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Modulation of the activity of phosphoenolypyruvate carboxylase during potassium-induced swelling of guard-cell protoplasts of Vicia faba L. after light and dark treatments

Abstract

Phosphoenolpyruvate carboxylase (PEPCase; EC 4.1.1.31) activity was found to be modulated by light and darkness when measured in the presence of K+, which had been added to induce swelling of guard-cell protoplasts (GCPs) from Vicia faba L., whereas no modulation was detected in the absence of K+ (PEPcase activity remained constant at 1.5±0.15 pmol PEP metabolized · GCP−1 ·h−1; subsequently, pmol GCP−1 ·h−1 will be used). The activity of PEPCase increased by 100% (from 1.5 to 3 pmol·protoplast−1·h−1) in darkness and by 200% (from 1.7 to 5 pmol·protoplast−1· h−1) in light and oscillations in activity of these magnitudes were repeated at intervals of 2 min (dark) and 2.5 min (light) for a period of 10 min during K+-induced increase in the volume of GCPs. The oscillations were reflected in changes in malate-pool sizes determined in plastids, mitochondria and the supernatant fraction (consisting of the cytosol and the vacuole). Malate probably functioned as a mitochondrial substrate, thus supplying ATP for K+ uptake and the swelling of the protoplasts. On the basis of the present paper and previous results (H. Schnabl and B. Michalke 1988, Life Sci. Adv. Plant Physiol. 7, 203–207) involving adenine nucleotidepool sizes in fractionated GCPs, a model is proposed to explain the cause-effect relationship between K+, PEPCase, the cytosolic and mitochondrial malate levels and ATP levels during the K+-induced increase of GCP volume.

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Abbreviations

GCP:

dtguard-cell protoplast

PEP:

phosphoenol-pyruvate

PEPCase:

PEP carboxylase

References

  1. Allaway, W.G. (1973) Accumulation of malate in guard cells of Vicia faba during stomatal opening. Planta 110, 63–70

  2. Assmann, S.M., Zeiger, E. (1987) Guard cell bioenergetics. In: Stomatal function, pp. 163–193, Zeiger, E., Farquhar, G.D., Cowen, J.R., eds. Stanford University Press, Stanford

  3. Briskin, D.P. (1986) Plasma membrane H+-transporting ATPase: role in potassium ion transport? Physiol. Plant. 68, 159–163

  4. Busacker, R.G., Saaty, T.L. (1968) Endliche Graphen und Netzwerke. Oldenbourg, München Wien

  5. Godehardt, E., Richter, O. (1983) Application of graph theory in modelling of biological systems. Proc. 1st Eur. Simulation Congr., ESC, Aachen 1983, pp. 580–87, Ameling, W., ed. Springer, Berlin Heidelberg New York

  6. Gotow, K., Sakaki, T., Kondo, N., Kobayashi, K., Syono, K. (1985a) Light-induced alkalinisation of the suspending medium of guard cell protoplasts from Vicia faba L. Plant Physiol. 79, 825–828

  7. Gotow, K., Tanaka, K., Kondo, N., Kobayashi, K., Syono, K. (1985b) Light activation of NADP-malate dehydrogenase in guard cell protoplasts from Vicia faba L. Plant Physiol. 79, 829–832

  8. Huber, S.C., Sugiyama, T., Akazawa, T. (1986) Light modulation of maize leaf phosphoenolpyruvate carboxylase. Plant Physiol. 82, 550–554

  9. Kluge, M., Maier, P., Brulfert, J., Faist, K., Wollny, E. (1988) Regulation of phosphoenolpyruvate carboxylase in Crassulacean acid metabolism: in vitro phosphorylation of the enzyme. J. Plant Physiol. 133, 252–256

  10. Kottmeier, C., Schnabl, H. (1986) The Km-value of phosphoenolpyruvate carboxylase as an indicator of swelling state of guard cell protoplasts. Plant Sci. 43, 213–217

  11. Lilley, R.M., Ebbinghausen, H., Heldt, H.W. (1987) The simultaneous determination of carbon dioxide release and oxygen uptake in suspensions of plant mitochondria oxidizing glycine. Plant Physiol. 83, 349–353

  12. Michalke, B., Schnabl, H. (1987) The status of adenine nucleotides and malate in chloroplasts, mitochondria and supernatant of guard protoplasts from Vicia faba. J. Plant Physiol. 130, 243–253

  13. Nimmo, G.A., Wilkins, M.B., Fewson, C.A., Nimmo, H.G. (1987) Persistent circadian rhythms in phosphorylation state of phosphoenolypruvate carboxylase from Bryophyllum fedtschenkoi leaves and its sensitivity to inhibition by malate. Planta 170, 408–415

  14. Ogawa, T., Ishikawa, H., Shimida, K., Shibata, K. (1979) Synergistic action of red and blue light and action spectra of malate formation in guard cells of Vicia faba L. Planta 142, 61–65

  15. Outlaw, W.H. (1983) Current concepts on the role of potassium in stomatal movements. Physiol. Plant 59, 302–311

  16. Petraglia, T., Poole, R.J. (1980) ATP-levels and their effects on plasmalemma influxes of potassium chloride in red beet. Plant Physiol. 65, 969–972

  17. Rao, M., Anderson, L.E. (1983) Light and stomatal metabolism. Plant Physiol. 71, 451–455

  18. Raschke, K. (1979) Movements of stomata. In: Encyclopedia of plant physiol., N. S. vol. 7: Physiology of movements, pp. 383–441, Haupt, W., Feinleib, M.E., eds. Springer, Berlin Heidelberg New York

  19. Raschke, K., Schnabl, H. (1978) Availability of chloride affects the balance between potassium chloride and potassium malate in guard cells of Vicia faba L. Plant Physiol. 62, 84–87

  20. Scheibe, R., Wagenpfeil, D., Fischer, J. (1986) NADP-malate dehydrogenase activity during photosynthesis in illuminated spinach chloroplasts. J. Plant Physiol. 124, 103–110

  21. Schnabl, H. (1980) CO2 and malate metabolism in starch-containing and starch lacking guard cell protoplasts. Planta 149, 52–58

  22. Schnabl, H. (1981) The compartmentation of carboxylating and decarboxylating enzymes in guard cell protoplasts. Planta 152, 307–313

  23. Schnabl, H., Kottmeier, C. (1984a) Determination of malate levels during the swelling of vacuoles isolated from guard cell protoplasts. Planta 161, 27–31

  24. Schnabl, H., Kottmeier, C. (1984b) Properties of phosphoenolpyruvate carboxylase in desalted extracts from isolated guard cell protoplasts. Planta 162, 220–225

  25. Schnabl, H., Michalke, B. (1988) The role of oxidative phosphorylation in stomatal opening. Adenylate pool sizes in light- and dark-treated swelling guard cell protoplasts. Life Sci. Adv. Plant Physiol. 7, 203–207

  26. Schnabl, H., Bornman, Ch., Ziegler, H. (1978) Studies in isolated starch-containing and starch-deficient guard cell protoplasts. Planta 143, 33–39

  27. Schröder, J.I., Hedrich, R., Fernandez, J.M. (1984) Potassium-selective single channels in guard cell protoplasts of Vicia faba. Nature 312, 361–362

  28. Sharkey, T.D., Ogawa, T. (1987) Stomatal responses to light. In: Stomatal function, pp. 163–193, Zeiger, E., Farquhar, G.D., Cowen, I.R., eds. Stanford University Press, Stanford

  29. Shimazaki, K., Gotow, K., Sakaki, T., Kondo, N. (1983) High respiratory activity of guard cell protoplasts from Vicia faba L. Plant Cell Physiol. 24, 1049–1056

  30. Wedding, R.T., Black, K. (1986) Malate inhibition of phosphoenolypruvate carboxylase from Crassula. Plant Physiol. 82, 985–990

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Author information

Correspondence to Heide Schnabl.

Additional information

The authors thank Professor Hermann Schnabl, University of Stuttgart (FRG), for his assistance in applying the graph theory analysis. This work was supported by Deutsche Forschungsgemeinschaft to H.S.

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Michalke, B., Schnabl, H. Modulation of the activity of phosphoenolypyruvate carboxylase during potassium-induced swelling of guard-cell protoplasts of Vicia faba L. after light and dark treatments. Planta 180, 188–193 (1990). https://doi.org/10.1007/BF00193994

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Key words

  • Guard cell protoplast
  • Malate Phospho
  • enolpyruvate caboxylase (guard cell)
  • Vicia (guard cell protoplast)