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Stretch-activated chloride, potassium, and calcium channels coexisting in plasma membranes of guard cells of Vicia faba L.

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Abstract

Mechanosensitive ion channels in the plasma membrane of Vicia faba guard cell protoplasts were studied by use of the patch clamp technique. Stretch-activated (SA) channels in outside-out patches were analyzed for channel conductance, kinetics and ion selectivity. We found three distinct SA channels, permeable to Cl, K+ and Ca2+ and distinguishable from spontaneous (non-SA) channels for these ions on the basis of conductance, kinetics, and voltage-dependence, as well as sensitivity to membrane stretch. In the attached patch configuration, light suction (2 to 10 kPa) reversibly induced channel opening with multiple amplitudes and complex kinetics. The open probability for SA channels increased nonlinearly with pipette suction. In guard cells in situ, these SA channels may mediate ion transport across the plasma membrane directly, as well as influence the activity of non-SA channels via effects on membrane voltage and cytoplasmic calcium. Through such effects, SA channels likely influence volume and turgor regulation of guard cells, and thereby control of leaf gas exchange.

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Abbreviations

EK:

equilibrium potential for potassium transport

ECl :

equilibrium potential for chloride transport

SA:

stretchactivated

References

  • Blatt, M.R. (1988) Mechanisms of fusicoccin action: a dominant role for secondary transport in a higher-plant cell. Planta 174, 187–200

    Google Scholar 

  • Colquhoun, D., Sigworth, F.J. (1983) Fitting and statistical analysis of single-channel records. In: Single-channel recording, pp. 191–264, Sakmann, B., Neher, E., eds., Plenum Press, New York London

    Google Scholar 

  • Delcour, A.H., Martinac, B., Adler, J., Kung, C. (1989) Modified reconstitution method used in patch-clamp studies of Escherichia coli ion channels. Biophys. J. 56, 631–636

    Google Scholar 

  • Falke, L., Edwards, K.L., Pickard, B.G., Misler, S.A. (1988) A stretch-activated anion channel in tobacco protoplasts. FEBS Lett. 237, 141–144

    Google Scholar 

  • Farquhar, G.D., Dubbe, D.R., Raschke, K. (1978) Gain of the feedback loop involving carbon dioxide and stomata: theory and measurement. Plant Physiol. 62, 406–412

    Google Scholar 

  • Fatt, P., Ginsborg, B.L. (1958) The ionic requirements for the production of action potentials in crustacean muscle fibres. J. Physiol. 142, 516–543

    Google Scholar 

  • Fenwick, E.M., Marty, A., Neher, E. (1982) A patch-clamp study of bovine chromaffin cells and of their sensitivity to acetylcholine. J. Physiol. 331, 577–597

    Google Scholar 

  • Guharay, F., Sachs, F.J. (1984) Stretch-activated single ion channel currents in tissue-cultured embryonic chick skeletal muscle. J. Physiol. 352, 685–701

    Google Scholar 

  • Gustin, M.C., Zhou, X.-L., Martinac, B., Kung, C. (1988) A mechanosensitive ion channel in the yeast plasma membrane. Science 242, 762

    Google Scholar 

  • 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

    Google Scholar 

  • Hedrich, R., Busch, H., Raschke, K. (1990) Ca2+- and nucleotide-dependent regulation of voltage-dependent anion channels in the plasma membrane of guard cells. EMBO J. 9, 3889–3892

    Google Scholar 

  • Hedrich, R., Neher, E. (1987) Cytosplamic calcium regulates voltage-dependent ion channels in plant vacuoles. Nature 329, 833–835

    Google Scholar 

  • Hedrich, R., Schroeder, J.I. (1989) The physiology of ion channels and electrogenic pumps in higher plants. Annu. Rev. Plant Physiol. 40, 539–569

    Google Scholar 

  • Howard, J., Roberts, W.M., Hudspeth, A.J. (1988) Mechanoelectrical transduction by hair cells. Annu. Rev. Biophys. Biophys. Chem. 17, 99–124

    Google Scholar 

  • Keller, B.U., Hedrich, R., Raschke, K. (1989) Voltage-dependent anion channels in the plasma membrane of guard cells. Nature 341, 450–453

    Google Scholar 

  • MacRobbie, E.A.C. (1988) Control of ion fluxes in stomatal guard cells. Bot. Acta 101, 140–148

    Google Scholar 

  • Mansfield, T.A., Hetherington, A.M., Atkinson, C.J. (1990) Some current aspects of stomatal physiology. Annu. Rev. Plant Physiol. Plant Mol. Biol. 41, 55–75

    Google Scholar 

  • Marten, I., Lohse, G., Hedrich, R. (1991) Plant growth hormons control voltage dependent activity of an ion channel in plasma membrane of guard cells. Nature, 353, 758–762

    Google Scholar 

  • Martinac, B., Buechner, M., Delcour, A.H., Adler, J., Kung, C. (1987) Pressure-sensitive ion channel in Escherichia coli. Proc. Nat. Acad. Sci. USA 84, 2297–2301

    Google Scholar 

  • Morris, C.E. (1990) Mechanosensitive ion channels. J. Membr. Biol. 113, 93–107

    Google Scholar 

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

    Google Scholar 

  • Pierce, S.K., Politis, A.D. (1990) Ca2+-activated cell volume receovery mechanisms. Annu. Rev. Physiol. 52, 27–42

    Google Scholar 

  • Raschke, K. (1970) Stomatal responses to pressure changes and interruptions in the water supply of detached leaves of Zea mays L. Plant Physiol. 45, 415–423

    Google Scholar 

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

    Google Scholar 

  • Raschke, K., Hedrich, R. (1989) Patch clamp measurements on isolated guard cell protoplasts and vacuoles. Methods Enzymol. 174, 312–330

    Google Scholar 

  • Sachs, F. (1986a) Mechanotransducing ion channels. In: Ionic channels in cells and model systems, pp. 181–193, Latorre, R., ed. Plenum, New York

    Google Scholar 

  • Sachs, F. (1986b) Biophysics of mechanoreception. Membr. Biochem. 6, 173–195

    Google Scholar 

  • Schroeder, J.I., Hagiwara, S. (1989) Cytosolic calcium regulates ion channels in the plasma membrane of Vicia faba guard cells. Nature 338, 427–430

    Google Scholar 

  • Schroeder, J.I., Hedrich, R. (1989) Involvement of ion channels and active transport in osmoregulation and signaling of higher plant cells. Trends Biochem. Sci. 14, 187–192

    Google Scholar 

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

    Google Scholar 

  • Schroeder, J.I., Raschke, K., Neher, E. (1987) Voltage dependence of K+ channels in guard-cell protoplasts. Proc. Nat. Acad. Sci. USA 84, 4108–4112

    Google Scholar 

  • Sharpe, P.J.H., Wu, H., Spence, R.D. (1987) Stomatal mechanics. In: Stomatal function, Zeiger, E., Farquhar, G.D., Cowan, I.R., eds. Stanford Univ. Press, Stanford

    Google Scholar 

  • Sigworth, F. (1983) An example of analysis. In: Single-channel recording, pp. 301–322, Sakmann, B., Neher, E., eds., Plenum Press, New York London

    Google Scholar 

  • Zeiger, E. (1983) The biology of stomatal guard cells. Annu. Rev. Plant Physiol. 34, 441–475

    Google Scholar 

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Dedicated to the 80. birthday of Franz Hedrich

Supported by a grant from the Deutsche Forschungsgemeinschaft to R.H. and a Department of Energy grant to D.J.C. gratefully acknowledges a John S. Guggenheim Fellowship and Fulbright Kommission Senior Professor Award. We thank Ingrid Baumann and Angela Schön for technical assistance, and Klaus Raschke and Heiner Busch for spirited discussions and support.

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Cosgrove, D.J., Hedrich, R. Stretch-activated chloride, potassium, and calcium channels coexisting in plasma membranes of guard cells of Vicia faba L.. Planta 186, 143–153 (1991). https://doi.org/10.1007/BF00201510

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