Jasmonic acid effect on the fatty acid and terpenoid indole alkaloid accumulation in cell suspension cultures of catharanthus roseus

Molecules

Volumn 19, Issue 7, 2014, Pages 10242-10260

  Goldhaber Pasillas, Guitele Dalia ^a   Mustafa, Natali Rianika ^a   Verpoorte, Robert ^a  

^a LEIDEN UNIVERSITY   (Netherlands)

Author keywords

Cell suspension cultures; Fatty acids; Jasmonic acid; Madagascar periwinkle; Multivariate data analysis; Terpenoid indole alkaloids

Indexed keywords

CYCLOPENTANE DERIVATIVE; FATTY ACID; JASMONIC ACID; OXYLIPIN; RAUWOLFIA ALKALOID;

BASAL METABOLIC RATE; BIOSYNTHESIS; CATHARANTHUS; CELL CULTURE; DRUG EFFECTS; METABOLISM; PHYSIOLOGICAL STRESS; PLANT CELL; SECONDARY METABOLISM;

BASAL METABOLISM; BIOSYNTHETIC PATHWAYS; CATHARANTHUS; CELLS, CULTURED; CYCLOPENTANES; FATTY ACIDS; OXYLIPINS; PLANT CELLS; SECOLOGANIN TRYPTAMINE ALKALOIDS; SECONDARY METABOLISM; STRESS, PHYSIOLOGICAL;

EID: 84904811935     PISSN: None     EISSN: 14203049     Source Type: Journal    
DOI: 10.3390/molecules190710242     Document Type: Article

References (61)

1. Millar, A.A.; Smith, M.A.; Kunst, L. All fatty acids are not equal: Discrimination in plant membrane lipids. Trends Plant. Sci. 2000, 5, 95-101.
2. Kachroo, A.; Kachroo, P. Fatty acid-derived signals in plant defense. Ann. Rev. Phytopathol. 2009, 47, 153-176.
3. Savchenko, T.; Walley, J.W.; Chehab, E.W.; Xiao, Y.; Kaspi, R.; Pye, M.F.; Mohamed, M.E.; Lazarus, C.M.; Bostock, R.M.; Dehesh, K. Arachidonic acid: An evolutionary conserved signaling molecule modulates plant stress signaling networks. Plant Cell 2010, 22, 3191-3205.
4. Feussner, I.; Wasternack, C. The lipoxygenase pathway. Ann. Rev. Plant Biol. 2002, 53, 275-297.
5. MacCarthy, J.J.; Stumpf, P.K. The effect of different temperatures on fatty- Acid synthesis and polyunsaturation in cell suspension cultures. Planta 1980, 147, 389-395.
6. Kazemi Shahandashti, S.S.; Maali Amiri, R.; Zeinali, H.; Sanaz Ramezanpour, S.S. Change in membrane fatty acid compositions and cold-induced responses in chickpea. Mol. Biol. Rep. 2013, 40, 893-903.
7. Elkahoui, S.; Smaoui, A.; Zarrouk, M.; Ghir, R.; Limam, F. Salt-induced lipid changes in Catharanthus roseus cultured cell suspensions. Phytochemistry 2004, 65, 1911-1917.
8. Creelman, R.A.; Mullet, J.E. Biosynthesis and action of jasmonates in plants. Ann. Rev. Plant Physiol. Plant. Mol. Biol. 1997, 48, 355-381.
9. Wasternack, C.; Hause, B. Jasmonates and octadecanoids: Signals in plant stress responses and development. Prog. Nucleic Acid. Res. Mol. Biol. 2002, 72, 165-221.
10. Wasternack, C.; Forner, S.; Strnad, M.; Hause, B. Jasmonates in flower and seed development. Biochimie 2013, 95, 79-85.
11. De Domenico, S.; Bonsegna, S.; Horres, R.; Pastor, V.; Taurino, M.; Poltronieri, P.; Imtiaz, M.; Kahl, G.; Flors, V.; Winter, P.; et al. Transcriptomic analysis of oxylipins biosynthesis genes and chemical profiling reveal early induction of jasmonates in chickpea roots under drought stress. Plant. Physiol. Biochem. 2012, 61, 115-122.
12. Collu, G.; Unver, N.; Peltenburg-Looman, A.M.G.; van der Heijden, R.; Verpoorte, R.; Memelink, J. Geraniol 10-hydroxylase, a cytochrome P450 enzyme involved in terpenoid indole alkaloid biosynthesis. FEBS Lett. 2001, 508, 215-220.
13. Lee-Parsons, C.W.T.; Ertürk, S.; Tengtrakool, J. Enhancement of ajmalicine production in Catharanthus roseus cell cultures with methyl jasmonate is dependent on timing and dosage of elicitation. Biotechnol. Lett. 2004, 0, 1595-1599.
14. Li, C.Y.; Leopold, A.L.; Sander, G.W.; Shanks, J.V.; Zhao, L.; Gibson, S.I. The ORCA2 transcription factor plays a key role in regulation of the terpenoid indole alkaloid pathway. BMC Plant. Biol. 2013, 13, 155.
15. Memelink, J.; Verpoorte, R.; Kijne, J.W. ORCAnization of jasmonate-responsive gene expression in alkaloid metabolism. Trends Plant. Sci. 2001, 6, 212-219.
16. Wei, S. Methyl jasmonic acid induced expression pattern of terpenoid indole alkaloid pathway genes in Catharanthus roseus seedlings. Plant Growth Reg. 2010, 61, 243-251.
17. Moreno, P.R.H.; Poulsen, C.; van der Heijden, R.; Verpoorte, R. Effects of elicitation on different metabolic pathways in Catharanthus roseus (L.) G. Don cell suspension cultures. Enz. Microb. Technol. 1996, 18, 99-107.
18. Vázquez-Flota, F.; Hernández-Domínguez, E.; Miranda-Ham, M.L.; Monforte-González, M. A differential response to chemical elicitors in Catharanthus roseus in vitro cultures. Biotechnol. Lett. 2009, 31, 591-595.
19. Glauser, G.; Dubugnon, L.; Mousavi, S.A.R.; Rudaz, S.; Wolfender, J.L.; Farmer, E.E. Velocity estimates for signal propagation leading to systemic jasmonic acid accumulation in wounded Arabidopsis. J. Biol. Chem. 2009, 284, 34506-34513.
20. Simkin, A.J.; Miettinen, K.; Claudel, P.; Burlat, V.; Guirimand, G.; Courdavault, V.; Papon, N.; Meyer, S.; Godet, S.; St-Pierre, B.; et al. Characterization of the plastidial geraniol synthase from Madagascar periwinkle which initiates the monoterpenoid branch of the alkaloid pathway in internal phloem associated parenchyma. Phytochemistry 2013, 85, 36-43.
21. Toivonen, L.; Laakso, S.; Rosenqvist, H. The effect of temperature on growth, indole alkaloid accumulation and lipid composition of Catharanthus roseus cell suspension cultures. Plant Cell Rep. 1992, 11, 390-394.
22. López, M.G.; Sánchez-Mendoza, I.R.; Ochoa-Alejo, N. Comparative study of volatile components and fatty acid of plants and in vitro cultures of parsley (Petroselinum crispum (Mill) Nym ex Hill. J. Agric. Food Chem. 1999, 47, 3292-3296.
23. MacCarthy, J.J.; Stumpf, P.K. Tissue culture of plants for studies of lipid metabolism. Methods Enzymol. 1981, 72, 754-768.
24. Radwan, S.S.; Mangold, H.K.; Spener, F. Lipids in plant tissue cultures. III. Very long-chain fatty acids in the lipids of callus cultures and suspension cultures. Chem. Phys. Lipids 1974, 13, 103-107.
25. Leathers, R.R.; Scragg, A.H. The effect of different temperatures on the growth, lipid content and fatty acid composition of Theobroma cacao cell suspension cultures. Plant Sci. 1989, 62, 217-227.
26. Pandey-Rai, S.; Rao Mallavarapu, G.; Naqvi, A.A.; Yadav, A.N.; Kumar Rai, S.; Srivastava, S.; Singh, D.; Mishra, R.; Kumar, S. Volatile components of leaves and flowers of periwinkle Catharanthus roseus (L.) Don from New Delhi. Flav. Fragr. J. 2006, 21, 427-430.
27. Brun, G.; Bessière, J.M.; Dijoux-Franca, M.G.; David, B.; Mariotte, A.M. Volatile components of Catharanthus roseus (L.) Don (Apocynaceae). Flav. Fragr. J. 2001, 16, 116-119.
28. Guedes De Pinho, P.; Gonçalves, R.F.; Valentão, P.; Pereira, D.M.; Seabra, R.M.; Andrade, P.B.; Sotomayor, M. Volatile composition of Catharanthus roseus (L.) Don using solid-phase microextraction and gas chromatography/mass spectrometry. J. Pharm. Biomed. Anal. 2009, 49, 674-685.
29. Rezanka, T.; Sigler, K. Odd-numbered very-long-chain fatty acids from the microbial, animal and plant kingdoms. Prog. Lipid Res. 2009, 48, 206-238.
30. Carriere, F.; Chagvardieff, P.; Gil, G.; Pean, M.; Sigoillot, J.C.; Tapie, P. Fatty acid patterns of neutral lipids from seeds, leaves and cell suspension cultures of Euphorbia characias. Phytochemistry 1992, 31, 2351-2353.
31. Gemmrich, A.R.; Schraudolf, H. Fatty acid composition of lipids from differentiated tissues and cell cultures of Euonymus europaeus. Chem. Phys. Lipids 1980, 26, 259-264.
32. Hansen, C.E.; Rossi, P. Effects of culture condition on accumulation of arachidonic and eicosapentaenoic acids cultured cells of Rhytidiadelphus squarrosus and Eurhynchium striatum. Phytochemistry 1991, 30, 1837-1841.
33. Chiou, S.Y.; Su, W.W.; Su, Y.C. Optimizing production of polyunsaturated fatty acids in Marchantia polymorpha cell suspension culture. J. Biotechnol. 2001, 85, 247-257.
34. Miersch, O.; Neumerkel, J.; Dippe, M.; Stenzel, I.; Wasternack, C. Hydroxylated jasmonates are commonly occurring metabolites of jasmonic acid and contribute to a partial switch-off in jasmonate signaling. New Phytol. 2008, 177, 114-127.
35. Fonseca, S.; Chini, A.; Hamberg, M.; Adie, B.; Porzel, A.; Kramell, R.; Miersch, O.; Wasternack, C.; Solano, R. (+)-7-iso-Jasmonoyl-L-isoleucine is the endogenous bioactive jasmonate. Nat. Chem. Biol. 2009, 5, 344-350.
36. Conconi, A.; Miquel, M.; Browse, J.A.; Ryan, C.A. Intracellular levels of free linolenic and linoleic acids increase in tomato leaves in response to wounding. Plant. Physiol. 1996, 111, 797-803.
37. Mueller, M.J.; Brodschelm, W.; Spannagl, E.; Zenk, M.H. Signaling in the elicitation process is mediated through the octadecanoid pathway leading to jasmonic acid. Proc. Natl. Acad. Sci. USA 1993, 90, 7490-7494.
38. Dewir, Y.H.; Chakrabarty, D.; Wu, C.H.; Hahn, E.J.; Jeon, W.K.; Paek, K.Y. Influences of polyunsaturated fatty acids (PUFAs) on growth and secondary metabolite accumulation in Panax ginseng C.A. Meyer adventitious roots cultures in air-lift bioreactors. South Afr. J. Bot. 2010, 76, 354-358.
39. Wu, C.H.; Popova, E.V.; Hahn, E.J.; Paek, K.Y. Linolenic and α-linolenic fatty acids affect biomass and secondary metabolite production and nutritive properties of Panax. ginseng adventitious roots cultured in bioreactors. Biochem. Eng. J. 2009, 47, 109-115.
40. Gundlach, H.; Zenk, M.H. Biological activity and biosynthesis of pentacyclic oxylipins: The linoleic acid pathway. Phytochemistry 1998, 47, 527-537.
41. Véronési, C.; Pouénat, M.L.; Rickauer, M.; Esquerrê-Tugayé, M.T. Regulation of tobacco lipoxygenase by methyl jasmonate and fatty acids. Comp. Rend Acad. Sci. Series III Sci. Vie 1999, 322, 491-497.
42. El-Sayed, M.; Verpoorte, R. Effect of phytohormones on growth and alkaloid accumulation by a Catharanthus roseus cell suspension cultures fed with alkaloid precursors tryptamine and loganin. Plant Cell Tis. Org. Cult. 2002, 68, 265-270.
43. Saiman, M.Z.; Mustafa, R.N.; Pomahacova, B.; Verbenne, M.; Verpoorte, R.; Choi, Y.H.; Schulte, A.E. Analysis of metabolites in the terpenoid pathway of Catharanthus roseus cell suspensions. Plant Cell Tissue Organ. Cult. 2014, 117, 225-239.
44. Endo, T.; Goodbody, A.; Misawa, M. Alkaloid production in root and shoot cultures of Catharanthus roseus. Planta Med. 1987, 53, 479-482.
45. Vázquez-Flota, F.; de Luca, V.; Carrillo-Pech, M.; Canto-Flick, A.; Miranda-Ham, M.L. Vindoline biosynthesis is transcriptionally blocked in Catharanthus roseus cell suspension cultures. Mol. Biotechnol. 2002, 22, 1-8.
46. Shukla, A.K.; Shasany, A.K.; Verma, R.K.; Gupta, M.M.; Mathur, A.K.; Khanuja, S.P.S. Influence of cellular differentiation and elicitation on intermediate and late steps of terpenoid indole alkaloid biosynthesis in Catharanthus roseus. Protoplasma 2010, 242, 35-47.
47. Besseau, S.; Kellner, F.; Lanoue, A.; Thamm, A.M.K.; Salim, V.; Schneider, B.; Geu-Flores, F.; Höfer, R.; Guirimand, G.; Guihur, A.; et al. A pair of tabersonine 16-hydroxylases initiates the synthesis of vindoline in an organ-dependent manner in Catharanthus roseus. Plant Physiol. 2013, 163, 1792-1803.
48. Verpoorte, R.; van der Heijden, R.; Moreno, P.R.H. Biosynthesis of terpenoid indole alkaloids in Catharanthus roseus cells. In The Alkaloids; Cordell, G.A., Ed.; Academic Press: Waltham, MA, USA, 1997; Volume 49, pp. 221-299.
49. Schröder, G.; Unterbusch, E.; Kaltenbach, M.; Schmidt, J.; Strack, D.; de Luca, V.; Schröder, J. Light-induced cytochrome P450-dependent enzyme in indole alkaloid biosynthesis: Tabersonine 16-hydroxylase. FEBS Lett. 1999, 458, 97-102.
50. St-Pierre, B.; de Luca, V. A cytochrome P-450 monooxygenase catalyzes the first step in the conversion of tabersonine to vindoline in Catharanthus roseus. Plant Physiol. 1995, 109, 131-139.
51. Gundlach, H.; Müeller, M.J.; Kutchan, T.M.; Zenk, M.H. Jasmonic acid is a signal transducer in elicitor-induced plant cell cultures. Proc. Natl. Acad. Sci. USA 1992, 89, 2389-2393.
52. Bell, E.; Creelman, R.A.; Mullet, J.E. A chloroplast lipoxygenase is required for wound-induced jasmonic acid accumulation in Arabidopsis. Proc. Natl. Acad. Sci. USA 1995, 92, 8675-8679.
53. Chauvin, A.; Caldelari, D.; Wolfender, J.L.; Farmer, E.E. Four lipoxygenases contribute to rapid jasmonate synthesis in wounded Arabidopsis thaliana leaves: A role for lipoxygenase 6 in response to long-distance wound signals. New Phytol. 2013, 197, 566-575.
54. Peebles, C.A.M.; Shanks, J.V.; San, K.Y. The role of the octadecanoid pathway in the production of terpenoid indole alkaloids in Catharanthus roseus hairy roots under normal and UV-B stress conditions. Biotechnol. Bioeng. 2009, 103, 1248-1254.
55. Lee-Parsons, C.W.T.; Ertürk, S. Ajmalicine production in methyl jasmonate-induced Catharanthus roseus cell cultures depends on Ca2+ level. Plant Cell Rep. 2005, 24, 677-682.
56. Van der Fits, L.; Zhang, H.; Menke, F.L.H.; Deneka, M.; Memelink, J. A Catharanthus roseus BPF-1 homologue interacts with an elicitor-responsive region of the secondary metabolite biosynthetic gene Str. and is induced by elicitor via a JA-dependent signal transduction pathway. Plant Mol. Biol. 2000, 44, 675-685.
57. Hisamatsu, Y.; Goto, N.; Hasegawa, K.; Shigemori, H. Arabidopsides A and B, tow new oxylipins from Arabidopsis thaliana. Tehtrah. Lett. 2003, 44, 5553-5556.
58. Hisamatsu, Y.; Goto, N.; Sekiguchi, M.; Hasegawa, K.; Shigemori, H. Oxylipins arabidopsides C and D from Arabidopsis thaliana. J. Nat. Prod. 2005, 68, 600-603.
59. Gamborg, O.L.; Miller, R.A.; Ojima, K. Nutrient requirements of suspension cultures of soybean root cells. Exp. Cell. Res. 1968, 50, 151-158.
60. Moreno, P.R.H.; van de Heijden, R.; Verpoorte, R. Effect of terpenoid precursor feeding and elicitation on formation of indole alkaloids in cell suspension cultures or Catharanthus roseus. Plant Cell Rep. 1993, 12, 702-705.
61. Tikhomiroff, C.; Jolicoeur, M. Screening of Catharanthus roseus secondary metabolites by high-performance liquid chromatography. J. Chromatogr. A 2002, 955, 87-93.