Advertisement

Metabolomics

, Volume 9, Issue 3, pp 590–598 | Cite as

An antagonist treatment in combination with tracer experiments revealed isocitrate pathway dominant to oxalate biosynthesis in Rumex obtusifolius L.

  • Atsuko Miyagi
  • Minori Uchimiya
  • Maki Kawai-Yamada
  • Hirofumi UchimiyaEmail author
Original Article

Abstract

Oxalate accumulates in leaves of certain plants such as Rumex species (Polygonaceae). Oxalate plays important roles in defense to predator, detoxification of metallic ions, and in hydrogen peroxide formation upon wounding/senescence. However, biosynthetic pathways of soluble oxalate are largely unknown. In the present study we analysed Rumex obtusifolius L. treated with itaconate (an antagonist to isocitrate). Comprehensive metabolome analysis using capillary electrophoresis-mass spectrometry showed that oxalate content of “new leaves” was notably down-regulated by itaconate, as opposed to the accumulation of citrate. The 13CO2 feeding experiment revealed that oxalate accumulation in new leaves was affected by citrate translocation from stems. The results suggested that excess oxalate in new leaves of R. obtusifolius was synthesized primarily via the isocitrate pathway utilizing citrate delivered from stems.

Keywords

Rumex obtusifolius L. Capillary electrophoresis–mass spectrometry Oxalate Citrate Itaconate Isocitrate lyase 

Notes

Acknowledgments

This research was supported by a grant from the Program for Promotion of Basic and Applied Researches for Innovations in Bio-oriented Industry (BRAIN), Japan, and a grand from MEXT, Japan. We thank Dr. Ko Noguchi (The University of Tokyo), Dr. Masatoshi Yamaguchi (Saitama University) and Dr. Kentaro Takahara (The University of Tokyo) for helpful advice.

Supplementary material

11306_2012_486_MOESM1_ESM.docx (16 kb)
Supplementary material 1 (DOCX 15 kb)
11306_2012_486_MOESM2_ESM.ppt (7.9 mb)
Supplementary material 2 (PPT 8132 kb)

References

  1. Davoine, C., Le Deunff, E., Ledger, N., Avice, J. C., Billard, J. P., Dumas, B., et al. (2001). Specific and constitutive expression of oxalate oxidase during the ageing of leaf sheaths of ryegrass stubble. Plant, Cell and Environment, 24, 1033–1043.CrossRefGoogle Scholar
  2. Dickie, C. W., Hamann, M. H., Carroll, W. D., & Chow, F. (1978). Oxalate (Rumex venosus) poisoning in cattle. Journal of the American Veterinary Medical Association, 173, 73–74.PubMedGoogle Scholar
  3. Franceschi, V. R. (1989). Calcium oxalate formation is a rapid and reversible process in Lemna minor L. Protoplasma, 148, 130–137.CrossRefGoogle Scholar
  4. Franceschi, V. R., & Loewus, F. A. (1995). Oxalate biosynthesis and function in plants and fungi. In S. R. Khan (Ed.), Calcium oxalate in biological systems (pp. 113–130). Florida: CRC press.Google Scholar
  5. Franceschi, V. R., & Nakata, P. A. (2005). Calcium oxalate in plants: Formation and function. Annual Review of Plant Biology, 56, 41–71.PubMedCrossRefGoogle Scholar
  6. Giachetti, E., Pinzauti, G., Bonaccorsi, R., Vincenzini, M. T., & Vanni, P. (1987). Isocitrate lyase from higher plants. Phytochemistry, 26, 2439–2446.CrossRefGoogle Scholar
  7. Keates, S. A., Tarlyn, N., Loewus, F. A., & Franceschi, V. R. (2000). l-Ascorbic acid and l-galactose are sources of oxalic acid and calcium oxalate in Pistia stratiotes. Phytochemistry, 53, 433–440.PubMedCrossRefGoogle Scholar
  8. Khan, F. R., & Macfadden, B. A. (1979). Enzyme profiles in seedling development and the effect of itaconate, an isocitrate lyase-directed reagent. Plant Physiology, 64, 228–231.PubMedCrossRefGoogle Scholar
  9. Kostman, T. A., Tarlyn, N. M., Loewus, F. A., & Franceschi, V. R. (2001). Biosynthesis of l-ascorbic acid and conversion of carbons 1 and 2 of l-ascorbic acid to oxalic acid occurs within individual calcium oxalate crystal idioblasts. Plant Physiology, 125, 634–640.PubMedCrossRefGoogle Scholar
  10. Le Deunff, E., Davoine, C., Le Dantec, C., Billard, J. P., & Huault, C. (2004). Oxidative burst and expression of germin/oxo genes during wounding of ryegrass leaf blades: comparison with senescence of leaf sheaths. Plant Journal, 38, 421–431.PubMedCrossRefGoogle Scholar
  11. Ma, J. F., Ryan, P. R., & Delhaize, E. (2001). Aluminium tolerance in plants and the complexing role of organic acids. Trends in Plant Science, 6, 273–278.PubMedCrossRefGoogle Scholar
  12. Millerd, A., Morton, R. K., & Wells, J. R. K. (1963a). Oxalic acid synthesis in shoots of Oxalis pes-caprae (L.). Biochemical Journal, 86, 57–62.PubMedGoogle Scholar
  13. Millerd, A., Morton, R. K., & Wells, J. R. K. (1963b). Enzymatic synthesis of oxalic acid in Oxalis pes-caprae. Biochemical Journal, 88, 281–288.PubMedGoogle Scholar
  14. Miyagi, A., Takahara, K., Kasajima, K., Takahashi, H., Kawai-Yamada, M., & Uchimiya, H. (2011). Fate of 13C in metabolic pathways and effects of high CO2 on the alteration of metabolites in Rumex obtusifolius L. Metabolomics, 7, 524–535.CrossRefGoogle Scholar
  15. Miyagi, A., Takahara, K., Takahashi, H., Kawai-Yamada, M., & Uchimiya, H. (2010b). Targeted metabolomics in an intrusive weed, Rumex obtusifolius L., grown under different environmental conditions reveals alterations of organ related metabolite pathway. Metabolomics, 6, 497–510.CrossRefGoogle Scholar
  16. Miyagi, A., Takahashi, H., Takahara, K., Hirabayashi, T., Nishimura, Y., Tezuka, T., et al. (2010a). Principal component and hierarchical clustering analysis of metabolites in destructive weeds; polygonaceous plants. Metabolomics, 6, 146–155.CrossRefGoogle Scholar
  17. Miyagi, A., Uchimiya, M., Kawai-Yamada, M., & Uchimiya H. (2013). Impact of aluminum stress in oxalate and other metabolites in Rumex obtusifolius L. Weed Research, 53, 30–41.CrossRefGoogle Scholar
  18. Munir, E., Yoon, J.-J., Tokimatsu, T., Hattori, T., & Shimada, M. (2001). New role for glyoxylate cycle enzymes in wood-rotting basidiomycetes in relation to biosynthesis of oxalic acid. Journal of Wood Science, 47, 368–373.CrossRefGoogle Scholar
  19. Panciera, R. J., Martin, T., Burrows, G. E., Taylor, D. S., & Rice, L. E. (1990). Acute oxalate poisoning attributable to ingestion of curly dock (Rumex crispus) in sheep. Journal of the American Veterinary Medical Association, 196, 1981–1984.PubMedGoogle Scholar
  20. Rao, G. R., & McFadden, B. A. (1965). Isocitrate lyase from Pseudomonas indigofera. IV. Specificity and inhibition. Archives of Biochemistry and Biophysics, 112, 294–303.PubMedCrossRefGoogle Scholar
  21. Reig, R., Sanz, P., Blanche, C., Fontarnau, R., Dominguez, A., & Corbella, J. (1990). Fatal poisoning by Rumex crispus (curled dock): Pathological findings and application of scanning electron microscopy. Veterinary and Human Toxicology, 32, 468–470.PubMedGoogle Scholar
  22. Richardson, K. E., & Tolbert, N. E. (1961). Oxidation of glyoxylic acid to oxalic acid by glycolic acid oxidase. Journal of Biology and Chemistry, 236, 1280–1284.Google Scholar
  23. Runquist, M., & Kruger, N. (1999). Control of gluconeogenesis by isocitrate lyase in endosperm of germinating castor bean seedlings. The Plant Journal, 19, 423–431.PubMedCrossRefGoogle Scholar
  24. Schöttelndreier, M., Norddahl, M. M., Ström, L., & Falkengren-Grerup, U. (2001). Organic acid exudation by wild herbs in response to elevated Al concentrations. Annals of Botany, 87, 769–775.CrossRefGoogle Scholar
  25. Seal, S. N., & Sen, S. P. (1970). The photosynthetic production of oxalic acid in Oxalis corniculata. Plant and Cell Physiology, 11, 119–128.Google Scholar
  26. Spoerke, D. G., & Smolinske, S. C. (1990). Oxalates. In D. G. Spoerke & S. C. Smolinske (Eds.), Toxicity of Houseplants (pp. 29–32). Florida: CRC press.Google Scholar
  27. Tian, H., Jiang, L., Liu, E., Zhang, J., Liu, F., & Peng, X. (2008). Dependence of nitrate-induced oxalate accumulation on nitrate reduction in rice leaves. Physiologia Plantarum, 133, 180–189.PubMedCrossRefGoogle Scholar
  28. Zhang, Y., Lin, X., Zhang, Y., Zheng, S. J., & Du, S. (2005). Effects of nitrogen levels and nitrate/ammonium ratios on oxalate concentrations of different forms in edible parts of spinach. Journal of Plant Nutrition, 28, 211–2025.Google Scholar

Copyright information

© Springer Science+Business Media New York 2013

Authors and Affiliations

  • Atsuko Miyagi
    • 1
  • Minori Uchimiya
    • 2
  • Maki Kawai-Yamada
    • 1
    • 3
  • Hirofumi Uchimiya
    • 1
    Email author
  1. 1.Institute for Environmental Science and Technology, Saitama UniversitySaitamaJapan
  2. 2.USDA-ARS Southern Regional Research CenterNew OrleansUSA
  3. 3.Graduate School of Science and EngineeringSaitama UniversitySaitamaJapan

Personalised recommendations