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Comparison of K+-channel activation and deactivation in guard cells from a dicotyledon (Vicia faba L.) and a graminaceous monocotyledon (Zea mays)

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Abstract

We describe and compare inward and outward whole-cell K+ currents across the plasma membrane surrounding guard-cell protoplasts from the dicotyledon, Vicia faba, and the graminaceous monocotyledon, Zea mays. Macrosopic whole-cell current is considered in terms of microscopic single-channel activity, which involves discrete steps between conducting (open) and nonconducting (closed) states of the channel protein. Kinetic equations are used to model the number of open and closed states for channels conducting K+ influx (K(in)) and K+ efflux (K(out)) in the two species, and to calculate the rate at which open-closed transitions occur. The opening and closure of K(in) channels in both Vicia and Zea follow single-exponential timecourses, indicating that K(in)-channel proteins in each species simply fluctuate between one open and one closed state. In both species, opening of K(in) channels is voltage-independent, but closure of K(in) channels is faster at more positive membrane potentials. In response to identical voltage stimuli, K(in) channels in Zea open and close approximately three times as fast as in Vicia. In contrast to K(in), K(out) channels in Zea open and close more slowly than in Vicia. The closure of K(out) channels follows a single-exponential timecourse in each species, indicating one open state. The kinetics of K(out)-channel opening are more complicated and indicate the presence of at least two (Vicia) or three (Zea) closed states.

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Abbreviations

C, O:

closed, open state of channel

EK :

equilibrium potential

Iinf :

current at infinite time (t)

K(in),K(out):

K+ influx, efflux

P:

number of independent membranebound particles that control opening of the channel

τIA, τoa :

time constant for activation of inward and outward current

τID,τod :

time constant for deactivation of inward and outward current

Vm :

membrane potential

References

  • Armstrong, C.M. (1969) Inactivation of the potassium conductance and related phenomena caused by quaternary ammonium ion injected in squid axons. J. Gen. Physiol. 54, 553–575

    Article  PubMed  CAS  Google Scholar 

  • Armstrong, C.M. (1981) Sodium channels and gating currents. Physiol. Rev. 61, 644–683

    PubMed  CAS  Google Scholar 

  • Assmann, S.M., Grantz, D.A. (1990) Stomatal response to humidity in sugarcane and soybean: effect of vapour pressure difference on the kinetics of the blue light response. Plant Cell Environ. 13, 163–169

    Article  Google Scholar 

  • Barry, P.W., Lynch, J.W. (1991) Liquid junction potentials and small cell effects in patch-clamp analysis. J. Membr. Biol. 121, 101–117

    Article  PubMed  CAS  Google Scholar 

  • Blatt, M.R. (1987) Electrical characteristics of stomatal guard cells: The ionic basis of the membrane potential and the consequences of potassium chloride leakage from microelectrodes. Planta 170, 272–287

    Article  CAS  Google Scholar 

  • Blatt, M.R. (1988) Potassium-dependent, bipolar gating of K+ channel in guard cells. J. Membr. Biol. 102, 235–246

    Article  Google Scholar 

  • Blatt, M.R. (1991) Ion channel gating in plants: physiological implications and integration for stomatal function. J. Membr. Biol. 124, 95–112

    Article  PubMed  CAS  Google Scholar 

  • Blatt, M.R., Thiel, G., Trentham, D.R. (1990) Reversible inactivation of K+ channels of Vicia stomatal guard cells following the photolysis of caged inositol 1,4,5-trisphosphate. Nature 346, 766–769

    Article  PubMed  CAS  Google Scholar 

  • Colquhoun, D., Hawkes, A.G. (1981) On the stochastic properties of single ion channels. Proc. R. Soc. London Ser. B. 211, 205–235

    Article  CAS  Google Scholar 

  • Colquhoun, D., Hawkes, A.G. (1983) The principles of stochastic interpretation of ion-channel mechanisms. In: Single-channel recording, pp. 135–175, Sakmann, B., Neher, E., eds. Plenum Press, New York

    Google Scholar 

  • Fairley, K.A., Laver, D.R., Walker, N.A. (1991) Single-channel and whole-cell currents across the corn plasmalemma. J. Membr. Biol. 108, 153–164

    Google Scholar 

  • Fairley-Grenot, K.A., Assmann, S.M. (1991) Evidence for Gprotein regulation of inward K+ current in guard cells of fava bean. Plant Cell 3, 1037–1044

    Article  PubMed  CAS  Google Scholar 

  • Fairley-Grenot, K.A., Assmann, S.M. (1992a) Whole-cell K+ current across the plasma membrane of guard cells from a grass: Zea mays. Planta 186, 282–293

    Article  CAS  Google Scholar 

  • Fairley-Grenot, K.A., Assmann, S.M. (1992b) Permeation of Ca2+ through K+ channels in the plasma membrane of Vicia faba guard cells. J. Membr. Biol. 128, 103–113

    CAS  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

    PubMed  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Gilroy, S., Read, N.D., Trewavas, A.J. (1990) Elevation of cytoplasmic calcium by caged calcium or caged inositol trisphosphate initiates stomatal closure. Nature 346, 769–771

    Article  PubMed  CAS  Google Scholar 

  • Grantz, D.A., Zeiger, E. (1986) Stomatal responses to light and leaf-air water vapor pressure difference show similar kinetics in sugarcane and soybean. Plant Physiol. 81, 865–858

    PubMed  CAS  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. Pflügers Arch. 391, 85–100

    Article  PubMed  CAS  Google Scholar 

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

    Google Scholar 

  • Hodgkin, A.L., Huxley, A.F. (1952) A quantitative description of membrane current and its application to conduction and excitation in nerve. J. Physiol. (London) 144, 505–524

    Google Scholar 

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

    CAS  Google Scholar 

  • Ketchum, K.A., Shrier, A., Poole, R.J. (1989) Characterization of potassium-dependent currents in protoplasts of corn suspension cells. Plant Physiol. 89, 1184–1192

    Article  PubMed  Google Scholar 

  • Kruse, T., Tallman, G., Zeiger, E. (1989) Isolation of guard cell protoplasts from mechanically prepared epidermes of Vicia faba. leaves. Plant Physiol. 90, 1382–1386

    PubMed  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 

  • Schroeder, J.I. (1988) K+ transport properties of K+ channels in the plasma membrane of Vicia faba guard cells. J. Gen. Physiol. 92, 667–683

    Article  PubMed  CAS  Google Scholar 

  • Schroeder, J.I. (1989) Quantitative analysis of outward rectifying K+ channel currents in guard cell protoplasts from Vicia faba. J. Membr. Biol. 107, 229–235

    Article  PubMed  CAS  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

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Thiel, G., Blatt, M.R. (1991) The mechanism of ion permeation through K+ channels of stomatal guard cells: voltage-dependent block by Na+. J. Plant Physiol. 138, 326–332

    CAS  Google Scholar 

  • Thiel, G., MacRobbie, E.A.C., Blatt, M.R. (1992) Membrane transport in guard cells: the importance of voltage control. J. Membr. Biol. 126, 1–18

    PubMed  CAS  Google Scholar 

  • Van Duijn, B. Hodgkin-Huxley analysis of whole-cell outwardly rectifying K+ current in protoplasts from tobacco cell suspension culture. J. Membr. Biol., in press

  • Vandenberg, C.A., Bezanilla, F. (1991) A sodium channel gating model based on single channel, macroscopic ionic, and gating currents in the squid giant axon. Biophys. J. 60, 1511–1533

    PubMed  CAS  Google Scholar 

  • Yellen, G. (1984) Ionic permeation and blockade of Ca2+-activated K+ channels of bovine chromaffin cells. J. Gen. Physiol. 84, 157–186

    Article  PubMed  CAS  Google Scholar 

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Author notes

  1. K. A. Fairley-Grenot

    Present address: School of Biological Sciences, A12, The University of Sydney, 2006, Australia

Authors and Affiliations

  1. Harvard Biological Laboratories, 16 Divinity Avenue, 02138, Cambridge, MA, USA

    K. A. Fairley-Grenot & S. M. Assmann

Authors
  1. K. A. Fairley-Grenot
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  2. S. M. Assmann
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Additional information

The authors thank Professor N.A. Walker and Dr. D.R. Laver for the use of laboratory equipment, for helpful discussion and for provision of the program, GETHH. Thanks also to Dr. R.J. Ritchie for assistance with statistical analyses and to Ms. Janet Sherwood for maintenance of Vicia and Zea plants. This work was supported by grants from the National Science Foundation (DCB-89-04041) and the McKnight Foundation (S.M.A) and by a Charles Gilbert Heydon Travelling Fellowship (K.F-G).

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Fairley-Grenot, K.A., Assmann, S.M. 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 (1993). https://doi.org/10.1007/BF00194439

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