The Role of Potassium Channels in the Temperature Control of Stomatal Aperture

Abstract

We used the patch-clamp technique to examine the effect of temperature (1 3-36OC) on the depolarization-activated K channels (K, channels) and on the hyperpolarization-activated channels (K, channels) in the plasma membrane of Vicia faba guard-cell protoplasts. The steady-state whole-cell conductance of both K channel types increased with temperature up to 20°C. However, whereas the whole-cell conductance of the K, channels increased further and saturated at 2 8 T , that of K, channels decreased at higher temperatures. The unitary conductance of both channel types increased with temperature like the rate of diffusion in water (temperature quotient of approximately 1.5), constituting the major contribution to the conductance increase in the whole cells. The mean number of available K, channels was not affected significantly by temperature, but the mean number of available K, channels increased significantly between 1 3 and 20°C and declined drastically above 2OOC. This decrease and the reduced steady-state voltage-dependent probability of opening of the K, channels above 28°C (because of a shift of voltage dependence by +21 mV) account for the depression of the whole-cell K, conductance at the higher temperatures. This may be a basic mechanism by which leaves of well-watered plants keep their stomata open during heat stress to promote cooling by transpiration.Diffusion of both water vapor and CO, across the leaf epidermal tissue is modulated by variation in stomatal aperture. In the intact leaf as well as in isolated epidermal strips, the aperture of the stomatal pore is controlled by diverse environmental signals, such as light, humidity, CO, concentration, and temperature (Zeiger, 1983;Mansfield et al., 1990;Assmann, 1993). When the leaf temperature increases, stomata tend to open wider in unstressed plants of a number of C, and C, species (Raschke, 1975; Sheriff, 1979; Berry and Bjorkman, 1980, and refs. therein). In leaves of a well-watered plant at high temperature, large stomatal conductance will promote transpirational cooling and thereby will keep the leaf temperature lower than that of the surrounding air (Gates, 1968;Radin et al., 1994). to heat-stress conditions (>40"C), indicated that stomatal conductance remained high even when photosynthesis was temporarily impaired. Furthermore, down-regulation of leaf temperature in extreme heat conditions will be more efficient if stomata closing signals are ignored. Indeed, at high temperature (>35"C) open stomata of Z. mays became insensitive to the increase in the leaf internal CO, concentration, a known signal for stomatal closing. In intact leaves of Xantkium pennsylvanicum that were exposed to high temperature (36"C), stomata opened even in the dark. The dark opening was then followed by a slow reclosure. The rate of stomatal closure in the dark was significantly slower at a high (36°C) than at a lower (27°C) temperature (Mansfield, 1965). Similarly, in intact leaves of Vicia faba (Kappen et al., 1994) and in isolated epidermal strips of the same species (...

Actin Filaments Modulate Both Stomatal Opening and Inward K+-Channel Activities in Guard Cells of Vicia faba L

“…6 and 7). The channels observed were the real component of IK, since their voltage dependence and reversal potential matched those of IK, (data not shown) and their single-channel conductance was similar to that reported previously for single inward K+ channels in guard cells (Schroeder and Hagiwara, 1989;Ilan et al, 1995). Channel opening increased after treatment with 20 p~ CD in five of seven membrane patches (a representative recording is shown in Fig.…”

Cold Transiently Activates Calcium-Permeable Channels in Arabidopsis Mesophyll Cells

“…The cold response of ion channels has been the subject of very few earlier studies (Ding and Pickard, 1993b;Ilan et al, 1995). In their studies on onion epidermis protoplasts, Ding and Pickard (1993b) could document the cold stimulation of a previously characterized channel (Ding and Pickard, 1993a) preactivated by membrane stretch.…”

“…B, Current-voltage relationship of ionic currents following voltage ramps (which have been substituted in A by numbers for the sake of clarity) applied during cold stimulation in solutions containing 10 mM Cs 1 (1) and 100 mM Ca 21 and 10 mM Cs 1 (2). In this experiment, the reversal voltage of (1) and (2) Working with V. faba guard cells, Ilan et al (1995) explored the temperature sensitivity of voltageactivated inward and outward K 1 rectifiers. While the whole-cell current of the inward rectifier dropped with the decrease in temperature from about 30°C to 25°C and finally 13°C, the outward rectifier was characterized by a peak at 20°C.…”

Rapid Low Temperature-Induced Stomatal Closure Occurs in Cold-Tolerant Commelina communis Leaves But Not in Cold-Sensitive Tobacco Leaves, via a Mechanism That Involves Apoplastic Calcium But Not Abscisic Acid

“…Honor et al, 1995). Low temperature may affect the enzymes and ion channels responsible for the active maintenance of guard cell osmotic potential (Ilan et al, 1995).…”