Skip to main content
SpringerLink
Log in

Analysis of celery (Apium graveolens) mannitol dehydrogenase (Mtd) promoter regulation in Arabidopsis suggests roles for MTD in key environmental and metabolic responses

  • Published:
Plant Molecular Biology Aims and scope Submit manuscript

Abstract

Of the growing list of promising genes for plant improvement, some of the most versatile appear to be those involved in sugar alcohol metabolism. Mannitol, one of the best characterized sugar alcohols, is a significant photosynthetic product in many higher plants. The roles of mannitol as both a metabolite and an osmoprotectant in celery (Apium graveolens) are well documented. However, there is growing evidence that `metabolites' can also have key roles in other environmental and developmental responses in plants. For instance, in addition to its other properties, mannitol is an antioxidant and may have significant roles in plant-pathogen interactions. The mannitol catabolic enzyme mannitol dehydrogenase (MTD) is a prime modulator of mannitol accumulation in plants. Because the complex regulation of MTD is central to the balanced integration of mannitol metabolism in celery, its study is crucial in clarifying the physiological role(s) of mannitol metabolism in environmental and metabolic responses. In this study we used transformed Arabidopsis to analyze the multiple environmental and metabolic responses of the Mtd promoter. Our data show that all previously described changes in Mtd RNA accumulation in celery cells mirrored changes in Mtd transcription in Arabidopsis. These include up-regulation by salicylic acid, hexokinase-mediated sugar down-regulation, and down-regulation by salt, osmotic stress and ABA. In contrast, the massive up-regulation of Mtd expression in the vascular tissues of salt-stressed Arabidopsis roots suggests a possible role for MTD in mannitol translocation and unloading and its interrelation with sugar metabolism.

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

Access this article

Log in via an institution

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

  • An, G., Ebert, P.R., Mitra, A. and Ha, S.B. 1988. Binary vectors, In: S. Gelvin and R. Schilperoort (Eds.) Plant Molecular Biology Manual (Supplement 4, 1992), Kluwer Academic Publishers, Dordrecht, Netherlands, pp. A3: 1–19.

    Google Scholar 

  • Chiu, W.-L., Niwa, Y., Zeng, W., Hirano, T., Kobayashi, H. and Sheen, J. 1996. Engineered GFP as a vital reporter in plants. Curr. Biol. 63: 325–330.

    Google Scholar 

  • Clough, S.J. and Bent, A.F. 1998. Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 16: 735–743.

    Google Scholar 

  • Creelman, R.A. and Mullet, J.E. 1997. Biosynthesis and action of jasmonates in plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 48: 355–381.

    Google Scholar 

  • Doares, S.H., Narvaez-Vasquez, J., Conconi, A. and Ryan, C.A. 1995. Salicylic acid inhibits synthesis of proteinase inhibitors in tomato leaves induced by systemin and jasmonic acid. Plant Physiol. 108: 1741–1746.

    Google Scholar 

  • Durner, J. and Klessig, D.F. 1996. Salicylic acid is a modulator of tobacco and mammalian catalases. J. Biol. Chem. 271: 28492–28501.

    Google Scholar 

  • Everard, J.D., Gucci, R., Kann, S.C., Flore, J.A. and Loescher, W.H. 1994. Gas exchange and carbon partitioning in the leaves of celery (Apium graveolens L.) at various levels of root zone salinity. Plant Physiol. 106: 281–292.

    Google Scholar 

  • Fellman, J.K. and Loescher, W.H. 1987. Comparative studies on sucrose and mannitol utilization in celery (Apium graveolens L.). Physiol. Plant. 69: 337–341.

    Google Scholar 

  • Geigenberger, P., Langenberger, S., Wilke, I., Heineke, D., Heldt, H.W. and Stitt, M. 1993. Sucrose is metabolized by sucrose synthase and glycolysis within the phloem complex of Ricinis communis L. seedlings. Planta 190: 446–453.

    Google Scholar 

  • Hause, B., Demus, U., Teichmann, C., Parthier B. and Wasternack C. 1996. Developmental and tissue-specific expression of JIP-23, a jasmonate-inducible protein of barley. Plant Cell Physiol. 37: 641–649.

    Google Scholar 

  • Hood, E.E., Gelvin, S.B., Melchers, L.S. and Hoekema, A. 1993. New Agrobacterium helper plasmids for gene transfer to plants. Transgenic Res. 2: 208–218.

    Google Scholar 

  • Huijser, C., Kortstee, A., Pego, J.V., Wisman, E., Weisbeek, P. and Smeekens, S.C.M. 2000. The Arabidopsis SUN6 gene is identical to ABI4. Plant J. 23: 577–585.

    Google Scholar 

  • Iwasaki, T., Yamaguchi-Shinozaki, K. and Shinozaki, K. 1995. Identification of a cis-regulatory region of a gene in Arabidopsis thaliana whose induction by dehydration is mediated by abscisic acid and requires protein synthesis. Mol. Gen. Genet. 247: 391–398.

    Google Scholar 

  • Jennings, D.B., Eherenshaft, M., Pharr, D.M. and Williamson, J.D. 1998. Roles for mannitol and mannitol dehydrogenase in active-oxygen-mediated plant defense. Proc. Natl. Acad. Sci. USA 95: 15129–15133.

    Google Scholar 

  • Koch, K.E. 1996. Carbohydrate-modulated gene expression in plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 47: 509–540.

    Google Scholar 

  • Korfhage, U., Trezzini, G.F., Meier, I., Hahlbrock, K. and Somssich, I.E. 1994. Plant homeodomain protein involved in transcriptional regulation of a pathogen defense-related gene. Plant Cell 6: 695–708.

    Google Scholar 

  • Korsmeyer, S.J. 1995. Regulators of cell death. Trends Genet. 11: 101–105.

    Google Scholar 

  • Leung, J. and Giraudat, J. 1998. Abscisic acid signal transduction. Annu. Rev. Plant Physiol. Plant Mol. Biol. 49: 199–222.

    Google Scholar 

  • Lew, R.R. 1996. Pressure regulation of the electrical properties of growing Arabidopsis thaliana L. root hairs. Plant Physiol. 112: 1089–1100.

    Google Scholar 

  • Lu, C.A., Lim, E.K. and Yu, S.M. 1998. Sugar response sequence in the promoter of a rice α-amylase gene serves as a transcriptional enhancer. J. Biol. Chem. 273: 10120–10131.

    Google Scholar 

  • Mathur, J. and Koncz, C. 1998. Establishment and maintenance of cell suspension cultures. In: J. Martinez and J. Salinas (Eds.) Methods in Molecular Biology, Vol. 82: Arabidopsis Protocols, Humana Press, Totowa, NJ, pp. 27–30.

    Google Scholar 

  • Murashige, T. and Skoog, F. 1962. A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiol. Plant. 15: 473–497.

    Google Scholar 

  • Noiraud, N., Delrot, S. and Lemoine, R. 2000. The sucrose transporter of celery. Identification and expression during salt stress. Plant Physiol. 122: 1447–1456.

    Google Scholar 

  • Nolte, K.D. and Koch, K.E. 1993. Companion-cell-specific localization of sucrose synthase in zones of phloem loading and unloading. Plant Physiol. 101: 899–905.

    Google Scholar 

  • Obaton, M.F. 1929. Evolution de la mannite chez les végétaux. Rev. Gén. Bot. 41: 622–633.

    Google Scholar 

  • PeÑa-Cortés, H., Albrecht, T., Prat, S., Weiler, E.W. and Willmitzer, L. 1993. Aspirin prevents wound-induced gene expression in. tomato leaves by blocking jasmonic acid biosynthesis. Planta 191: 123–128.

    Google Scholar 

  • Prata, R.T.N., Williamson, J.D., Conkling, M.A. and Pharr, D.M. 1997. Sugar repression of mannitol dehydrogenase activity in celery cells. Plant Physiol. 114: 307–314.

    Google Scholar 

  • Riesmeier, J.W., Hirner, B. and Frommer, W.B. 1993. Potato sucrose transporter expression in minor veins indicate a role in phloem loading. Plant Cell 5: 1591–1598.

    Google Scholar 

  • Salmon, S., Lemoine, R., Jamai, A., Bouché-Pillon, S. and Fromont, J.C. 1995. Study of sucrose and mannitol transport in plasma-membrane vesicles from phloem and non-phloem tissues of celery (Apium graveolens L.) petioles. Planta 197: 76–83.

    Google Scholar 

  • Schindler, U., Terzaghi, W., Beckmann, H., Kadesch, T. and Cashmore, A.R. 1992. DNA binding site preferences and transcriptional activation properties of the Arabidopsis transcription factor GBF1. EMBO J. 11: 1275–1289.

    Google Scholar 

  • Shah, J. and Klessig, D.F. 1996. Identification of a salicylic acid-responsive element in the promoter of the tobacco pathogenesis-related β-1,3-glucanase gene, PR-2d. Plant J. 10: 1089–1101.

    Google Scholar 

  • Sheen, J., Hwang, S., Niwa, Y., Kobayashi, H. and Galbraith, D.W. 1995. Green-fluorescent protein as a new vital marker in plant cells. Plant J. 8: 777–784.

    Google Scholar 

  • Shen, B., Jensen, R. and Bohnert, H.J. 1997. Increased resistance to oxidative stress in transgenic plants by targeting mannitol biosynthesis to chloroplasts. Plant Physiol. 113: 1177–1183.

    Google Scholar 

  • Smeekens, S. 2000. Sugar-induced signal transduction in plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 51: 49–81.

    Google Scholar 

  • Smirnoff, N. and Cumbes, Q.J. 1989. Hydroxyl radical scavenging activity of compatible solutes. Phytochemistry 28: 1057–1060.

    Google Scholar 

  • Stoop, J.M.H. and Pharr, D.M. 1992. Partial purification and characterization of mannitol:mannose 1-oxidoreductase from celeriac (Apium graveolens var. rapaceum) roots. Arch. Biochem. Biophys. 298: 612–619.

    Google Scholar 

  • Stoop, J.M.H. and Pharr, D.M. 1994. Mannitol metabolism in celery stressed by excess macronutrients. Plant Physiol. 106: 503–511.

    Google Scholar 

  • Stoop, J.M.H., Williamson, J.D., Conkling, M.A. and Pharr, D.M. 1995. Purification of NAD-dependent mannitol dehydrogenase from celery suspension cultures. Plant Physiol. 108: 1219–1225.

    Google Scholar 

  • Stoop, J.M.H., Williamson, J.D. and Pharr, D.M. 1996. Mannitol metabolism in plants: a method for coping with stress. Trends Plant Sci. 1: 139–144.

    Google Scholar 

  • Sutherland, M.W. 1991. The generation of oxygen radicals during host plant responses to infection. Physiol. Mol. Plant Path. 39: 79–93.

    Google Scholar 

  • Truernit, E. and Sauer, N. 1995. The promoter of the Arabidopsis thaliana SUC2 sucrose-H+symporter gene directs expression of β-glucuronidase to the phloem: evidence for phloem loading and unloading by SUC2. Planta 196: 564–570.

    Google Scholar 

  • Urwin, N.A. and Jenkins, G.I. 1997. A sucrose repression element in the Phaseolus vulgaris rbcS2 gene promoter resembles elements responsible for sugar stimulation of plant and mammalian genes. Plant Mol. Biol. 35: 929–942.

    Google Scholar 

  • Vreugdenhil, D. 1983. Abscisic acid inhibits phloem loading of sucrose. Physiol. Plant. 57: 463–467.

    Google Scholar 

  • Williamson, J.D. and Scandalios J.G. 1992. Differential response of maize catalases to abscisic acid: Vp1 transcriptional activator is not required for ABA-regulated Cat1 expression. Proc. Natl. Acad. Sci. USA 89: 8842–8846.

    Google Scholar 

  • Williamson, J.D. and Scandalios, J.G. 1994. The maize (Zea mays L.) Cat1 catalase promoter displays differential binding of nuclear proteins isolated from germinated and developing embryos and from embryos grown in the presence and absence of abscisic acid. Plant Physiol. 106: 1373–1380.

    Google Scholar 

  • Williamson, J.D., Stoop, J.M.H., Massel, M.O., Conkling, M.A. and Pharr, D.M. 1995. Sequence analysis of a mannitol dehydrogenase cDNA from plants reveals a function for the PR protein ELI3. Proc. Natl. Acad. Sci. USA 92: 7148–7152.

    Google Scholar 

  • Williamson, J.D., Guo, W-W. and Pharr, D. M. 1998. Cloning and characterization of a genomic clone (Accession No. AF067082) encoding mannitol dehydrogenase from celery (Apium grave-olens) (PGR98-137). Plant Physiol. 118: 329.

    Google Scholar 

  • Yamamoto, Y.T., Zamski, E., Williamson, J.D., Conkling, M.A. and Pharr, D.M. 1997. Subcellular localization of celery mannitol dehydrogenase: a cytoplasmic metabolic enzyme in nuclei. Plant Physiol. 115: 1397–1403.

    Google Scholar 

  • Zamski, E., Yamamoto, Y.T., Williamson, J.D., Conkling, M.A. and Pharr, D.M. 1996. Immunolocalization of mannitol dehydrogenase in celery plants and cells. Plant Physiol. 112: 931–938.

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Departments of Horticultural Science, USA

    Eli Zamski, Wei-Wen Guo, D. Mason Pharr & John D. Williamson

  2. Forestry, North Carolina State University, Raleigh, NC, 27695-7609, USA

    Yuri T. Yamamoto

Authors
  1. Eli Zamski
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Wei-Wen Guo
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Yuri T. Yamamoto
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. D. Mason Pharr
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. John D. Williamson
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Zamski, E., Guo, WW., Yamamoto, Y.T. et al. Analysis of celery (Apium graveolens) mannitol dehydrogenase (Mtd) promoter regulation in Arabidopsis suggests roles for MTD in key environmental and metabolic responses. Plant Mol Biol 47, 621–631 (2001). https://doi.org/10.1023/A:1012395121920

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/A:1012395121920

Search

Navigation