Abstract
A quantitative analysis of the time- and voltage-dependent kinetics of the guard cell anion channel (GCAC1) current in guard cell protoplasts from Vicia faba was analyzed using the whole-cell patch clamp technique. The voltage-dependent steady-state activation of GCAC1 current followed a Boltzmann distribution. For the corresponding steady-state value of the activation variable a power of two was derived which yielded suitable fits of the time course of voltage-dependent current activation. The GCAC1 mediated chloride current could successfully be described in terms of the Hodgkin-Huxley equations commonly evoked for the Na channel in nerve. After step depolarizations from a potential in the range of the resting potential to potentials above the equilibrium potential for chloride an activation and also an inactivation could be described. The gating of both processes exhibited an inverse relationship on the polarity of the applied step potentials in the order of milliseconds. Deactivating tail currents decline exponentially. The presented analysis contributes to the understanding of the rising phase of the observed action potentials in guard cells of V. faba. Evidence is presented that the voltage-dependent kinetic properties of the GCAC1 current are different from those properties described for the excitable anion currents in the plasmalemma of Chara corallina (Beilby & Coster, 1979a).
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Beilby, M.J., Coster, H.G.L. 1979a. The action potential in Chara corallina III. The Hodgkin-Huxley parameters for the plasmalemma. Austr. J. Plant Physiol. 6:337–353
Beilby, M.J., Coster, H.G.L. 1979b. The action potential in Chara corallina II. Two activation-inactivation transients in voltage clamps of the plasmalemma. Austr. J. Plant Physiol. 6:323–335
Beilby, M.J. 1984. Calcium and plant action potentials. Plant Cell Environ. 7:415–421
Barry, P.W., Lynch, J.W. 1991. Liquid junction potential and small cell effects in patch-clamp analysis. J. Membrane Biol. 121:101–117
Blatt, M.R. 1991. Ion channel gating in plants: Physiological implications and integration for stomatal function. J. Membrane Biol. 124:95–112
Fairley-Grenot, K.A., Assmann, S.M. 1993. Comparison of K+-channel activation and deactivation in guard cells from a dicotyledon (Vicia faba L.) and a graminaceous monocotyledon (Zea mays). Planta 189:410–419
Gradmann, D., Blatt, M.R., Thiel, G. 1993. Electrocoupling of ion transport in plants. J. Membrane Biol. 136:327–332
Hamill, O.P., Marty, A., Neher, E., Sakmann, B., Sigworth, F.J. 1981. Improved patch-clamp techniques for high-resolution current recording from cells and cell-free membrane patches. Pfluegers Arch. 391:85–100
Hedrich, R. 1994. Voltage-dependent chloride channels in plant cells. Identification, characterization, and regulation of a guard cell anion channel. Current Topics in Membranes and Transport 42:1–33
Hedrich, R., Becker, D. 1994. Green circuits—The potential of plant specific ion channels. Plant Molec. Biol. 26:1637–1650
Hedrich, R., Busch, H., Raschke 1990. Ca2+-and nucleotide dependent regulation of voltage-dependent anion channels in the plasma membrane of guard cells. EMBO J. 9:3889–3892
Hedrich, R., Dietrich, P. 1994. Interconversion of fast and slow gating modes of GCAC1, a guard cell anion channel. Planta 195:301–304
Hedrich, R., Marten, I. 1993. Malate-induced feedback regulation of plasma membrane anion channels could provide a CO2 sensor to guard cells. EMBO J. 12:897–901
Hedrich, R., Marten, I., Lohse, G., Dietrich, P., Winter, H., Lohaus, G., Heldt, H.-W. 1994. Malate-sensitive anion channels enable guard cells to sense changes in the ambient CO2 concentration. Plant J. 6:741–748
Hille, B. 1978. Ionic channels in excitable membranes. Current problems and biophysical approaches. Biophys. J. 22:283–294
Hille, B. 1992. Ionic Channels of Excitable Membranes. Sinauer Associates, Sunderland, MA
Hodgkin, A.L., Huxley, A.F. 1952. A quantitative description of membrane current and its application to conduction and excitation in nerve. J. Physiol. 117:500–544
Keller, B.U., Hedrich, R., Raschke, K. 1989. Voltage-dependent anion channels in the plasma membrane of guard cells. Nature 341:450–453
Kikuyama, M., Oda, K., Shimmen, T., Hayama, T., Tazawa, M. 1984. Potassium and chloride efflux during excitation of Characeae cells. Plant Cell Physiol. 25:965–974
Linder, B., Raschke, K. 1992. A slow anion channel in guard cells, activating at large hyperpolarization, may be principal for stomatal closing. FEBS Lett. 313:27–30
Lohse, G., Hedrich, R. 1992. Characterization of the plasma-membrane H+-ATPase from Vicia faba guard cells. Modulation by extracellular factors and seasonal changes. Planta 188:206–214
Lohse, G., Hedrich R. 1995. Anions modify the response of guard cell anion channels to auxin. Planta (in press)
Marten, I., Lohse, G., Hedrich, R. 1991. Plant growth hormones control voltage-dependent activity of anion channels in plasma membrane of guard cells. Nature 353:758–762
Marten, I., Zeilinger, C., Redhead, C., Landry, D.W., Al-Awqati, Q., Hedrich, R. 1992. Identification and modulation of a voltagedependent anion channel in the plasma membrane of guard cells by high-affinity ligands. EMBO J. 11:3569–3575
Marty, A., Neher, E. 1983. Tight seal whole-cell recording. In Single Channel Recording. B. Sakmann and E. Neher, editors, pp. 107–121. Plenum, New York
Neher, E. 1992. Correction for liquid junction potentials in patch-clamp experiments. Meth. in Enzymol. 207:128–131
Schroeder, J.I. 1989. Quantitative analysis of outward rectifying K+ channel currents in guard cell protoplasts from Vicia faba. J. Membrane Biol. 107:229–235
Schroeder, J.I., Hagiwara, S. 1989. Cytosolic calcium regulates ion channels in the plasma membrane of Vicia faba guard cells. Nature 338:427–430
Schroeder, J.I., Hedrich, R. 1989. Involvement of ion channels and active transport in osmoregulation and signaling of higher plant cells. Trends Biochem. Sci. 5:187–192
Schroeder, J.I., Keller, B.U. 1992. Two types of anion channel currents in guard cells with distinct voltage regulation. Proc. Natl. Acad. Sci. USA 89:5025–5029
Schroeder, J.I., Raschke, K., Neher, E. 1987. Voltage-dependence of K+ channels in guard-cell protoplasts. Proc. Natl. Acad. Sci. USA 84:4108–4112
Sussman M.R. 1992. Shaking Arabidopsis thaliana. Science 256:619
Tazawa, M., Shimmen, T., Mimura, T. 1987. Membrane control in the Characeae. Ann. Rev. Plant Physiol. 38:95–117
Thiel, G., Homann, U., Gradmann, D. 1993. Microscopic elements of electrical excitation in Chara: Transient activity of Cl− channels in the plasma membrane. J. Membrane Biol. 134:53–66
Thiel, G., MacRobbie, E.A.C., Blatt, M.R. 1992. Membrane transport in stomatal guard cells: The importance of voltage control. J. Membrane Biol. 126:1–18
Van Duijn, B. 1993. Hodgkin-Huxley analysis of whole-cell outward rectifying K+-currents in protoplasts from tobacco cell suspension cultures. J. Membrane Biol. 132:77–85
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The authors gratefully acknowledge the encouragement of Dr. David Colquhoun to apply the Hodgkin-Huxley model to the GCAC1 channel. The work was in part supported by a grant of the Deutsche Forschungsgemeinschaft to R.H. and a grant of the Herman and Lilly Schilling Stiftung to H.-A.K.
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Kolb, H.A., Marten, I. & Hedrich, R. Hodgkin-Huxley analysis of a GCAC1 anion channel in the plasma membrane of guard cells. J. Membarin Biol. 146, 273–282 (1995). https://doi.org/10.1007/BF00233947
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DOI: https://doi.org/10.1007/BF00233947