Skip to main content
SpringerLink
Log in

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

  • Chapter
The Plant Plasma Membrane

  • 214 Accesses

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.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 84.99
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 109.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

Abbreviations

FV:

fast vacuole

SV:

slow vacuole

TEA:

triethanolamine

References

  • Assmann SM, Simoncini L, Schroeder JI (1985) Blue light activates electrogenic ion pumping in guard cell protoplasts of Vicia faba. Nature 318: 285–287

    Article  CAS  Google Scholar 

  • Beilby MJ (1982) CI- channels in Chara. Philos Trans R Soc Lond B 299: 435–455

    Article  CAS  Google Scholar 

  • Bertl A, Gradmann D (1987) Current-voltage relationships of potassium channels in the plasmalemma of Acetabularia. J Membr Biol 99: 41–49

    Article  CAS  Google Scholar 

  • Bertl A, Klieber HG, Gradmann D (1988) Slow kinetics of a potassium channel in Acetabularia. J Membr Biol 102: 141–152

    Article  CAS  Google Scholar 

  • 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: 2737–2741

    Article  PubMed  CAS  Google Scholar 

  • 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: 954–959

    Article  PubMed  CAS  Google Scholar 

  • Bush DS, Hedrich R, Schroeder JI, Jones RL (1988) Channel-mediated K+ flux in barley aleurone protoplasts. Planta 176: 368–377

    Article  CAS  Google Scholar 

  • Catterall WA (1988) Structure and function of voltage-sensitive ion channels. Science 242: 50–61

    Article  PubMed  CAS  Google Scholar 

  • Cole KS, Curtis HJ (1938) Electric impedance of Nitella during activity. J Gen Physiol 22: 37–64

    Article  PubMed  CAS  Google Scholar 

  • Coleman HA (1986) CI- currents in Chara — a patch clamp study. J Membr Biol 93: 55–61

    Article  CAS  Google Scholar 

  • 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: 227–236

    Article  CAS  Google Scholar 

  • 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: 263–268

    Article  CAS  Google Scholar 

  • 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 41–66

    Chapter  Google Scholar 

  • Ettlinger C, Lehle L (1988) Auxin induces rapid changes in phosphatidylinositol metabolites. Nature 331: 176–178

    Article  PubMed  CAS  Google Scholar 

  • Falke LC, Edwards KL, Pickard BG, Misler S (1988) A stretch-activated anion channel in tobacco protoplasts. FEBS Lett 237: 141–144

    Article  PubMed  CAS  Google Scholar 

  • Findlay GP (1961) Voltage-clamp experiments with Nitella. Nature 191: 812–814

    Article  Google Scholar 

  • 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 53–92

    Google Scholar 

  • 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 26–51

    Google Scholar 

  • Gilroy S, Blowers DP, Trewavas A J (1987) Calcium: a regulation system emerges in plant cells. Development 100: 181–184

    CAS  Google Scholar 

  • 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: 85–100

    Article  PubMed  CAS  Google Scholar 

  • Hedrich R, Kurkdjian A (1988) Characterization of an anion-permeable channel from sugar beet vacuoles: effect of inhibitors. EMBO J 7: 3661–3666

    PubMed  CAS  Google Scholar 

  • Hedrich R, Neher E (1987) Cytoplasmic calcium regulates voltage-dependent ion channels in plant vacuoles. Nature 329: 833–836

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Hedrich R, Flttgge UI, Fernandez JM (1986) Patch-clamp studies of ion transport in isolated plant vacuoles. FEBS Lett 204: 228–232

    Article  CAS  Google Scholar 

  • Hedrich R, Schroeder JI, Fernandez JM (1987) Patch-clamp studies on higher plant cells: a perspective. Trends Biochem Sci 12: 49–52

    Article  CAS  Google Scholar 

  • 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: 7–13

    CAS  Google Scholar 

  • Hille B (1984) Ionic channels of excitable membranes. Sinauer, Sunderland

    Google Scholar 

  • Hodgkin AL (1964) The conduction of the nervous impulse. Ch C Thomas, Springfield, MA

    Google Scholar 

  • Homble F, Ferrier JM, Dainty J (1987) Voltage-dependent K+ -channels in protoplasmic droplets of Chara corallina. Plant Physiol 83: 53–57

    Article  PubMed  CAS  Google Scholar 

  • Hornberg C, Weiler EW (1984) High-affinity binding sites for abscisic acid on the plasmalemma of Vicia faba guard cells. Nature 370: 321–324

    Article  Google Scholar 

  • Hosoi S, Lino M, Shimazaki K (1988) Outward-rectifying K+ channels in stomatal guard cell protoplasts. Plant Cell Physiol 29: 907–911

    CAS  Google Scholar 

  • Iijima T, Hagiwara S (1987) Voltage dependent K+ channels in protoplasts of trap-lobe cells of Dionea muscipula. J Membr Biol 100: 73–81

    Article  PubMed  CAS  Google Scholar 

  • Jaffe LF, Nuccitelli R (1977) Electrical controls of development. Annu Rev Biophys Bioeng 6: 445–476

    Article  PubMed  CAS  Google Scholar 

  • Jones RL (1973) Gibberellic acid and ion release from barley aleurone tissue. Plant Physiol 52: 303–308

    Article  PubMed  CAS  Google Scholar 

  • Kado RT, Kurkdjian A, Takeda K (1986) Transport mechanisms in plant cell membranes: an application for the patch clamp technique. Physiol Veg 24: 227–244

    CAS  Google Scholar 

  • Kolb HA, Kohler K, Martinoia E (1987) Single potassium channels in membranes of isolated mesophyll barley vacuoles. J Membr Biol 95: 163–169

    Article  CAS  Google Scholar 

  • Krawczyk S (1978) Ionic channel formation in a living cell membrane. Nature 273: 56–57

    Article  PubMed  CAS  Google Scholar 

  • 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: 31–42

    Article  Google Scholar 

  • Lühring HE (1986) Recording of single K+ channels in the membrane of cytoplasmic drop of Chara australis. Protoplasma 133: 19–28

    Article  Google Scholar 

  • 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: 43–58

    Article  Google Scholar 

  • Lüttge U, Pitman MG (eds) (1976) Transport in plants. Vols. I, II & III. Springer, Berlin Heidelberg New York

    Google Scholar 

  • Michaelis L (1925) Contribution to the theory of permeability of membranes for electrolytes. J Gen Physiol 8: 33–59

    Article  PubMed  CAS  Google Scholar 

  • Moran N, Ehrenstein G, Iwasa K, Bare C, Mischke C (1984) Ion channels in plasmalemma of wheat protoplast. Science 226: 835–838

    Article  PubMed  CAS  Google Scholar 

  • 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: 643–648

    Article  PubMed  CAS  Google Scholar 

  • Muller U, Malchow D, Hartung K (1986) Single ion channels in the slime mold Dictyostelium discoideum. Biochim Biophys Acta 857: 287–290

    Article  PubMed  CAS  Google Scholar 

  • Mullins LJ (1962) Efflux of chloride ions during the action potential of Nitella. Nature 196: 986–987

    Article  PubMed  CAS  Google Scholar 

  • Nagata T, Takebe I (1970) Cell wall regeneration and cell division in isolated tobacco mesophyll protoplasts. Planta 92: 301–308

    Article  Google Scholar 

  • Neher E, Sakmann B (1976) Single-channel currents recorded from membrane of denervated frog muscle fibres. Nature 260: 799–802

    Article  PubMed  CAS  Google Scholar 

  • Neher E, Stevens CF (1977) Conductance fluctuations and ionic pores in membranes. Annu Rev Biophys Bioeng 6: 345–381

    Article  PubMed  CAS  Google Scholar 

  • 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: 219–228

    Article  PubMed  CAS  Google Scholar 

  • Outlaw WH (1983) Current concepts on the role of potassium in stomatal movements. Physiol Plant 59: 302–311

    Article  CAS  Google Scholar 

  • Pilet PE (ed) (1985) The physiological properties of plant protoplasts. Springer, Berlin Heidelberg New York Tokyo

    Google Scholar 

  • Poovaiah BW, Reddy ASN (1987) Calcium messenger systems in plants. CRC Crit Rev Plant Sci 6: 47–103

    Article  PubMed  CAS  Google Scholar 

  • Rae JL, Levis RA (1984) Patch voltage clamp of lens epithelial cells: theory and practise. Mol Physiol 6: 115–162

    CAS  Google Scholar 

  • Ranjeva R, Boudet AM (1987) Phosphorylation of proteins in plants: regulatory effects and potential in stimulus/response coupling. Annu Rev Plant Physiol 38: 73–93

    Article  CAS  Google Scholar 

  • 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 383–441

    Google Scholar 

  • Raschke K, Hedrich R (1989) Patch-clamp measurements on isolated guard cell protoplasts and vacuoles. Methods Enzymol 174, in press

    Google Scholar 

  • 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: 304–309

    Article  PubMed  CAS  Google Scholar 

  • Sakmann B, Neher E (eds) (1983) Single channel recording. Plenum, New York

    Google Scholar 

  • 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: 417–449

    Article  Google Scholar 

  • Satter RL, Moran N (1988) Ionic channels in plant cell membranes. Physiol Plant 72: 816–820

    Article  CAS  Google Scholar 

  • Satter RL, Geballe GT, Applewhite PB, Galston AW (1974) Potassium flux of leaf movements in Samanea saman. I. Rhythmic movement. J Gen Physiol 64: 413–430

    Article  PubMed  CAS  Google Scholar 

  • 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: 205–213

    CAS  Google Scholar 

  • Schauf CL, Wilson KJ (1987a) Properties of single K+ and CI- channels in Asclepias tuberose protoplasts. Plant Physiol 85: 413–441

    Article  PubMed  CAS  Google Scholar 

  • Schauf CL, Wilson KJ (1987b) Effect of abscisic acid on K+ channels in Vicia faba guard cell protoplasts. Biochem Biophys Res Commun 145: 284–290

    Article  PubMed  CAS  Google Scholar 

  • Schroeder JI (1988) K+ transport properties of K+ channels in the plasma membrane of Vicia faba guard cells. J Gen Physiol 92: 667–684

    Article  PubMed  CAS  Google Scholar 

  • Schroeder JI, Hedrich R (1989) A model for the concerted action of ion transport mechanisms across guard cell membranes. Trends Biochem Sci 14: 187–192

    Article  PubMed  CAS  Google Scholar 

  • Schroeder JI, Hedrich R, Fernandez JM (1984) Potassium-selective single channels in guard cell protoplasts. Nature 312: 361–362

    Article  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Schumaker K, Sze H (1987) Inositol 1,4,5-triphosphate releases Ca2+ from vacuolar membrane vesicles of oat roots. J Biol Chem 262: 3944–3946

    PubMed  CAS  Google Scholar 

  • 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: 436–440

    Article  PubMed  CAS  Google Scholar 

  • Serrano R (1988) Structure and function of proton translocating ATPase in plasma membranes of plants and fungi. Biochim Biophys Acta 947: 1–28

    PubMed  CAS  Google Scholar 

  • 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: 255–264

    Article  CAS  Google Scholar 

  • Sibaoka T (1966) Action potentials in plant organs. Symp Soc Exp Biol 20: 49–74

    PubMed  CAS  Google Scholar 

  • Simons PJ (1981) The role of electricity in plant movements. New Phytol 87: 11–37

    Article  CAS  Google Scholar 

  • Smith TG, Lecar H, Redman SJ, Gage PW (eds) (1985) Voltage and patch clamping with microelectrodes. Williams & Wilkins, Baltimore

    Google Scholar 

  • Sokolik AI, Yurin VM (1986) Potassium channels in plasmalemma of Nitella cells at rest. J Membr Biol 89: 9–22

    Article  CAS  Google Scholar 

  • Spray DC, Harris AL, Bennett MVL (1981) Equilibrium properties of a voltage-dependent junctional conductance. J Gen Physiol 77: 77–93

    Article  PubMed  CAS  Google Scholar 

  • 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 press

    Google Scholar 

  • Stoeckel H, Takeda K (1989b) Voltage-activated, delayed rectifier K+ current from pulvinar protoplasts of Mimosa pudica. Pflugers Arch, in press

    Google Scholar 

  • Strickholm A (1961) Impedance of a small electrically isolated area of the muscle cell surface. J Gen Physiol 44: 1073–1088

    Article  PubMed  CAS  Google Scholar 

  • Takeda K, Kurkdjian A, Kado RT (1985) Ionic channels, ion transport and plant cell membranes: potential applications of the patch-clamp technique. Protoplasma 127: 147–162

    Article  CAS  Google Scholar 

  • Takeuchi A, Takeuchi N (1959) Active phase of frog’s end-plate potential. J Neurophysiol 22: 395–411

    PubMed  CAS  Google Scholar 

  • Tazawa M (1964) Studies on Nitella having artificial sap. I. Replacement of the cell sap with artificial solutions. Plant Cell Physiol 5: 33–43

    CAS  Google Scholar 

  • Tazawa M, Shimmen T, Mimura T (1987) Membrane control in the Characeae. Annu Rev Plant Physiol 38: 95–117

    Article  CAS  Google Scholar 

  • Umrath K (1937) Der Errungsvorgang bei hoheren Pflanzen. Ergeb Biol 14: 1–142

    Google Scholar 

  • Wada Y, Ohsumi Y, Tanifuji M, Kasai M, Anraku Y (1987) Vacuolar ion channel of the yeast, Saccharomyces cerevisiae. J Biol Chem 262: 17260–17263

    PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Pflanzenphysiologisches Institut, Universität Göttingen, D-3400, Göttingen, Germany

    R. Hedrich

  2. Laboratoire de Biologie Cellulaire Végétale-CNRS UA1182, Université Louis Pasteur de Strasbourg, F-67083, Strasbourg, France

    H. Stoeckel

  3. Laboratoire de Pharmacologic Cellulaire et Moléculaire-CNRS UA600, Université Louis Pasteur de Strasbourg, BP. 24, F-67401, Illkirch, France

    K. Takeda

Authors
  1. R. Hedrich
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. H. Stoeckel
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. K. Takeda
    View author publications

    You can also search for this author in PubMed Google Scholar

Editor information

Editors and Affiliations

  1. Department of Plant Biochemistry, University of Lund, Box 7007, S-220 07, Lund, Sweden

    Christer Larsson

  2. Department of Plant Physiology, University of Lund, Box 7007, S-220 07, Lund, Sweden

    Ian M. Møller

Rights and permissions

Reprints and permissions

Copyright information

© 1989 Kluwer Academic Publishers

About this chapter

Cite this chapter

Hedrich, R., Stoeckel, H., Takeda, K. (1989). Electrophysiology of the Plasma Membrane of Higher Plant Cells: New Insights from Patch-Clamp Studies. In: Larsson, C., Møller, I.M. (eds) The Plant Plasma Membrane. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-74522-5_8

Download citation

  • DOI: https://doi.org/10.1007/978-3-642-74522-5_8

  • Publisher Name: Springer, Berlin, Heidelberg

  • Print ISBN: 978-3-642-74524-9

  • Online ISBN: 978-3-642-74522-5

  • eBook Packages: Springer Book Archive

Publish with us

Policies and ethics

Search

Navigation