Permeation of Ca2+ through K+ channels in the plasma membrane of Vicia faba guard cells

K. A. Fairley-Grenot, Sarah Mary Assmann

Research output: Contribution to journalArticle

64 Citations (Scopus)

Abstract

The whole-cell patch-clamp method has been used to measure Ca2+ influx through otherwise K+-selective channels in the plasma membrane surrounding protoplasts from guard cells of Vicia faba. These channels are activated by membrane hyperpolarization. The resulting K+ influx contributes to the increase in guard cell turgor which causes stomatal opening during the regulation of leaf-air gas exchange. We find that after opening the K+ channels by hyperpolarization, depolarization of the membrane results in tail current at voltages where there is no electrochemical force to drive K+ inward through the channels. Tail current remains when the reversal potential for permeant ions other than Ca2+ is more negative than or equal to the K+ equilibrium potential (-47 mV), indicating that the current is due to Ca2+ influx through the K+ channels prior to their closure. Decreasing internal [Ca2+] (Cai) from 200 to 2 n m or increasing the external [Ca2+] (Cao) from 1 to 10 m m increases the amplitude of tail current and shifts the observed reversal potential to more positive values. Such increases in the electrochemical force driving Ca2+ influx also decrease the amplitude of time-activated current, indicating that Ca2+ permeation is slower than K+ permeation, and so causes a partial block. Increasing Cao also (i) causes a positive shift in the voltage dependence of current, presumably by decreasing the membrane surface potential, and (ii) results in a U-shaped current-voltage relationship with peak inward current ca. -160 mV, indicating that the Ca2- block is voltage dependent and suggesting that the cation binding site is within the electric field of the membrane. K+ channels in Zea mays guard cells also appear to have a Cai-, and Cao-dependent ability to mediate Ca2+ influx. We suggest that the inwardly rectiying K+ channels are part of a regulatory mechanism for Cai. Changes in Caoand (associated) changes in Cai regulate a variety of intracellular processes and ion fluxes, including the K+ and anion fluxes associated with stomatal aperture change.

Original languageEnglish (US)
Pages (from-to)103-113
Number of pages11
JournalThe Journal of Membrane Biology
Volume128
Issue number2
DOIs
StatePublished - Jun 1 1992

Fingerprint

Vicia faba
Cell Membrane
Ions
Membranes
Protoplasts
Ion Channels
Membrane Potentials
Zea mays
Anions
Cations
Gases
Binding Sites
Air

All Science Journal Classification (ASJC) codes

  • Biophysics
  • Physiology
  • Cell Biology

Cite this

@article{867e8822382f4ff0b16505e1c82fd419,
title = "Permeation of Ca2+ through K+ channels in the plasma membrane of Vicia faba guard cells",
abstract = "The whole-cell patch-clamp method has been used to measure Ca2+ influx through otherwise K+-selective channels in the plasma membrane surrounding protoplasts from guard cells of Vicia faba. These channels are activated by membrane hyperpolarization. The resulting K+ influx contributes to the increase in guard cell turgor which causes stomatal opening during the regulation of leaf-air gas exchange. We find that after opening the K+ channels by hyperpolarization, depolarization of the membrane results in tail current at voltages where there is no electrochemical force to drive K+ inward through the channels. Tail current remains when the reversal potential for permeant ions other than Ca2+ is more negative than or equal to the K+ equilibrium potential (-47 mV), indicating that the current is due to Ca2+ influx through the K+ channels prior to their closure. Decreasing internal [Ca2+] (Cai) from 200 to 2 n m or increasing the external [Ca2+] (Cao) from 1 to 10 m m increases the amplitude of tail current and shifts the observed reversal potential to more positive values. Such increases in the electrochemical force driving Ca2+ influx also decrease the amplitude of time-activated current, indicating that Ca2+ permeation is slower than K+ permeation, and so causes a partial block. Increasing Cao also (i) causes a positive shift in the voltage dependence of current, presumably by decreasing the membrane surface potential, and (ii) results in a U-shaped current-voltage relationship with peak inward current ca. -160 mV, indicating that the Ca2- block is voltage dependent and suggesting that the cation binding site is within the electric field of the membrane. K+ channels in Zea mays guard cells also appear to have a Cai-, and Cao-dependent ability to mediate Ca2+ influx. We suggest that the inwardly rectiying K+ channels are part of a regulatory mechanism for Cai. Changes in Caoand (associated) changes in Cai regulate a variety of intracellular processes and ion fluxes, including the K+ and anion fluxes associated with stomatal aperture change.",
author = "Fairley-Grenot, {K. A.} and Assmann, {Sarah Mary}",
year = "1992",
month = "6",
day = "1",
doi = "10.1007/BF00231883",
language = "English (US)",
volume = "128",
pages = "103--113",
journal = "Journal of Membrane Biology",
issn = "0022-2631",
publisher = "Springer New York",
number = "2",

}

Permeation of Ca2+ through K+ channels in the plasma membrane of Vicia faba guard cells. / Fairley-Grenot, K. A.; Assmann, Sarah Mary.

In: The Journal of Membrane Biology, Vol. 128, No. 2, 01.06.1992, p. 103-113.

Research output: Contribution to journalArticle

TY - JOUR

T1 - Permeation of Ca2+ through K+ channels in the plasma membrane of Vicia faba guard cells

AU - Fairley-Grenot, K. A.

AU - Assmann, Sarah Mary

PY - 1992/6/1

Y1 - 1992/6/1

N2 - The whole-cell patch-clamp method has been used to measure Ca2+ influx through otherwise K+-selective channels in the plasma membrane surrounding protoplasts from guard cells of Vicia faba. These channels are activated by membrane hyperpolarization. The resulting K+ influx contributes to the increase in guard cell turgor which causes stomatal opening during the regulation of leaf-air gas exchange. We find that after opening the K+ channels by hyperpolarization, depolarization of the membrane results in tail current at voltages where there is no electrochemical force to drive K+ inward through the channels. Tail current remains when the reversal potential for permeant ions other than Ca2+ is more negative than or equal to the K+ equilibrium potential (-47 mV), indicating that the current is due to Ca2+ influx through the K+ channels prior to their closure. Decreasing internal [Ca2+] (Cai) from 200 to 2 n m or increasing the external [Ca2+] (Cao) from 1 to 10 m m increases the amplitude of tail current and shifts the observed reversal potential to more positive values. Such increases in the electrochemical force driving Ca2+ influx also decrease the amplitude of time-activated current, indicating that Ca2+ permeation is slower than K+ permeation, and so causes a partial block. Increasing Cao also (i) causes a positive shift in the voltage dependence of current, presumably by decreasing the membrane surface potential, and (ii) results in a U-shaped current-voltage relationship with peak inward current ca. -160 mV, indicating that the Ca2- block is voltage dependent and suggesting that the cation binding site is within the electric field of the membrane. K+ channels in Zea mays guard cells also appear to have a Cai-, and Cao-dependent ability to mediate Ca2+ influx. We suggest that the inwardly rectiying K+ channels are part of a regulatory mechanism for Cai. Changes in Caoand (associated) changes in Cai regulate a variety of intracellular processes and ion fluxes, including the K+ and anion fluxes associated with stomatal aperture change.

AB - The whole-cell patch-clamp method has been used to measure Ca2+ influx through otherwise K+-selective channels in the plasma membrane surrounding protoplasts from guard cells of Vicia faba. These channels are activated by membrane hyperpolarization. The resulting K+ influx contributes to the increase in guard cell turgor which causes stomatal opening during the regulation of leaf-air gas exchange. We find that after opening the K+ channels by hyperpolarization, depolarization of the membrane results in tail current at voltages where there is no electrochemical force to drive K+ inward through the channels. Tail current remains when the reversal potential for permeant ions other than Ca2+ is more negative than or equal to the K+ equilibrium potential (-47 mV), indicating that the current is due to Ca2+ influx through the K+ channels prior to their closure. Decreasing internal [Ca2+] (Cai) from 200 to 2 n m or increasing the external [Ca2+] (Cao) from 1 to 10 m m increases the amplitude of tail current and shifts the observed reversal potential to more positive values. Such increases in the electrochemical force driving Ca2+ influx also decrease the amplitude of time-activated current, indicating that Ca2+ permeation is slower than K+ permeation, and so causes a partial block. Increasing Cao also (i) causes a positive shift in the voltage dependence of current, presumably by decreasing the membrane surface potential, and (ii) results in a U-shaped current-voltage relationship with peak inward current ca. -160 mV, indicating that the Ca2- block is voltage dependent and suggesting that the cation binding site is within the electric field of the membrane. K+ channels in Zea mays guard cells also appear to have a Cai-, and Cao-dependent ability to mediate Ca2+ influx. We suggest that the inwardly rectiying K+ channels are part of a regulatory mechanism for Cai. Changes in Caoand (associated) changes in Cai regulate a variety of intracellular processes and ion fluxes, including the K+ and anion fluxes associated with stomatal aperture change.

UR - http://www.scopus.com/inward/record.url?scp=0026610965&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=0026610965&partnerID=8YFLogxK

U2 - 10.1007/BF00231883

DO - 10.1007/BF00231883

M3 - Article

C2 - 1501238

AN - SCOPUS:0026610965

VL - 128

SP - 103

EP - 113

JO - Journal of Membrane Biology

JF - Journal of Membrane Biology

SN - 0022-2631

IS - 2

ER -