Plant Cell Reports

, Volume 24, Issue 11, pp 677–682 | Cite as

Ajmalicine production in methyl jasmonate-induced Catharanthus roseus cell cultures depends on Ca2+ level

Physiology and Biochemistry

Abstract

Cytosolic Ca2+ and jasmonate mediate signals that induce defense responses in plants. In this study, the interaction between Ca2+ and methyl jasmonate (MJ) in modulating defense responses was investigated by monitoring ajmalicine production in Catharanthus roseus suspension cultures. C. roseus suspensions were treated with nine combinations of CaCl2 (3, 23, and 43 mM) and MJ (0, 10, and 100 μM) on day 6 of growth. Increased Ca2+ influx through the addition of extracellular CaCl2 suppressed ajmalicine production in MJ-induced cultures. The highest ajmalicine production (4.75 mg/l) was observed when cells were treated with a low level of calcium (3 mM) combined with a high level of MJ (100 μM). In the presence of 3 mM CaCl2 in the medium, the addition of Ca2+ chelator EGTA (1, 2.5, and 5 mM) or Ca2+ channel blocker verapamil (1, 10, and 50 μM) to MJ-induced (100 μM) cultures on day 6 also inhibited ajmalicine production at higher levels of the Ca2+ inhibitors. Hence, ajmalicine production in MJ-induced C. roseus cultures depended on the intracellular Ca2+ concentration and a low extracellular Ca2+ concentration (3 mM) enhanced MJ-induced ajmalicine production.

Keywords

Ajmalicine Calcium Catharanthus roseus Methyl jasmonate Signal transduction 

References

  1. Aerts RJ, Gisi D, De Carolis E, De Luca V, Bauman TW (1994) Methyl jasmonate vapor increases the developmentally controlled synthesis of alkaloids in Catharanthus and Cinchona seedlings. Plant J 5:635–643CrossRefGoogle Scholar
  2. Bramble JL, Graves DJ (1991) Calcium and phosphate effects on growth and alkaloid production in Coffea arabica: experimental results and mathematical model. Biotechnol Bioeng 37:859–868CrossRefGoogle Scholar
  3. Cheng SH, Willmann MR, Chen HC, Sheen J (2002) Calcium signaling through protein kinases. The Arabidopsis calcium-dependent protein kinase gene family. Plant Physiol 129:469–485Google Scholar
  4. Contin A, van der Heijden R, ten Hoopen HJG, Verpoorte R (1998) The inoculum size triggers tryptamine or secologanin biosynthesis in a Catharanthus roseus cell culture. Plant Sci 139:205–211CrossRefGoogle Scholar
  5. Dmitriev A, Djatsok J, Grodzinsky D (1996) The role of Ca2+ in elicitation of phytoalexin synthesis in cell culture of onion. Plant Cell Rep 15:945–948CrossRefGoogle Scholar
  6. Ellard-Ivey M, Douglas CJ (1996) Role of jasmonates in the elicitor- and wound-inducible expression of defense genes in parsley and transgenic tobacco. Plant Physiol 112:183–192PubMedGoogle Scholar
  7. Farmer EE, Ryan CA (1990) Interplant communication: airborne methyl jasmonate induces synthesis of proteinase inhibitors in plant leaves. Proc Natl Acad Sci USA 87:7713–7716PubMedCrossRefGoogle Scholar
  8. Gamborg OL, Miller RA, Ojima K (1968) Nutrient requirements of suspension cultures of soybean root cells. Exp Cell Res 50:155–158CrossRefGoogle Scholar
  9. Gantet P, Imbault N, Thiersault M, Doireau P (1998) Necessity of a functional octadecanoid pathway for indole alkaloid synthesis by Catharanthus roseus cell suspensions cultured in an auxin-starved medium. Plant Cell Physiol 39:220–225Google Scholar
  10. Gundlach H, Muller MJ, Kutchan TM, Zenk MH (1992) Jasmonic acid is a signal transducer in elicitor-induced plant cell cultures. Proc Natl Acad Sci USA 89:2389–2393PubMedCrossRefGoogle Scholar
  11. Kurosaki F, Tsurusawa Y, Nishi A (1987) The elicitation of phytoalexins by Ca2+ and cyclic AMP in carrot cells. Phytochemistry 26:1919–1923CrossRefGoogle Scholar
  12. Lee-Parsons CWT, Ertürk S, Tengtrakool J (2004) Enhancement of ajmalicine production in Catharanthus roseus cell cultures with methyl jasmonate is dependent on timing and dosage of elicitation. Biotechnol Lett 26(20):1595–1599CrossRefPubMedGoogle Scholar
  13. Memelink J, Verpoorte R, Kijne W (2001) ORCAnization of jasmonate-responsive gene expression in alkaloid metabolism. Trends Plant Sci 6:212–219CrossRefPubMedGoogle Scholar
  14. Menke FLH, Parchmann S, Mueller MJ, Kijne JW, Memelink J (1999a) Involvement of the octadecanoid pathway and protein phosphorylation in fungal elicitor-induced expression of terpenoid indole alkaloid biosynthetic genes in Catharanthus roseus. Plant Physiol 119:1289–1296CrossRefPubMedGoogle Scholar
  15. Menke FLH, Champion A, Kijne JW, Memelink J (1999b) A novel jasmonate- and elicitor-responsive element in the periwinkle secondary metabolite biosynthetic gene Str interacts with a jasmonate- and elicitor-inducible AP2-domain transcription factor, ORCA2. EMBO J 18:4455–4463CrossRefPubMedGoogle Scholar
  16. Merillon J-M, Liu D, Huguet F, Chenieux J-C, Rideau M (1991) Effects of calcium entry blockers and calmodulin inhibitors on cytokinin-enhanced alkaloid accumulation in Catharanthus roseus cell cultures. Plant Physiol Biochem 29(3):289–296Google Scholar
  17. Moreno-Valenzuela OA, Minero-Garcia Y, Chan W, Mayer-Geraldo E, Carbajal E, Loyola-Vargas VM (2003) Increase in the indole alkaloid production and its excretion into the culture medium by calcium antagonists in Catharanthus roseus hairy roots. Biotechnol Lett 25:1345–1349CrossRefPubMedGoogle Scholar
  18. Ning W, Wang JX, Liu YM, Li N, Cao R-Q (1998) The effects of Ca2+ during the elicitation of shikonin derivatives in Onosma paniculatum cells. In Vitro Cell Dev Biol Plant 34:261–265CrossRefGoogle Scholar
  19. Odjakova M, Hadjiivanova C (2001) The complexity of pathogen defense in plants. Bulg J Plant Physiol 27:101–109Google Scholar
  20. Radman R, Saez T, Bucke C, Keshavarz T (2003) Elicitation of plants and microbial cell systems. Biotechnol Appl Biochem 37:91–102CrossRefPubMedGoogle Scholar
  21. Stab MR, Ebel J (1987) Effects of Ca2+ on phytoalexin induction by fungal elicitor in soybean cells. Arch Biochem Biophys 257:416–423CrossRefPubMedGoogle Scholar
  22. Talarczyk A, Hennig J (2001) Early defense responses in plants infected with pathogenic organisms. Cell Mol Biol Lett 6:955–970PubMedGoogle Scholar
  23. Van der Fits L, Memelink J (2000a) ORCA3, a jasmonate-responsive transcriptional regulator of plant primary and secondary metabolism. Science 289:295–297CrossRefPubMedGoogle Scholar
  24. Van der Fits L, Memelink J (2001) The jasmonate-inducible AP2/ERF-domain transcription factor ORCA3 activates gene expression via interaction with a jasmonate-responsive promoter element. Plant J 25:43–53CrossRefPubMedGoogle Scholar
  25. Van der Fits L, Zhang H, Menke FLH, Deneka M, Memelink J (2000b) 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-independent signal transduction pathway. Plant Mol Biol 44:675–685CrossRefPubMedGoogle Scholar
  26. Wong PL, Royce AJ, Lee-Parsons CWT (2004) Improved ajmalicine production and recovery from Catharanthus roseus suspensions with increased product removal rates. Biochem Eng J 21:253–258CrossRefGoogle Scholar
  27. Zhao J, Sakai K (2003) Multiple signaling pathways mediate fungal elicitor-induced β-thujaplicin biosynthesis in Cupressus lusitanica cell cultures. J Exp Bot 54:647–656CrossRefPubMedGoogle Scholar
  28. Zhao J, Hu Q, Guo YQ, Zhu WH (2001) Elicitor-induced indole alkaloid biosynthesis in Catharanthus roseus cell cultures is related to Ca2+ influx and the oxidative burst. Plant Sci 161:423–431CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2005

Authors and Affiliations

  1. 1.Chemical Engineering Department, 342 Snell Engineering Center360 Huntington Avenue, Northeastern UniversityBostonUSA

Personalised recommendations