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Uptake of Malate and Citrate into Plant Vacuoles

  • E. Martinoia
  • D. Rentsch

Abstract

Of the different organic anions which are often present a high concentrations in plants, malate plays a central role. Plants exhibiting crassulacean acid metabolism (CAM) fix CO2 with the enzyme phosphoenolpyruvate carboxylase during the night and accumulate large amounts of malic acid. During the light period, malic acid is decarboxylated and the released CO2 is fixed in the Calvin cycle. C4 plants fix CO2 in the mesophyll in a similar reaction during the day, as CAM in the dark. In these plants, malate is transferred to the bundle sheaths, decarboxylated and the CO2 fixed in the photosynthetic reaction. This reaction enables the plant to fix CO2 more efficiently, since the affinity of phosphoenolpyruvate carboxylase to HCO3 - is much higher than that of ribulose-1,5- diphosphate carboxylase to CO2. Diurnal fluctuations of malate can also be observed in C3 plants. However, in these plants malate is accumulated during the day and used as an energy source for respiration in the dark (Winter, Usuda, Tsuzuki, Schmitt, Edwards, Thomas, and Evert, 1982; Gerhardt, Stitt, and Heldt, 1987). Malate metabolism and accumulation also play an important role during the opening of stomata since, in most plants, malate is used for balancing K+ (Schnabl and Kottmeier, 1984). Other prominent organic acids often accumulated at high concentrations in plants include shikimic acid, which is present mainly in gymnosperms and some woody angiosperms, as well as gallic, oxalic and citric acid.

Keywords

Malic Acid Crassulacean Acid Metabolism Shikimic Acid Pyridoxal Phosphate FEBS Letter 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

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References

  1. Amrhein, N., Schneebeck, D., Skorupka, H., Tophof, S., and Stöckigt, J., 1981. Identification of a major metabolite of the ethylene precursor 1-aminocyclopropane-1-carboxylic acid in higher plants. Naturwissenschaften, 68, 619–620.CrossRefGoogle Scholar
  2. Blom-Zandstra, M., Koot, H.T.M., Hattum, J., and Borstlap, A.C., 1990. Interactions of uptake of malate and nitrate into isolated vacuoles from lettuce leaves. Planta, 183, 10–16.Google Scholar
  3. Bouyssou, H., Canut, H., and Marigo, G., 1990. A reversible carrier mediates the transport of malate at the tonoplast of Catharanthus roseus ells. FEBS Letters, 275, 73–76.PubMedCrossRefGoogle Scholar
  4. Bouzayen, M., Latche, A., Alibert, G., and Pech, J.C., 1989. Carrier mediated uptake of 1(malonylamino)cyclopropane-l-carboxylic acid in vacuoles isolated from Catharanthus roseus cells. Plant Physiology, 91, 1317–1322.PubMedCrossRefGoogle Scholar
  5. Buser, C., and Matile, P., 1977. Malic acid in vacuoles isolated from Bryophyllum leaf cells. Zeitschrifl fiir Pflanzenphysiologie, 82, 462–466.Google Scholar
  6. Buser-Sutter, C., Wiemken, A., and Matile, P., 1981. A malic acid permease in isolated vacuoles of a crassulacean acid metabolism plant. Plant Physiology, 69, 456–459.CrossRefGoogle Scholar
  7. Coyaud, L., Kurkdjian, A., Kado, R., and Hedrich, R., 1987. Ion channels and ATP-driven pumps involved in ion transport across the tonoplast of sugar beet vacuoles. Biochimica et Biophysica Acta, 902, 263–268.CrossRefGoogle Scholar
  8. Flügge, U.I., and Heldt, H.W., 1977. Specific labelling of a protein involved in phosphate transport of chloroplasts by pyridoxal-5-phosphate. FEBS Letters, 82, 29–33.PubMedCrossRefGoogle Scholar
  9. Gerhardt, R., Sti1t, M., and Heldt, H.W., 1987. Subcellular metabolite levels in spinach leaves. Plant Physiology, 83, 399–407.PubMedCrossRefGoogle Scholar
  10. Grob, K., and Matile, P., 1980. Compartmentation of ascorbic acid in vacuoles of horseradish root cells. Note on vacuolar peroxidase. Zeitschrii flir Pflanzenphysiologie, 98, 235–243.Google Scholar
  11. Hedrich, R., Flügge, U.I., and Fernandez, J.M., 1986. Patch-clamp studies of ion transport in isolated plant vacuoles. FEBS Letters, 204, 228–232.CrossRefGoogle Scholar
  12. Holländer-Czytko, H., and Amrhein, N., 1983. Subcellular compartmentation of shikimic acid and phenylalanine in buckwheat cell suspension cultures grown in the presence of shikimate pathway inhibitors. Plant Science Letters, 29, 89–96.CrossRefGoogle Scholar
  13. Kaiser, G., Martinoia, E., and Wiemken, A., 1982. Rapid appearance of photosynthetic products in the vacuoles isolated from barley mesophyll protoplasts by a new fast method. Zeitschrh far Pflanzenphysiologie, 107, 103–113.Google Scholar
  14. Kaiser, G., Martinoia, E., Schröppel-Meier, G., and Heber, U., 1989. Active transport of sulfate into the vacuole of plant cells provides halotolerance and can detoxify SO2. Journal of Plant Physiology, 133, 756–763.CrossRefGoogle Scholar
  15. Kaiser, W., and Förster, J., 1989. Low CO, prevents nitrate reduction in leaves. Plant Physiology, 91, 970–974.PubMedCrossRefGoogle Scholar
  16. Kästner, K.H., and Sze, H., 1987. Potential-dependent anion transport in tonoplast vesicles from oat roots. Plant Physiology, 83, 483–489.CrossRefGoogle Scholar
  17. Lüttge, U., Smith, J.A.C., Marigo, G., and Osmond, C.B., 1981. Energetics of malate accumulation in the vacuoles of Kalanchoe tubiflora cells. FEBS Letters, 126, 81–84.CrossRefGoogle Scholar
  18. Lüttge, U., and Smith, J.A.C., 1984. Mechanism of passive malic-acid efflux from vacuoles of the CAM plant Kalanchoe daigremontiana. Journal of Membrane Biology, 81, 149–158.CrossRefGoogle Scholar
  19. Lüttge, U., 1988. Day-night changes of citric-acid levels in crassulacean acid metabolism: phenomenon and ecophysiological significant. Plant Cell and Environment, 11, 445–451.CrossRefGoogle Scholar
  20. Marigo, C., Couyssou, H., and Belkoura, M. 1985. Vacuolar efflux of malate and its influence on nitrate accumulation in Catharanthus roseus cells. Plant Science, 39, 97–103.CrossRefGoogle Scholar
  21. Marigo, G., Bouyssou, H., and Laborie, D., 1988. Evidence for malate transport into vacuoles isolated from Catharanthus roseus cells. Botanica Acta, 101, 187–191.Google Scholar
  22. Marin, B., Cretin, H., and D’auzac, J., 1982. Energisation of solute transport and accumulation at the tonoplast in Hevea latex. Physiologie Vegetate, 20, 333–346.Google Scholar
  23. Marquardt-Jarczyk, G, and Luttge, U., 1990. Anion transport at the tonoplast of mesophyll cells of the CAM plant Kalanchoe daigremontiana. Journal of Plant Physiology, 136, 129–136.CrossRefGoogle Scholar
  24. Martinoia, E., Heck. U., and Wiemken, A., 1981. Vacuoles as storage compartments of nitrate in barley leaves. Nature, 289, 292–294.CrossRefGoogle Scholar
  25. Martinoia, E., Flügge, U.I., Kaiser, G., Heber, U., and Heldt, H.W., 1985. Energy-dependent uptake of malate into vacuoles isolated from barley mesophyll photoplasts. Biochimica et Biophysica Acta, 806, 311–319.CrossRefGoogle Scholar
  26. Martinoia, E., Vogt, E., and Amrhein, N., 1990. Transport of malate and chloride into barley mesophyll vacuoles. Different carriers are involved. FEBS Letters, 261, 109–111.CrossRefGoogle Scholar
  27. Martinoia, E., Vogt, E., Rentsch, D., and Amrhein, N., 1991. Functional reconstitution of the malate carrier of barley mesophyll vacuoles in liposomes. Biochimica et Biophysica Acta, 1062, 271–278.PubMedCrossRefGoogle Scholar
  28. Nishida, K., and Tominaga, P., 1987. Energy-dependent uptake of malate into vacuoles isolated from CAM plants Kalanchoe daigremontiana. Journal of Plant Physiology, 127, 385–393.CrossRefGoogle Scholar
  29. Oleski, N.M Mahdavi, P., and Bennett, A.B., 1987. Transport properties of the tomato fruit tonoplast. II. Citrate transport. Plant Physiology, 84, 997–1000.PubMedCrossRefGoogle Scholar
  30. Pope, A.J., and Leigh, R.A., 1987. Some characteristics of anion transport at the tonoplast of oat roots, determined from the effects of anions on pyrophosphate-dependent proton transport. Planta, 172, 91–100.CrossRefGoogle Scholar
  31. Rea, P.A., and Sanders, E., 1987. Tonoplast energisation: two H+ pumps, one membrane. Physiologia Plantarum, 71, 131–141.CrossRefGoogle Scholar
  32. Rentsch, D., and Martinoia, E., 1991. Citrate transport into barley mesophyll vacuoles - comparison with malate uptake activity. Planta, 184, 532–537.CrossRefGoogle Scholar
  33. Schnabl, H., and Kottmeier, C., 1984. Determination of malate levels during the swelling of vacuoles isolated from guard-cell protoplasts. Planta, 161, 27–31.CrossRefGoogle Scholar
  34. Sze, H., 1985. H+-translocating ATPases: advances using membrane vesicles. Annual Review of Plant Physiology, 36, 175–208.CrossRefGoogle Scholar
  35. Tophof, S., Martinoia, E., Kaiser, G., Hartung, W., and Amrhein, N., 1989. Compartmentation and transport of 1-aminocyclopropane-1-carboxylic acid and N-malonyl-1aminocyclopropane-1-carboxylic acid in barley and wheat mesophyll cells and protoplasts. Plant Physiology, 75, 333–339.CrossRefGoogle Scholar
  36. White, P.J., and Smith, J.A.C., 1989. Proton and anion transport at the tonoplast in crassulacean-acidmetabolism plants: specificity of the malate-influx system in Kalanchoe daigremontiana. Planta, 179, 265–274.CrossRefGoogle Scholar
  37. Winter, K., Usuda, H., Tsuzuki, M., Schmitt, M., Edwards, G.E., Thomas, R.J., and Evert, R.F., 1982. Influence of nitrate nand ammonia on photosynthetic characteristics and leaf anatomy of Moricandia arvensis. Plant Physiology, 70, 615–625.Google Scholar

Copyright information

© Springer Science+Business Media New York 1992

Authors and Affiliations

  • E. Martinoia
    • 1
  • D. Rentsch
    • 1
  1. 1.Institute of Plant SciencesSwiss Federal Institute of TechnologyZürichSwitzerland

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