Low Levels of Gibberellic Acid Control the Biosynthesis of Ajmalicine in Catharanthus roseus Cell Suspension Cultures

Abstract

In periwinkle cell suspensions, amounts of gibberellic acid ranging from 10^– 10 M to 10^– 7 M significantly antagonized, in a dose-dependant manner, the stimulation of ajmalicine biosynthesis by cytokinins (CKs). This inhibitory effect was strictly correlated with the abolition of the expression of two genes encoding enzymes of the monoterpenoid indole alkaloid (MIA) biosynthetic pathway and was normally upregulated after CK treatments. Moreover, low concentrations of the gibberellin biosynthesis inhibitor paclobutrazol could reverse the inhibitory effects of low auxin levels on ajmalicine accumulation in the cells. On the other hand, gibberellic acid could not affect the expression of two type-A response regulators considered to be CK primary response genes in periwinkle cells. The antagonistic effects of gibberellins and cytokinins on MIA biosynthesis and their possible impact on elements of the signal transduction are discussed.

Key words

gibberellin - cytokinin - monoterpenoid indole alkaloids - Catharanthus roseus - Apocynaceae

References

• 1 van Der Heijden R, Jacobs D I, Snoeijer W, Hallard D, Verpoorte R. The Catharanthus alkaloids: pharmacognosy and biotechnology.  Curr Med Chem. 2004;  11 607-28
• 2 Giglioli-Guivarc′h N, Courdavaut V, Oudin A, Creche J, St-Pierre B. Madagascar periwinkle, an attractive model for studying the control of the biosynthesis of terpenoid derivative compounds. Floriculture Ornamental Plant Biotechnol Advances Topical 2006: 496-506
• 3 Décendit A, Liu D, Ouelhazi L, Doireau P, Mérillon J M, Rideau M. Cytokinin-enhanced accumulation of indole alkaloids in Catharanthus roseus cell cultures.The factors affecting the cytokinin response.  Plant Cell Reports. 1992;  11 400-3
• 4 Papon N, Bremer J, Vansiri A, Andreu F, Rideau M, Creche J. Cytokinin and ethylene control indole alkaloid production at the level of the MEP/terpenoid pathway in Catharanthus roseus suspension cells.  Planta Med. 2005;  71 572-4
• 5 Oudin A, Mahroug S, Courdavault V, Hervouet N, Zelwer C, Rodríguez-Concepción . et al . Spatial distribution and hormonal regulation of gene products from methyl erythritol phosphate and monoterpene-secoiridoid pathways in Catharanthus roseus. .  Plant Mol Biol. 2007;  65 13-30
• 6 Fu X, Harberd N P. Auxin promotes Arabidopsis root growth by modulating gibberellin response.  Nature. 2003;  421 740-3
• 7 Ross J J, O′Neill D P, Smith J J, Kerckhoffs L H, Elliott R C. Evidence that auxin promotes gibberellin A1 biosynthesis in pea.  Plant J. 2000;  21 547-52
• 8 Greenboim-Wainberg Y, Maymon I, Borochov R, Alvarez J, Olszewski N, Ori N. et al . Cross talk between gibberellin and cytokinin: the Arabidopsis GA response inhibitor SPINDLY plays a positive role in cytokinin signaling.  Plant Cell. 2005;  17 92-102
• 9 Jasinski S, Piazza P, Craft J, Hay A, Woolley L, Rieu I. et al . KNOX action in Arabidopsis is mediated by coordinate regulation of cytokinin and gibberellin activities.  Curr Biol. 2005;  15 1560-5
• 10 Weiss D, Ori N. Mechanisms of cross talk between gibberellin and other hormones.  Plant Physiol. 2007;  144 1240-6
• 11 Hinderer W, Petersen M, Seitz H. Inhibition of flavonoid biosynthesis by gibberellic acid in cell suspension cultures of Daucus carota L. .  Planta. 1984;  160 544-9
• 12 Carpin S, Ouelhazi L, Filali M, Chénieux J C, Rideau M, Hamdi S. The relationship between the accumulation of a 28kD polypeptide and that of indole alkaloids in Catharanthus roseus cell suspension cultures.  J Plant Physiol. 1997;  150 452-7
• 13 Gamborg O L, Miller R A, Ojima K. Nutrients requirements of suspension cultures of soybean root cells.  Exp Cell Res. 1968;  50 151-68
• 14 Menke F L, Parchmann S, Mueller M J, Kijne J W, Memelink J. Involvement of the octadecanoid pathway and protein phosphorylation in fungal elicitor-induced expression of terpenoid indole alkaloid biosynthetic genes in Catharanthus roseus. .  Plant Physiol. 1999;  119 1286-96
• 15 Yahia A, Kevers C, Gaspar T, Chénieux J C, Rideau M, Crèche J. Cytokinins and ethylene stimulate indole alkaloid accumulation in cell suspension cultures of Catharanthus roseus by two distinct mechanisms.  Plant Sci. 1998;  133 9-15
• 16 O′Neill D P, Ross J J. Auxin regulation of the gibberellin pathway in pea.  Plant Physiol. 2002;  130 1974-82
• 17 Nemhauser J L, Hong F, Chory J. Different plant hormones regulate similar processes through largely non overlapping transcriptional responses.  Cell. 2006;  126 467-75
• 18 Amini A, Glevarec G, Andreu F, Reverdiau P, Rideau M, Creche J. Effects of phosphatidic acid on cytokinin signal transduction in periwinkle cells.  J Plant Growth Regul. 2008;  27 394-99
• 19 El-Sayed M, Verpoorte R. Growth, metabolic profiling and enzymes activities of Catharanthus roseus seedlings treated with plant growth regulators.  Plant Growth Regul. 2004;  44 53-8
• 20 Abdul Jaleel C, Gopi R, Manivannan P, Sankar B, Kishorekumar A, Panneerselvam R. Antioxidant potentials and ajmalicine accumulation in Catharanthus roseus after treatment with gibberellic acid.  Colloids Surf B Biointerfaces. 2007;  60 195-200
• 21 Ohlsson A B, Berglund T. Gibberellic acid-induced changes in glutathione metabolism and anthocyanin content in plant tissue.  Plant Cell Tissue Organ Cult. 2001;  64 77-80
• 22 Cai G, Li G, Ye H, Li G. Hairy root culture of Artemisia annua L. by Ri plasmid transformation and biosynthesis of artemisinin.  China J Biotechnol. 1995;  11 227-35
• 23 Smith T C, Weathers P J, Cheetham R D. Effects of gibberellic acid on hairy root cultures of Artemisia annua: Growth and artemisinin production.  In Vitro Cell Dev Biol Plant. 1997;  33 75-9
• 24 Dupraz J M, Christen P, Kapetanidis I. Tropane Alkaloids in transformed roots of Datura quercifolia. .  Planta Med. 1994;  60 158-62
• 25 Davies P J. PLANT HORMONES. Biosynthesis, Signal Transduction, Action!, 3rd edition. Dordrecht/Boston/London; Kluwer Academic Publishers 2004: 750-1
• 26 Collu G, Unver N, Peltenburg-Looman A M, van der Heijden R, Verpoorte R, Memelink J. Geraniol 10-hydroxylase, a cytochrome P450 enzyme involved in terpenoid indole alkaloid biosynthesis.  FEBS Lett. 2001;  508 215-20
• 27 Weiss D, van der Luit A, Knegt E, Vermeer E, Mol J NM, Kooter J M. Identification of endogenous gibberellins in Petunia flowers. Induction of anthocyanin biosynthetic gene expression and the antagonistic effect of abscisic acid.  Plant Physiol. 1995;  107 695-702