Skip to main content
Springer Nature Link
Log in

Differential induction by methyl jasmonate of genes encoding ornithine decarboxylase and other enzymes involved in nicotine biosynthesis in tobacco cell cultures

  • Published:
Plant Molecular Biology Aims and scope Submit manuscript

Abstract

A cDNA of tobacco BY-2 cells corresponding to an mRNA species which was rapidly induced by methyl jasmonate (MeJA) in the presence of cycloheximide (CHX) was found to encode ornithine decarboxylase (ODC). Another cDNA from a MeJA-inducible mRNA encoded S-adenosylmethionine synthase (SAMS). Although these enzymes could be involved in the biosynthesis of polyamines, the level of putrescine, a reaction product of ODC, increased slowly and while the levels of spermidine and spermine did not change following treatment of cells with MeJA. However, N-methylputrescine, which is a precursor of pyrrolidine ring of nicotine, started to increase shortly after MeJA-treatment of cells and the production of nicotine occured thereafter. The levels of mRNA for arginine decarboxylase (ADC), an alternative enzyme for putrescine synthesis, and that for S-adenosylmethionine decarboxylase (SAMDC), required for polyamine synthesis, were not affected by MeJA. In addition to mRNAs for ODC and SAMS, mRNA for putrescine N-methyltransferase (PMT) was also induced by MeJA. Unlike the MeJA-induction of ODC mRNA, MeJA-induction of SAMS and PMT mRNAs were blocked by CHX. The level of ODC mRNA declined after 1 to 4 h following MeJA treatment, while the levels of mRNAs for SAMS and PMT continued to increase. Auxin significantly reduced the MeJA-inducible accumulation of mRNAs for ODC, SAMS and PMT. These results indicate that MeJA sequentially induces expression of a series of genes involved in nicotine biosynthesis by multiple regulatory mechanisms.p>

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. Aerts RJ, Gisi D, De Carolis E, De Luca V, Baumann TW: Methyl jasmonate vapor increases the developmentally controlled synthesis of alkaloids in Catharanthus and Cinchona seedlings. Plant J 5: 635–643 (1994).

    Google Scholar 

  2. Baldwin IT, Schmelz EA, Ohnmeiss TE: Wound-induced changes in root and shoot jasmonic acid pools correlate with induced nicotine synthesis in Nicotiana sylvestris Spegazzini and Comes. J Chem Ecol 20: 2139–2157 (1994).

    Google Scholar 

  3. Baldwi n IT, Zhang Z-P, Diab N, Ohnmeiss TE, McCloud ES, Lynds GY, Schmelz EA: Quantification, correlations and manipulations of wound-induced changes in jasmonic acid and nicotine in Nicotiana sylvestris. Planta 201: 397–404 (1997).

    Google Scholar 

  4. Bassez T, Paris J, Omilli F, Dorel C, Osborne HB: Posttranscriptional regulation of ornithine decarboxylase in Xenopus laevis oocytes. Development 110: 955–962 (1990).

    Google Scholar 

  5. Berger S, Bell E, Mullet JE: Two methyl jasmonateinsensitivbe mutants show altered expression of AtVsp in response to methyl jasmonate and wounding. Plant Physiol 111: 525–531 (1996).

    Google Scholar 

  6. Boutry M, Chua N-H: A nuclear gene encoding the beta subunit of the mitochondrial ATP synthase in Nicotiana plumbaginifolia. EMBO J 4: 2159–2165 (1985).

    Google Scholar 

  7. Chen CT, Kao CH: Osmotic stress and water stress have opposite effects on putrescine and proline production in excised rice leaves. Plant Growth Regul 13: 197–202 (1993).

    Google Scholar 

  8. Creelman RA, Tierney ML, Mullet JE: Jasmonic acid/methyl jasmonate accumulatein wounded soybean hypocotyls and modulate wound gene expression. Proc Natl Acad Sci USA 89: 4938–4941 (1992).

    Google Scholar 

  9. Doares SH, Syrovets T, Weiler EW, Ryan CA: Oligogalacturonides and chitosanactivate Plant defensive genes through the octadecanoid pathway. Proc Natl Acad Sci USA 92: 4095–4098 (1995).

    Google Scholar 

  10. Espartero J, P intor-Toro JA, Pardo JM: Differential accumulation of S-adenosylmethionine synthetase transcripts in response to salt stress. Plant Mol Biol 25: 217–227 (1994).

    Google Scholar 

  11. Evans PT, Malmberg RL: Do polyamines have roles in Plant development? Annu Rev Plant Physiol Plant Mol Biol 40: 235–269 (1989).

    Google Scholar 

  12. Feys BJF, Benedetti CE, Penfold CN, Turner JG: Arabidopsis mutants selected forresistance to the phytotoxin coronatine are male sterile, insensitive to methyljasmonate, and resistant to a bacterial pathogen. Plant Cell 6: 751–759 (1994).

    Google Scholar 

  13. Flores HE, Galston AW: Analysis of polyamines in higher Plants by highperformance liquid chromatography. Plant Physiol 69: 701–706 (1982).

    Google Scholar 

  14. Flores HE, Galston AW: Polyamines and Plant stress: activation of putrescinebiosynthesis by osmotic shock. Science 217: 1259–1261 (1982).

    Google Scholar 

  15. Fonzi WA, Sypherd PS: The gene and the primary structure of ornithinedecarboxylase from Saccharomyces cerevisiae. J Biol Chem 262: 10127–10133 (1987).

    Google Scholar 

  16. Galston AW: Polyamines and Plant response to stress. In: Bachrach U, Heimer YM (eds) The Physiology of Polyamines, vol 2, pp. 99–106. CRC Press, Boca Raton, FL (1989).

    Google Scholar 

  17. Gomez-Gomez L, Carrasco P: Hormonal regulation of Sadenosylmethionine synthase transcripts in pea ovaries. Plant Mol Biol 30: 821–832 (1996).

    Google Scholar 

  18. Gundlach H, Muller MJ, Kutchan TM, Zenk MH: Jasmonic acid is a signal transducer in elicitor-induced Plant cell cultures. Proc Natl Acad Sci USA 89: 2389–2393 (1992).

    Google Scholar 

  19. Hayashi S, Murakami Y, Matsufuji S: Ornithine decarboxylase antizyme: a novel type of regulatory protein. Trends Biochem Sci 21: 27–30 (1996).

    Google Scholar 

  20. Heby O, Persson L: Molecular genetics of polyamine synthesis in eukaryotic cells. Trends Biochem Sci 15: 153–158 (1990).

    Google Scholar 

  21. Hibi N, Higashiguchi S, Hashimoto T, Yamada Y: Gene expression in tobacco low-nicotine mutants. Plant Cell 6: 723–735 (1994).

    Google Scholar 

  22. Hughes KT, Dessen A, Gray JP, Grubmeyer C: The Salmonella typhimuriumnadC gene: sequence determination by use of Mud-P22 and purification of quinolinate phosphoribosyltransferase. J Bact 175: 479–486 (1993).

    Google Scholar 

  23. Ikeda T, Matsuomoto T, Noguchi M: Effects of nutritional factors on the formation of ubiquinone by tobacco Plant cells in suspension culture. Agric Biol Chem 40: 1765–1770 (1976).

    Google Scholar 

  24. Imanishi S, Hashizume K, Kojima H, Ichihara A, Nakamura K: An mRNA oftobacco cell that is rapidly inducible by methyl jasmonate in the presence of cycloheximide codes for a putative glycosyltransferase. Plant Cell Physiol 39: 202–211 (1998).

    Google Scholar 

  25. Ishikawa A, Yoshihara T, Nakamura K: Jasmonate-inducible expression of a potato cathepsin D inhibitor-GUS gene fusion in tobacco cells. Plant Mol Biol 26: 403–414 (1994).

    Google Scholar 

  26. Kashiwagi K, Yamaguchi Y, Sakai Y, Kobayashi H, Igarashi K: Identification of the polyamine-induced protein as a periplasmic oligopeptide binding protein. J Biol Chem 265: 8387–8391 (1990).

    Google Scholar 

  27. Kawalleck P, Plesch g, Hahlbrock K, Somssich IE: Induction by fungal elicitor of S-adenosyl-L-methionine synthetase and S-adenosyl-L-homocysteine hydrolase mRNAs in cultured cells and leaves of Petroselinum crispum. Proc Natl Acad SciUSA 89: 4713–4717 (1992).

    Google Scholar 

  28. Kim SR, Kim Y, An G: Identification of methyl jasmonate and salicylic acid response elements from the nopaline synthase (nos) promoter. Plant Physiol 103: 97–103 (1993).

    Google Scholar 

  29. Kumar A, Altabella T, Taylor MA, Tiburcio AF: Recent advances in polyamine research. Trends Plant Sci 2: 124–130 (1997).

    Google Scholar 

  30. Kutchan TM: Alkaloid biosynthesis: the basis for metabolic engineering of medicinal Plants. Plant Cell 7: 1059–1070 (1995).

    Google Scholar 

  31. Lorberth R, Dammann C, Ebneth M, Amati S, Sanchez-Serrano JJ: Promoter elements involved in environmental and developmental control of potato proteinase inhibitor II expression. Plant J 2: 477–486 (1992).

    Google Scholar 

  32. Mad Arif SA, Taylor MA, George LA, Butler AR, Burch LR, Davies HV, Stark MJ, Kumar A: Characterization of the Sadenosylmethionine decarboxylase (SAMDC) gene of potato. Plant Mol Biol 26: 327–338 (1994).

    Google Scholar 

  33. Mason HS, DeWald DB, Mullet JE: Identification of a methyl jasmonate-responsive domain in the soybean vspB promoter. Plant Cell 5: 241–251 (1993).

    Google Scholar 

  34. Matsuoka K, Nakamura K: Propeptide of a precursor to a Plant vacuolar proteinrequired for vacuolar targeting. Proc Natl Acad Sci USA 88: 834–838 (1991).

    Google Scholar 

  35. Michael AJ, Furze JM, Rhodes MJC, Burtin D: Molecular cloning and functionalidentification of a Plant ornithine decarboxylase cDNA. Biochem J 314: 241–248 (1996).

    Google Scholar 

  36. Mizukami H, Tabira Y, Ellis EE: Methyl jasmonate-induced rosemarinic acid biosynthesis in Lithospermum erythrorhizon cell suspension cultures. Plant Cell Rep 12: 706–709 (1993).

    Google Scholar 

  37. Mizusaki S, Tanabe Y, Noguchi M, Tamaki E: Changes in the activities of ornithine decarboxylase, putrescine N1111 methyltransferase and N-methylputrescine oxidase in tobacco roots in relation to nicotine biosynthesis. Plant Cell Physiol 14: 103–110 (1973).

    Google Scholar 

  38. Mueller MJ, Brodschelm W, Spannagl E, Zenk MH: Signaling in the elicitoation process is mediated through the octadecanoid pathway leading to jasmonic acid. Proc Natl Acad Sci USA 90: 7490–7494 (1993).

    Google Scholar 

  39. Peña-Cortés H, Fisahn J, Willmitzer L: Signals invovled in wound-induced proteinase inhibitor II gene expression in tomato and potato Plants. Proc Natl AcadSci USA 92: 4106–4113 (1995).

    Google Scholar 

  40. Perez-Amador MA, Carbonell J, Granell A: Expression of arginine decarboxylase is induced during early fruit development and in young tissues of Pisum sativum (L.). Plant Mol Biol 28: 997–1009 (1995).

    Google Scholar 

  41. Rastogi R, Dulson J, Rothstein SJ: Cloning of tomato (Lycopersicon esculentum Mill.) arginine decarboxylase gene and its expression during fruit ripening. Plant Physiol 193: 829–834 (1993).

    Google Scholar 

  42. Saunders JA, Blume DE: Quantitation of major tobacco alkaloids by high-performance liquid chromatography. J Chramatography 205: 147–154 (1981).

    Google Scholar 

  43. Schröder G, Eichel J, Breinig S, Schröder J: Three differentially expressed S-adenosylmethionine synthetases from Catharanthus roseus: molecular and functional characterization. Plant Mol Biol 33: 211–222 (1997).

    Google Scholar 

  44. Sembdner G, Parthier B: The biochemistry and the physiological and molecularactions of jasmonates. Annu Rev Plant Physiol Plant Mol Biol 44: 569–589 (1993).

    Google Scholar 

  45. Slocum RD, Galston AW: Inhibition of polyamine biosynthesis in Plants and Plant pathogenic fungi. In: McCann PP, Peggy AE, Sjoerdsma A (eds), Inhibition of Polyamine Metabolism, pp. 305–316. Academic Press, San Diego (1987).

    Google Scholar 

  46. Suzuki G, Ohta H, Kato T, Igarashi T, Sakai F, Shibata D, Takano T, Shioi Y, Takamiya K-I: Induction of a novel cytochrome P450 (CYP93 family) by methyl jasmonate in soybean suspension-cultured cells. FEBS Lett 383: 83–86 (1996).

    Google Scholar 

  47. Tiburico AF, Galston AW: Arginine decarboxylase as the source of putrescine for tobacco alkaloid. Phytochemistry 25: 107–110 (1986).

    Google Scholar 

  48. Walden R, Cordeiro A, Tiburcio AF: Polyamines: small molecules triggering pathways in Plant growth and development. Plant Physiol 113: 1009–1013 (1997).

    Google Scholar 

  49. Waller GR, Dermer OC: Enzymology of alkaloid metabolism in Plants and microorganisms. In: Conn EE (eds) The Biochemistry of Plants, vol 7, pp. 317–395. Academic Press, San Diego (1981).

    Google Scholar 

  50. Watson MB, Malmberg RL: Regulation of Arabidopsis thaliana (L.) Heynh arginine decarboxylase by potassium deficiency stress. Plant Physiol 111: 1077–1083 (1996).

    Google Scholar 

  51. Weiler EW, Kutchan TM, Gorba T, Brodschelm W, Niesel U, Bublitz F: The Pseudomonas phytotoxin coronatine mimics octadecanoid signalling molecules of higher Plants. FEBS Lett 345: 9–13 (1994).

    Google Scholar 

  52. Yao J, Zadworny D, Kuhnlein U, Hayes JF: Molecular cloning of a bovine ornithine decarboxylase cDNA and its use in the detection of restriction fragment length polymorphisms in Holsteins. Genome 38: 325–331 (1995).

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Laboratory of Biochemistry, Gaduate School of Bioagricultural Sciences Nagoya University, Chikusa, Nagoya, 464-01, Japan

    Shunsuke Imanishi, Katsuhito Hashizume, Makiko Nakakita, Hisae Kojima & Kenzo Nakamura

  2. Department of Applied Biological Sciences, School of Agricultural Sciences, Nagoya University, Chikusa, Nagoya, 464-01, Japan

    Yoshikatsu Matsubayashi & Youji Sakagami

  3. Nara Institute of Science and Technology, 8916-5 Takayama, Ikoma, 630-01, Japan

    Takashi Hashimoto & Yasuyuki Yamada

Authors
  1. Shunsuke Imanishi
    View author publications

    You can also search for this author inPubMed Google Scholar

  2. Katsuhito Hashizume
    View author publications

    You can also search for this author inPubMed Google Scholar

  3. Makiko Nakakita
    View author publications

    You can also search for this author inPubMed Google Scholar

  4. Hisae Kojima
    View author publications

    You can also search for this author inPubMed Google Scholar

  5. Yoshikatsu Matsubayashi
    View author publications

    You can also search for this author inPubMed Google Scholar

  6. Takashi Hashimoto
    View author publications

    You can also search for this author inPubMed Google Scholar

  7. Youji Sakagami
    View author publications

    You can also search for this author inPubMed Google Scholar

  8. Yasuyuki Yamada
    View author publications

    You can also search for this author inPubMed Google Scholar

  9. Kenzo Nakamura
    View author publications

    You can also search for this author inPubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Imanishi, S., Hashizume, K., Nakakita, M. et al. Differential induction by methyl jasmonate of genes encoding ornithine decarboxylase and other enzymes involved in nicotine biosynthesis in tobacco cell cultures. Plant Mol Biol 38, 1101–1111 (1998). https://doi.org/10.1023/A:1006058700949

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/A:1006058700949