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Potassium channels in Eremosphaera viridis

I. Influence of cations and pH on resting membrane potential and on an action-potential-like response

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Abstract

The dependence of the membrane potential of Eremosphaera viridis on different external concentrations of potassium, sodium, calcium, and protons was compared with the diffusion potential measured in the dark and in the presence of NaN3. In contrast to some other algae, the membrane potential in the light as well as in the dark seemed to be predominantly determined by the calculated diffusion potential and less by an electrogenic pump which, however, seemed to be involved at potassium concentrations >1 mol·m-3 and at higher pHos (>pH 6). Furthermore, some characteristics of an action-potential-like response (CAP) triggered by light-off, and independent of the membrane-potential threshold value, were determined. The CAP had a delay period of 5.4 s and needed 4.5 s for polarization to a plateau. On average, the plateau held for 8.8 s and the CAP lasted 37.7 s. The peak amplitudes of CAP (P AP) exactly followed the Nernst potential of potassium. Other cations like sodium, calcium and protons did not appreciably affect the peak amplitudes of CAP. From these and other results it can be assumed that the CAP is caused by a temporary opening of potassium channels in the plasma membrane of Eremosphaera (Köhler et al., 1983, Planta 159, 165–171). The release of a CAP by light-off has been partly explained by the participation of a transient increase of proton concentration in the cytoplasm. It was possible to trigger a CAP by external pH changes and by the addition of sodium acetate, thus supporting the hypothesis that a pH decrease in the cytoplasm may be one element of the signal transfer from the photosynthetic system to the potassium channels in the plasmalemma. Calcium also seemed to have an influence on triggering the CAP.

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Abbreviations

CAP:

chemical-induced action-potential-like response

E D :

calculated diffusion potential (mV)

E D * :

measured diffusion potential (mV)

E K :

potassium equilibrium potential (mV)

E m :

membrane potential (mV)

P AP :

peak of action potential (mV)

References

  • Beilby, M.J., Coster, H.G.L. (1979) The action potential in Chara corallina. IV. The Hodgkin-Huxley parameters for the plasmalemma. Aust. J. Plant. Physiol. 6, 337–353

    Google Scholar 

  • Beilby, M.J., MacRobbie, E.A.C. (1984) Is calmodulin involved in electrophysiology of Chara corallina. J. Exp. Bot. 35, 568–580

    Google Scholar 

  • Bentrup, F.W. (1974) Lichtabhängige Membranpotentiale bei Pflanzen. Ber. Dtsch. Bot. Ges. 87, 515–528

    Google Scholar 

  • Bentrup, F.W. (1979) Reception and transduction of electrical and mechanical stimuli. In: Encyclopedia of Plant Physiol, N.S., vol. 7: Physiology of movements, pp. 42–70, Haupt, W., Feinleib, M.E., eds. Springer, Berlin Heidelberg New York

    Google Scholar 

  • Bertl, A., Felle, H., Bentrup, F.W. (1984) Amine transport in Riccia fluitans. Cytoplasmic and vacuolar pH recorded by a pH-sensitive microelectrode. Plant Physiol. 76, 75–78

    Google Scholar 

  • Bisson, M.A. (1984) Calcium effects on electrogenic pump and passive permeability of the plasma membrane of Chara corallina. J. Membr. Biol. 82, 59–67

    Google Scholar 

  • Boels, H.D., Hansen, U.P. (1982) Light and electrical current stimulate the same feed-back system in Nitella. Plant Cell Physiol. 30, 289–311

    Google Scholar 

  • Bowman, B.J., Mainzer, S.E., Allen, K.E., Slayman, C.W. (1978) Effects of inhibitors on the plasma membrane and mitochondrial adenosine triphosphatases of Neurospora crassa. Biochim. Biophys. Acta 512, 13–28

    Google Scholar 

  • Bulychev, A.A., Turovetsky, V.B. (1983) Light-triggered changes of membrane potentials in cells of Anthoceros punctatus and their relations to activation of chloroplast ATPase. J. Exp. Bot., 34, 1181–1188

    Google Scholar 

  • Felle, H. (1982) Effects of fusicoccin upon membrane potential. Resistance and current-voltage characteristics in root hairs of Sinapis alba. Plant Sci. Lett. 25, 219–225

    Google Scholar 

  • Felle, H., Bentrup, F.W. (1976) Effect of light upon membrane potential, conductance, and ion fluxes in Riccia fluitans. J. Membr. Biol. 27, 153–170

    Google Scholar 

  • Findlay, G.P., Hope, A.B. (1976) Electrical properties of plant cells. Methods and findings. In: Encyclopedia of plant physiology, vol. 2: Transport in plants II, Part A, Cells, pp. 53–92, Lüttge, U., Pitman, M.G. eds. Springer, Berlin Heidelberg New York

    Google Scholar 

  • Findlay, G.P. (1982) Electrogenic and diffusive components of the membrane of Hydrodictyon africanum. J. Membr. Biol. 68, 179–189

    Google Scholar 

  • Findlay, G.P., Coleman, H.A. (1983) Potassium channels in the membrane of Hydrodictyon africanum. J. Membr. Biol. 75, 241–251

    Google Scholar 

  • Geisweid, H.-J., Simonis, W., Urbach, W. (1982) Electrophysiological membrane properties of the unicellular green alga Eremosphaera viridis. (Abstr.) Plant Physiol. 69, Suppl. 67

    Google Scholar 

  • Gradmann, D. (1976) “Metabolic” action potentials in Acetabularia. J. Membr. Biol. 29, 23–45

    Google Scholar 

  • Gradmann, G., Mummert, H. (1980) Plant action potentials. In: Plant membrane transport: Current conceptual issues, pp. 333–344, Spanswick, R.M., Lucas, W.J., Dainty, J. eds. Elsevier Biomedical Press, Amsterdam

    Google Scholar 

  • Häder, D.-P. (1982) Dependence of the photophobic response of the blue-green alga Phormidium uncinatum, on cations. Arch. Microbiol. 132, 345–348

    Google Scholar 

  • Hansen, U.-P. (1980) Homeostasis in Nitella: Adaption of H+-transport to the photosynthetic load. In: Plant membrane transport: Current conceptual issues, pp. 587–588, Spanswick, R.M., Lucas, W.J., Dainty, J., eds. Elsevier Biomedical Press, Amsterdam

    Google Scholar 

  • Hille, B. (1978) Iomic channels in excitable membranes. Current problems and biophysical approaches. Biophys. J. 22, 283–294

    Google Scholar 

  • Higinbotham, N. (1973) Electropotentials of plant cells. Annu. Rev. Plant Physiol. 24, 25–46

    Google Scholar 

  • Kawamura, G., Shimmen, T., Tazawa, M. (1980) Dependence of the membrane potential of Chara cells on external pH in the presence or absence of internal adenosine triphosphate. Planta 149, 213–218

    Google Scholar 

  • Keifer, D.W., Spanswick, R.M. (1979) Correlation of adenosine triphosphate levels in Chara corallina with the activity of the elctrogenic pump. Plant Physiol. 64, 165–168

    Google Scholar 

  • Keifer, D.W., Lucas, W.J. (1982) Potassium channels in Chara corallina. Control and interaction with the electrogenic H+ pump. Plant Physiol. 69, 781–788

    Google Scholar 

  • Köhler, K. (1982) Untersuchungen zum elektrogenen Membrantransport bei einer photoautotrophen Suspensionskultur von Chenopodium rubrum. Ph. D. thesis, University of Tübingen

  • Köhler, K., Geisweid, H.-J., Simonis, W., Urbach, W. (1983) Changes in membrane potential and resistance caused by transient increase of potassium conductance in the unicellular green alga Eremosphaera viridis. Planta 159, 165–171

    Google Scholar 

  • Köhler, K., Steigner, W., Seubert, A., Urbach, W., Simonis, W. (1984) Action potential and potassium channels of the nnicellular green alga Eremosphaera viridis. In: Membrane transport in plants, pp. 214–215, Cram, W.J., janacek, K., Rybova, R., Sigler, K. eds. Academia, Praha

    Google Scholar 

  • Köhler, K., Steigner, W., Kolbowski, J., Hansen, U.-P., Simonis, W., Urbach, W. (1986) Potassium channels in Eremosphaera viridis. II. Current and voltage clamp experiments, Planta 167, in press

  • McLaughlin, S.G.A., Dilger, J.P. (1980) Transport of protons across membranes by weak acids. Physiol. Rev. 60, 825–863

    Google Scholar 

  • Marmé, D., Dieter, P. (1982) Calcium and calmodulin dependent enzyme regulation in higher plants. In: Plasmalemma and tonoplast: Their functions in the plant cell, pp. 111–120, Marmé, D., Marré, E., Hertel, R., eds. Elsevier biomedical press, Amsterdam

    Google Scholar 

  • Martens, J., Hansen, U.P., Warncke, J. (1979) Further evidence for the parallel pathway model of the metabolic control of the electrogenic pump in Nitella as obtained from the high frequency slope of the action of light. J. Membr. Biol. 48, 115–139

    Google Scholar 

  • Mummert, H., Gradmann, D. (1976) Voltage dependent potassium fluxes and the significance of action potentials in Acetabularia. Biochim. Biophys. Acta 443, 443–450

    Google Scholar 

  • Nultsch, W. (1983) The photocontrol of movement of Chlamydomonas. In: The Biology of photoreception, pp. 521–539, Cosens, D.J., Vince-Prue, D., eds. Symp. Soc. Exp. Biol. vol. 36. Cambridge Univ. Press.

  • Richards, J.L., Hope, A.B. (1974) The role of protons in determining membrane electrical characteristics in Chara corallina. J. Membr. Biol. 16, 121–144

    Google Scholar 

  • Sanders, D., Hansen, U.P., Slayman, C.L. (1981) Role of the plasma membrane proton pump in pH regulation in nonanimal cells. Proc. Natl. Acad. Sci. USA 78, 5903–5907

    Google Scholar 

  • Schefczik, K., Simonis, W., Schiebe, M. (1983) Continuous registration of membrane resistances of plant cells using a single electrode technique. Plant Physiol. 72, 368–375

    Google Scholar 

  • Schwarz, W., Passow, H. (1983) Ca2+-activated K+-channels in erythrocytes and excitable cells. Annu. Rev. Physiol. 45, 359–374

    Google Scholar 

  • Shimmen, T., Tazawa, M. (1980) Intracellular chloride and potassium ions in relation to excitability of Chara membrane. J. Membr. Biol. 55, 223–232

    Google Scholar 

  • Shimmen, T., Tazawa, M. (1983) Activation of K+-channel in membrane excitation of Nitella axilliformis. Plant Cell Physiol. 24, 1511–1524

    Google Scholar 

  • Sinclair, J. (1968) The influence of light on the ion fluxes and electrical potential of the leaf cells of the moss Hookeria lucens. J. Exp. Bot. 19, 254–263

    Google Scholar 

  • Smith, A., Raven, J.A. (1979) Intracellular pH and its regulation. Annu. Rev. Plant Physiol. 30, 289–311

    Google Scholar 

  • Smith, F.A. (1984) Regulation of cytoplasmic pH of Chara corallina: Responses to changes in external pH. J. Exp. Bot. 35, 43–50

    Google Scholar 

  • Song, P.-S. (1983) Protozoan and related photoreceptors; molecular aspects. Annu. Rev. Biophys. Bioeng. 12, 35–68

    Google Scholar 

  • Spanswick, R.M. (1972) Evidence for an electrogenic ion pump in Nitella translucens. I. The effects of pH, K+, Na+, light, and temperature on the membrane potential and resistance. Biochim. Biophys. Acta 82, 73–83

    Google Scholar 

  • Spanswick, R.M. (1981) Electrogenic ion pumps. Annu. Rev. Plant Physiol. 32, 267–289

    Google Scholar 

  • Taylor, R.E. (1974) Excitable membranes. Annu. Rev. Phys. Chem. 25, 387–405

    Google Scholar 

  • Tazawa, M., Shimmen, T. (1980) Action potential in Characeae: Some characteristics revealed by internal perfusion studies. In: Plant membrane transport: Current conceptual issues, pp. 349–362, Spanswick, R.M., Lucas, W.J., Dainty, J., eds. Elsevier/North-Holladn Biomedical Press

  • Ulbricht, W. (1977) Iortic channels and gating currents in excitable membranes. Annu. Rev. Biophys. Bioeng. 6, 7–31

    Google Scholar 

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Part II will appear in Planta, Vol. 167, No. 1, 1986

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Köhler, K., Steigner, W., Simonis, W. et al. Potassium channels in Eremosphaera viridis . Planta 166, 490–499 (1985). https://doi.org/10.1007/BF00391273

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