrins in industrial products and processes. J Mater Chem 1997, 7:575-587.
95. Tamogami S., Kodama O. Coronatine elicits phytoalexin production in rice leaves (Oryza sativa L.) in the same manner as jasmonic acid. Phytochemistry 2000, 54:689-694.
96. Tapia N., Zamilpa A., Bonfill M., Ventura E., Cruz-Vega D., Del Villar A., et al. Effect of the culture medium and biotic stimulation on taxane production in Taxus globosa Schltdl in vitro cultures. Acta Physiol Plant 2013, 10.1007/s11738-013-1380-0.
97. COI1 complex during jasmonate signalling. Nature 2007, 448:661-666.
98. Tyunin A.P., Kiselev K.V., Zhuralev Y.N. Effects of 5-azacytidine induced DNA demethylation on methyltransferase gene expression and resveratrol production in cell cultures of Vitis amurensis. Plant Cell Tiss Organ Cult 2012, 111:91-100.
99. Uppalapati S.R., Ayoubi P., Weng H., Palmer D.A., Mitchell R.E., Jones W., et al. The phytotoxin coronatine and methyl jasmonate impact multiple phytohormone pathways in tomato. Plant J 2005, 42:201-217.
100. Walji A.M., MacMillan D.W.C. Strategies to bypass the taxol problem. Enantioselective cascade catalysis, a new approach for the efficient construction of molecular complexity. Synlett 2007, 10:1477-1489.
101. Wang D.M., Zhou Y., Zhang Y.N., Wang W. A study on superior tree selection of Taxus wallichiana. J. West China For. Sci. 2007, 4:1-10.
102. Wani M.C., Taylor H.L., Wall M.E. Plant antitumor agents VI. The isolation and structure of taxol: a novel antileukemic and antitumour agent from Taxus brevifolia. J Am Chem 1971, 93:2325-2327.
103. Wasternack C. Action of jasmonates in plant stress responses and development - applied aspects. Biotechnol Adv 2014, 32(1):31-39.
104. Wilson S.A., Roberts S.C. Recent advances towards development and commercialization of plant cell culture processes for the synthesis of biomolecules. Plant Biotechnol J 2012, 10(3):249-268.
105. Wu Q., Sun C., Luo H., Li Y., Niu Y., Sun Y., et al. Transcriptome analysis of Taxus cuspidata needles based on 454 pyrosequencing. Planta Med 2011, 77:394-400.
106. Xiao J., Liang D., Liu Y., Zhang H., Liu Y., Zhao H., et al. Taxol, a microtubule stabilizer, improves cardiac functional recovery during postischemic reperfusion in rat in vitro. Cardiovasc Ther 2012, 30:12-30.
107. Xu M., Jin H., Dong J., Zhang M., Xu X., Zhou T. Abscisic acid plays critical role in ozone-induced taxol production of Taxus chinensis suspension cell cultures. Biotechnol Prog 2011, 27(5):1415-1420.
108. Yao N., Imai S., Tada Y., Nakayashiki H., Tosa Y., Park P., et al. Apoptotic cell death is a common response to pathogen attack in oats. Mol Plant Microbe Interact 2002, 15:1000-1007.
109. Yukimune Y., Tabata H., Higashi Y., Hara Y. Methyl jasmonate-induced overproduction of paclitaxel and baccatin III in Taxus cell suspension cultures. Nat Biotechnol 1996, 14(9):1129-1132.
110. Zamboni A., Gatto P., Cestaro A., Pilati S., Viola R., Mattivi F., et al. Grapevine cell early activation of specific responses to DIMEB, a resveratrol elicitor. BMC Genomics 2009, 10:363-376.
111. Zhao Y., Thilmony R., Bender C.L., Schaller A., He S.Y., Howe G.A. Virulence systems of Pseudomonas syringae pv. tomato promote bacterial speck disease in tomato by targeting the jasmonate signaling pathway. Plant J 2003, 36:485-499.
112. Zhao J., Davis L.C., Verpoorte R. Elicitor signal transduction leading to production of plant secondary metabolites. Biotechnol Adv 2005, 23:283-333.