Electrophysiology of the Plasma Membrane of Higher Plant Cells: New Insights from Patch-Clamp Studies

  • R. Hedrich
  • H. Stoeckel
  • K. Takeda

Abstract

There can be little argument as to the fundamental importance of ion transport mechanisms for the physiology of plant cells. While excitable electrical behavior was first observed in plant cells about a century ago (e.g., Sanderson 1888), the underlying mechanisms responsible for this behavior are only now being directly studied at the molecular level. Ion channels are integral transmembrane proteins, which when open allow the movement of ions and some nonelectrolytes down their electrochemical gradients (for review, Hille 1984; Catterall 1988). Although ionic currents in plant cell membranes were among the first to be studied in detail (e.g., Michaelis 1925; Cole and Curtis 1938), by comparison with their animal cell counterparts the electrophysiological characterization of plant ion channels has been somewhat slower. This has been due to problems specific to plant cells, such as the presence of the cell wall, having the plasma membrane and vacuolar membrane in series, and the relatively small cytoplasmic compartment. The latter is especially a problem in higher plants.

Keywords

Sugar Permeability Cellulose Sucrose Mold 

Abbreviations

FV

fast vacuole

SV

slow vacuole

TEA

triethanolamine

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References

  1. Assmann SM, Simoncini L, Schroeder JI (1985) Blue light activates electrogenic ion pumping in guard cell protoplasts of Vicia faba. Nature 318: 285–287CrossRefGoogle Scholar
  2. Beilby MJ (1982) CI- channels in Chara. Philos Trans R Soc Lond B 299: 435–455CrossRefGoogle Scholar
  3. Bertl A, Gradmann D (1987) Current-voltage relationships of potassium channels in the plasmalemma of Acetabularia. J Membr Biol 99: 41–49CrossRefGoogle Scholar
  4. Bertl A, Klieber HG, Gradmann D (1988) Slow kinetics of a potassium channel in Acetabularia. J Membr Biol 102: 141–152CrossRefGoogle Scholar
  5. Blatt MR, Slayman CL (1987) Role of “active” potassium transport in the regulation of cytoplasmic pH by nonanimal cells. Proc Natl Acad Sci USA 84: 2737–2741PubMedCrossRefGoogle Scholar
  6. Blum W, Hinsch K-D, Schulz G, Weiler EW (1988) Identification of GTP-binding proteins in the plasma membrane of higher plants. Biochem Biophys Res Commun 156: 954–959PubMedCrossRefGoogle Scholar
  7. Bush DS, Hedrich R, Schroeder JI, Jones RL (1988) Channel-mediated K+ flux in barley aleurone protoplasts. Planta 176: 368–377CrossRefGoogle Scholar
  8. Catterall WA (1988) Structure and function of voltage-sensitive ion channels. Science 242: 50–61PubMedCrossRefGoogle Scholar
  9. Cole KS, Curtis HJ (1938) Electric impedance of Nitella during activity. J Gen Physiol 22: 37–64PubMedCrossRefGoogle Scholar
  10. Coleman HA (1986) CI- currents in Chara — a patch clamp study. J Membr Biol 93: 55–61CrossRefGoogle Scholar
  11. Colombo R, Cerana R, Lado P, Peres A (1988) Voltage-dependent channels permeable to K+ and Na+ in the membrane of Acer pseudoplatanus vacuoles. J Membr Biol 103: 227–236CrossRefGoogle Scholar
  12. Coyaud L, Kurkdjian A, Kado R, Hedrich R (1987) Ion channels and ATP-driven pumps involved in ion transport across the tonoplast of sugarbeet vacuoles. Biochim Biophys Acta 902: 263–268CrossRefGoogle Scholar
  13. Edwards KL, Pickard BG (1987) Detection and transduction of physical stimuli in plants. In: Wagner E, Greppin H, Biller B (eds) The cell surface in signal transduction. NATO ASI Series H12. Springer, Berlin Heidelberg New York Tokyo, pp 41–66CrossRefGoogle Scholar
  14. Ettlinger C, Lehle L (1988) Auxin induces rapid changes in phosphatidylinositol metabolites. Nature 331: 176–178PubMedCrossRefGoogle Scholar
  15. Falke LC, Edwards KL, Pickard BG, Misler S (1988) A stretch-activated anion channel in tobacco protoplasts. FEBS Lett 237: 141–144PubMedCrossRefGoogle Scholar
  16. Findlay GP (1961) Voltage-clamp experiments with Nitella. Nature 191: 812–814CrossRefGoogle Scholar
  17. Findlay GP, Hope AB (1976) Electrical properties of plant cells: methods and findings. In: Luttge U, Pitman MG (eds) Encyclopedia of plant physiology, new series, Vol. 2, Part A. Transport in plants. Springer, Berlin Heidelberg New York, pp 53–92Google Scholar
  18. Frank E, Tauc L (1964) Voltage clamp studies of molluscan neuron membrane properties. In: Hoffmann JF (ed) The cellular functions of membrane transport. Prentice Hall, Englewoods Cliff NJ, pp 26–51Google Scholar
  19. Gilroy S, Blowers DP, Trewavas A J (1987) Calcium: a regulation system emerges in plant cells. Development 100: 181–184Google Scholar
  20. Hamill OP, Marty A, Neher E, Sakmann B, Sigworth FJ (1981) Improved patch clamp techniques for high resolution current recording from cells and cell-free membrane patches. Pflügers Arch 391: 85–100PubMedCrossRefGoogle Scholar
  21. Hedrich R, Kurkdjian A (1988) Characterization of an anion-permeable channel from sugar beet vacuoles: effect of inhibitors. EMBO J 7: 3661–3666PubMedGoogle Scholar
  22. Hedrich R, Neher E (1987) Cytoplasmic calcium regulates voltage-dependent ion channels in plant vacuoles. Nature 329: 833–836CrossRefGoogle Scholar
  23. Hedrich R, Schroeder JI (1989) The physiology of ion channels and electrogenic pumps in higher plants. Annu Rev Plant Physiol Plant Mol Biol 40: 539–569CrossRefGoogle Scholar
  24. Hedrich R, Flttgge UI, Fernandez JM (1986) Patch-clamp studies of ion transport in isolated plant vacuoles. FEBS Lett 204: 228–232CrossRefGoogle Scholar
  25. Hedrich R, Schroeder JI, Fernandez JM (1987) Patch-clamp studies on higher plant cells: a perspective. Trends Biochem Sci 12: 49–52CrossRefGoogle Scholar
  26. Hedrich R, Barbier-Brygoo H, Felle H, Flttgge UI, Maathuis FJM, Marx S, Prins HBA, Raschke K, Schnabl H, Schroeder JI, Struve I, Taiz L, Ziegler P (1988) General mechanisms for solute transport across the tonoplast of plant vacuoles: a patch-clamp survey of ion channels and proton pumps. Bot Acta 101: 7–13Google Scholar
  27. Hille B (1984) Ionic channels of excitable membranes. Sinauer, SunderlandGoogle Scholar
  28. Hodgkin AL (1964) The conduction of the nervous impulse. Ch C Thomas, Springfield, MAGoogle Scholar
  29. Homble F, Ferrier JM, Dainty J (1987) Voltage-dependent K+ -channels in protoplasmic droplets of Chara corallina. Plant Physiol 83: 53–57PubMedCrossRefGoogle Scholar
  30. Hornberg C, Weiler EW (1984) High-affinity binding sites for abscisic acid on the plasmalemma of Vicia faba guard cells. Nature 370: 321–324CrossRefGoogle Scholar
  31. Hosoi S, Lino M, Shimazaki K (1988) Outward-rectifying K+ channels in stomatal guard cell protoplasts. Plant Cell Physiol 29: 907–911Google Scholar
  32. Iijima T, Hagiwara S (1987) Voltage dependent K+ channels in protoplasts of trap-lobe cells of Dionea muscipula. J Membr Biol 100: 73–81PubMedCrossRefGoogle Scholar
  33. Jaffe LF, Nuccitelli R (1977) Electrical controls of development. Annu Rev Biophys Bioeng 6: 445–476PubMedCrossRefGoogle Scholar
  34. Jones RL (1973) Gibberellic acid and ion release from barley aleurone tissue. Plant Physiol 52: 303–308PubMedCrossRefGoogle Scholar
  35. Kado RT, Kurkdjian A, Takeda K (1986) Transport mechanisms in plant cell membranes: an application for the patch clamp technique. Physiol Veg 24: 227–244Google Scholar
  36. Kolb HA, Kohler K, Martinoia E (1987) Single potassium channels in membranes of isolated mesophyll barley vacuoles. J Membr Biol 95: 163–169CrossRefGoogle Scholar
  37. Krawczyk S (1978) Ionic channel formation in a living cell membrane. Nature 273: 56–57PubMedCrossRefGoogle Scholar
  38. Laver DR, Walker NA (1987) Steady-state voltage dependent gating and conduction kinetics of single K+ channels in the membrane of cytoplasmic drops of Chara australis. J Membr Biol 100: 31–42CrossRefGoogle Scholar
  39. Lühring HE (1986) Recording of single K+ channels in the membrane of cytoplasmic drop of Chara australis. Protoplasma 133: 19–28CrossRefGoogle Scholar
  40. Lunevsky VZ, Zherelova OM, Vostrikov IY, Berestovsky GN (1983) Excitation of Characeae cell membranes as a result of activation of calcium and chloride channels. J Membr Biol 72: 43–58CrossRefGoogle Scholar
  41. Lüttge U, Pitman MG (eds) (1976) Transport in plants. Vols. I, II & III. Springer, Berlin Heidelberg New YorkGoogle Scholar
  42. Michaelis L (1925) Contribution to the theory of permeability of membranes for electrolytes. J Gen Physiol 8: 33–59PubMedCrossRefGoogle Scholar
  43. Moran N, Ehrenstein G, Iwasa K, Bare C, Mischke C (1984) Ion channels in plasmalemma of wheat protoplast. Science 226: 835–838PubMedCrossRefGoogle Scholar
  44. Moran N, Ehrenstein G, Iwasa K, Mischke C, Bare C, Satter RL (1988) Potassium channels in motor cells of Samanea saman: a patch clamp study. Plant Physiol 88: 643–648PubMedCrossRefGoogle Scholar
  45. Muller U, Malchow D, Hartung K (1986) Single ion channels in the slime mold Dictyostelium discoideum. Biochim Biophys Acta 857: 287–290PubMedCrossRefGoogle Scholar
  46. Mullins LJ (1962) Efflux of chloride ions during the action potential of Nitella. Nature 196: 986–987PubMedCrossRefGoogle Scholar
  47. Nagata T, Takebe I (1970) Cell wall regeneration and cell division in isolated tobacco mesophyll protoplasts. Planta 92: 301–308CrossRefGoogle Scholar
  48. Neher E, Sakmann B (1976) Single-channel currents recorded from membrane of denervated frog muscle fibres. Nature 260: 799–802PubMedCrossRefGoogle Scholar
  49. Neher E, Stevens CF (1977) Conductance fluctuations and ionic pores in membranes. Annu Rev Biophys Bioeng 6: 345–381PubMedCrossRefGoogle Scholar
  50. Neher E, Sakmann B, Steinbach JH (1978) The extracellular patch clamp: a method for resolving currents through individual open channels in biological membranes. Pflügers Arch 375: 219–228PubMedCrossRefGoogle Scholar
  51. Outlaw WH (1983) Current concepts on the role of potassium in stomatal movements. Physiol Plant 59: 302–311CrossRefGoogle Scholar
  52. Pilet PE (ed) (1985) The physiological properties of plant protoplasts. Springer, Berlin Heidelberg New York TokyoGoogle Scholar
  53. Poovaiah BW, Reddy ASN (1987) Calcium messenger systems in plants. CRC Crit Rev Plant Sci 6: 47–103PubMedCrossRefGoogle Scholar
  54. Rae JL, Levis RA (1984) Patch voltage clamp of lens epithelial cells: theory and practise. Mol Physiol 6: 115–162Google Scholar
  55. Ranjeva R, Boudet AM (1987) Phosphorylation of proteins in plants: regulatory effects and potential in stimulus/response coupling. Annu Rev Plant Physiol 38: 73–93CrossRefGoogle Scholar
  56. Raschke K (1979) Movements of stomata. In: Haupt, W, Feinleib E (eds) Encyclopedia of plant physiology, new series. Vol. 7. Springer, Berlin Heidelberg New York, pp 383–441Google Scholar
  57. Raschke K, Hedrich R (1989) Patch-clamp measurements on isolated guard cell protoplasts and vacuoles. Methods Enzymol 174, in pressGoogle Scholar
  58. Saimi Y, Martinac B, Gustin MC, Culbertson MR, Adler J, Kung C (1988) Ion channels in Paramecium, yeast and Escherichia coli. Trends Biochem Sci 13: 304–309PubMedCrossRefGoogle Scholar
  59. Sakmann B, Neher E (eds) (1983) Single channel recording. Plenum, New YorkGoogle Scholar
  60. Sanderson JB (1888) On the electromotive properties of the leaf of Dionaea in the excited and unexcited states. Philos Trans R Soc Lond B 179: 417–449CrossRefGoogle Scholar
  61. Satter RL, Moran N (1988) Ionic channels in plant cell membranes. Physiol Plant 72: 816–820CrossRefGoogle Scholar
  62. Satter RL, Geballe GT, Applewhite PB, Galston AW (1974) Potassium flux of leaf movements in Samanea saman. I. Rhythmic movement. J Gen Physiol 64: 413–430PubMedCrossRefGoogle Scholar
  63. Satter RL, Morse MJ, Lee Y, Crain RC, Cote GG, Moran N (1988) Light- and clock-controlled leaflet movements in Samanea saman: a physiological, biophysical and biochemical analysis. Bot Acta 101: 205–213Google Scholar
  64. Schauf CL, Wilson KJ (1987a) Properties of single K+ and CI- channels in Asclepias tuberose protoplasts. Plant Physiol 85: 413–441PubMedCrossRefGoogle Scholar
  65. Schauf CL, Wilson KJ (1987b) Effect of abscisic acid on K+ channels in Vicia faba guard cell protoplasts. Biochem Biophys Res Commun 145: 284–290PubMedCrossRefGoogle Scholar
  66. Schroeder JI (1988) K+ transport properties of K+ channels in the plasma membrane of Vicia faba guard cells. J Gen Physiol 92: 667–684PubMedCrossRefGoogle Scholar
  67. Schroeder JI, Hedrich R (1989) A model for the concerted action of ion transport mechanisms across guard cell membranes. Trends Biochem Sci 14: 187–192PubMedCrossRefGoogle Scholar
  68. Schroeder JI, Hedrich R, Fernandez JM (1984) Potassium-selective single channels in guard cell protoplasts. Nature 312: 361–362CrossRefGoogle Scholar
  69. Schroeder JI, Raschke K, Neher E (1987) Voltage dependence of K+ channels in guard cell protoplasts. Proc Natl Acad Sci USA 84: 4108–4112PubMedCrossRefGoogle Scholar
  70. Schumaker K, Sze H (1987) Inositol 1,4,5-triphosphate releases Ca2+ from vacuolar membrane vesicles of oat roots. J Biol Chem 262: 3944–3946PubMedGoogle Scholar
  71. Serrano EE, Zeiger E, Hagiwara S (1988) Red light stimulates an electrogenic proton pump in Vicia faba guard cell protoplasts. Proc Natl Acad Sci USA 85: 436–440PubMedCrossRefGoogle Scholar
  72. Serrano R (1988) Structure and function of proton translocating ATPase in plasma membranes of plants and fungi. Biochim Biophys Acta 947: 1–28PubMedGoogle Scholar
  73. Shiina T, Wayne R, Lim Tung HY, Tazawa M (1988) Possible involvement of protein phosphorylation/dephosphorylation in the modulation of Ca2+ channel in tonoplast-free cells of Nitellopsis. J Membr Biol 102: 255–264CrossRefGoogle Scholar
  74. Sibaoka T (1966) Action potentials in plant organs. Symp Soc Exp Biol 20: 49–74PubMedGoogle Scholar
  75. Simons PJ (1981) The role of electricity in plant movements. New Phytol 87: 11–37CrossRefGoogle Scholar
  76. Smith TG, Lecar H, Redman SJ, Gage PW (eds) (1985) Voltage and patch clamping with microelectrodes. Williams & Wilkins, BaltimoreGoogle Scholar
  77. Sokolik AI, Yurin VM (1986) Potassium channels in plasmalemma of Nitella cells at rest. J Membr Biol 89: 9–22CrossRefGoogle Scholar
  78. Spray DC, Harris AL, Bennett MVL (1981) Equilibrium properties of a voltage-dependent junctional conductance. J Gen Physiol 77: 77–93PubMedCrossRefGoogle Scholar
  79. Stoeckel H, Takeda K (1989a) Calcium-activated, voltage-dependent, nonselective cation currents in endosperm plasma membrane from higher plants. Proc R Soc Lond B, in pressGoogle Scholar
  80. Stoeckel H, Takeda K (1989b) Voltage-activated, delayed rectifier K+ current from pulvinar protoplasts of Mimosa pudica. Pflugers Arch, in pressGoogle Scholar
  81. Strickholm A (1961) Impedance of a small electrically isolated area of the muscle cell surface. J Gen Physiol 44: 1073–1088PubMedCrossRefGoogle Scholar
  82. Takeda K, Kurkdjian A, Kado RT (1985) Ionic channels, ion transport and plant cell membranes: potential applications of the patch-clamp technique. Protoplasma 127: 147–162CrossRefGoogle Scholar
  83. Takeuchi A, Takeuchi N (1959) Active phase of frog’s end-plate potential. J Neurophysiol 22: 395–411PubMedGoogle Scholar
  84. Tazawa M (1964) Studies on Nitella having artificial sap. I. Replacement of the cell sap with artificial solutions. Plant Cell Physiol 5: 33–43Google Scholar
  85. Tazawa M, Shimmen T, Mimura T (1987) Membrane control in the Characeae. Annu Rev Plant Physiol 38: 95–117CrossRefGoogle Scholar
  86. Umrath K (1937) Der Errungsvorgang bei hoheren Pflanzen. Ergeb Biol 14: 1–142Google Scholar
  87. Wada Y, Ohsumi Y, Tanifuji M, Kasai M, Anraku Y (1987) Vacuolar ion channel of the yeast, Saccharomyces cerevisiae. J Biol Chem 262: 17260–17263PubMedGoogle Scholar

Copyright information

© Kluwer Academic Publishers 1989

Authors and Affiliations

  • R. Hedrich
    • 1
  • H. Stoeckel
    • 2
  • K. Takeda
    • 3
  1. 1.Pflanzenphysiologisches InstitutUniversität GöttingenGöttingenGermany
  2. 2.Laboratoire de Biologie Cellulaire Végétale-CNRS UA1182Université Louis Pasteur de StrasbourgStrasbourgFrance
  3. 3.Laboratoire de Pharmacologic Cellulaire et Moléculaire-CNRS UA600Université Louis Pasteur de StrasbourgIllkirchFrance

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