Plant Physiol. (1998) 116: 145-153

Regulation of K⁺ Channels in Maize Roots by Water Stress and Abscisic Acid¹

Stephen K. Roberts^{*, 2}

Department of Plant Sciences, University of Cambridge, Downing Street, Cambridge, CB2 3EA, United Kingdom

	ABSTRACT

Top Abstract Introduction Methods Results Discussion References

Root cortical and stelar protoplasts were isolated from maize (Zea mays L.) plants that were either well watered or water stressed, and the patch-clamp technique was used to investigate their plasma membrane K⁺ channel activity. In the root cortex water stress did not significantly affect inward- or outward-rectifying K⁺ conductances relative to those observed in well-watered plants. In contrast, water stress significantly reduced the magnitude of the outward-rectifying K⁺ current in the root stele but had little effect on the inward-rectifying K⁺ current. Pretreating well-watered plants with abscisic acid also significantly affected K⁺ currents in a way that was consistent with abscisic acid mediating, at least in part, the response of roots to water stress. It is proposed that the K⁺ channels underlying the K⁺ currents in the root stelar cells represent pathways that allow K⁺ exchange between the root symplasm and xylem apoplast. It is suggested that the regulation of K⁺ channel activity in the root in response to water stress could be part of an important adaptation of the plant to survive drying soils.

	INTRODUCTION

Top Abstract Introduction Methods Results Discussion References

Water availability is one of the most important determinants of plant growth globally (Alscher and Cummings, 1990). In particular, it is the single most important factor limiting maize (Zea mays L.) production in most areas of the world (Edmeades et al., 1989). Higher plants exhibit a range of biochemical, physiological, and morphological adaptations in response to water stress, including accumulation of ABA (Davies et al., 1986). ABA is known to influence a variety of processes characteristic of water stress (e.g. stomatal closure [MacRobbie, 1992] and solute accumulation in the roots [Sharp and Davies, 1979]), and thus it is thought to act as a signal for the initiation of regulatory processes involved in the adaptation of plants to drying soils. A number of studies have shown that ABA regulates ion transport across the root with no effect on ion uptake. In most studies ion release from the stelar symplasm into the xylem apoplast was inhibited by ABA (Cram and Pitman, 1972; Schaefer et al., 1975; Behl and Jeschke, 1981). However, in other studies ABA stimulated ion transport from the root stelar symplasm (Collins and Kerrigan, 1974). This contradiction has been explained by Pitman et al. (1974), who showed that ABA inhibits ion transport in "low-salt" roots (i.e. plants grown in nutrient-free solutions), whereas in "high-salt" roots (i.e. plants grown in high-nutrient solutions) ABA promoted ion transport.

The molecular mechanisms involved in the regulation of ion transport in roots are unknown. Most ion transport in higher plant roots is catalyzed by transport proteins; plasma membrane ion channels are central components of this ion-transport pathway. Root epidermal and cortical cells mediate the net uptake of ions into the root symplasm. A range of plasma membrane ion channels has been identified in these cells, which are likely to catalyze the uptake of K⁺ (Findlay et al., 1994; Gassmann and Schroeder, 1994; White and Lemtiri-Chlieh, 1995; Maathuis and Sanders, 1995; Roberts and Tester, 1995), Cl (Skerret and Tyerman, 1993), and Ca²⁺ (White, 1993; Piñeros and Tester, 1995). In contrast, the stelar cells of the root mediate the net loss of ions from the root symplasm into the xylem vessels for transport to the shoot. Plasma membrane ion channels have been identified in these cells, which probably catalyze the release of ions into the stelar apoplast (Wegner and Raschke, 1994; Roberts and Tester, 1995).

In previous experiments (Roberts and Tester, 1995) the patch-clamp technique was applied to protoplasts from the cortex and stele of maize roots, and K⁺-selective channels in these different cell types were characterized. A clear pattern emerged of the types of plasma membrane K⁺ channels observed in these different cell types, the activities of which paralleled the anticipated transport of K⁺ across the root (Roberts and Tester, 1995). In most cortical protoplasts a K⁺-selective inward channel was observed that would allow K⁺ uptake from the soil solution and would thus likely represent the pathway for low-affinity K⁺ uptake found in intact maize roots (Kochian et al., 1985). In maize root stelar cells a K⁺-selective outward channel was observed in most of these cells, which probably mediates the passive release of K⁺ from the root symplasm into the stelar apoplast (for subsequent transport to the shoot via the xylem vessels).

In the present study the patch-clamp technique was used to investigate: (a) previously uncharacterized TD outward and inward plasma membrane currents in maize root cortical and stelar cells, respectively, and (b) the effects of water stress and exogenous ABA on the plasma membrane currents in maize roots. A novel regulation of K⁺ channel activity by ABA is described that could be an important response of roots, enabling the plant to survive in drying soils.

	MATERIALS AND METHODS

Top Abstract Introduction Methods Results Discussion References

Plant Growth

2

1

Protoplast Isolation

Electrophysiology

The generation of voltage test pulses, recording of whole-cell currents, and storage of data were controlled by the software package pClamp6.0 (Axon Instruments) and a 486 personal computer. Analysis of data was done by pClamp software and FigP (version 2.2, Biosoft, Cambridge, UK). Outside-out patches were obtained from the whole-cell configuration by pulling away the pipette from the protoplast. Single-channel currents were measured and analyzed using the same equipment and software that was used for whole-cell experiments. Data were digitized at 1 kHz and filtered at 200 or 300 Hz for analysis. Liquid-junction potentials were corrected for in all experiments as described by Neher (1992). Tip potentials were measured at the end of an experiment by measuring the potential change when the pipette tip was broken. Only experiments in which the tip potential was less than 2 mV were used. Ion equilibrium potentials were calculated after correction for ionic activities (as calculated by GEOCHEM-PC; Parker et al., 1994). Variations in data are presented as the se.

Solutions

1

1

Analysis of K⁺ Channel Activity in Maize Roots

2

	RESULTS

Top Abstract Introduction Methods Results Discussion References

In a previous report TD K⁺-selective inward and outward currents were characterized in the plasma membrane of maize root cortical and stelar cells, respectively (Roberts and Tester, 1995). In that study small TD outward currents in cortical cells and TD inward currents in stelar cells were also observed but were not characterized. In the present study these previously uncharacterized TD currents are investigated further.

Outward Current in Maize Root Cortical Protoplasts

View larger version (30K): [in this window] [in a new window]   Figure 1. A, Current-voltage relationship of the TD () component of the currents shown in the inset. Inset, Plasma membrane currents resulting from voltage pulses ranging from +65 to 95 mV (in 20-mV steps at intervals of 8 s). Holding potential was 75 mV. B, Voltage dependence of the time constants of activation of whole-cell outward currents from maize root cortical protoplasts (error bars denote the se; n = 3). Inset, Examples of least-squares fits of Equation 1 to the activation of whole-cell outward currents from root cortical protoplasts from well-watered plants. Holding potential was 75 mV. C, Recordings of outward K+ channel activity in an outside-out patch from a cortical protoplast. Standard bath solution was used. The holding voltage for each recording is shown on the right. Upward deflections represent channel openings. D, Single-channel current as a function of voltage. Data shown are from two patches in standard bath solution (EK = 48 mV) with different symbols for each cell. The unitary conductance (G) and reversal potential (Erev) were determined by fitting a linear regression to the data; G = 30 pS, Erev = 38 mV.

The outward current in cortical protoplasts activated with a sigmoidal time course and could be fitted by a Hogkin-Huxley-type model (Hodgkin and Huxley, 1952), according to the equation:

(1)

where p is the number of independent membrane-bound gating particles that control the opening of the channel, I_L is a constant leak, and I is the steady-state current after activation. Currents were best fitted (using the least-squares fit method) when p was set to 2 (Fig. 1B, inset). The time constant () decreased slightly as voltage increased from +5 to +65 mV (Fig. 1B). Equation 1 also best fitted the activation kinetics of the outward current in maize root stelar protoplasts with a similar relationship between voltage and the activation time constant (Roberts and Tester, 1995).

Single-channel activity such as that shown in Figure 1C was observed in outside-out patches from cortical cell protoplasts. These single-channel currents also reversed approximately 10 mV positive of E_K, consistent with this channel activity underlying the macroscopic outward currents in cortical protoplasts (although ion channel activity other than that shown in Fig. 1C may also contribute to the macroscopic TD outward current). This channel had a unitary conductance of 30 pS (15:123 mm K⁺, outside:cytosol) (Fig. 1D), similar to that reported for the outward K⁺ channel in the stele of maize when recorded in similar solutions (Roberts and Tester, 1995).

Inward Current in Maize Root Stelar Protoplasts

(2)

2

View larger version (28K): [in this window] [in a new window]   Figure 2. A, Current-voltage relationship of the TD () component of the currents shown in the inset. Inset, Plasma membrane currents resulting from voltage pulses ranging from +65 to 175 mV (in 20-mV steps at intervals of 8 s). Holding potential was 75 mV. The displayed currents have had the leak current subtracted (leak conductance was 200 pS). B, Voltage dependence of the time constants of activation of the whole-cell inward current from maize root stelar protoplasts (the number of replicates is indicated in the parentheses for each point; error bars denote the se). Inset, Examples of least-squares fits of Equation 2 to the activation of whole-cell inward currents from root stelar protoplasts from water-stressed plants. Holding potential was 75 mV. C, Recordings of inward K+ channel activity in an outside-out patch from a stelar protoplast. A standard bath solution was used. The holding voltage for each recording is shown on the right. Downward deflections represent channel openings. D, Single-channel current as a function of voltage. Data are shown from three patches in standard bath solution (EK = 48 mV), with different symbols for each cell. The unitary conductance (G) and reversal potential (Erev) were determined by fitting a linear regression to the data; G = 10 pS, Erev = 53 mV.

Single-channel activity, such as that shown in Figure 2C, was observed in outside-out patches from stelar cell protoplasts. These single-channel currents reversed close to E_K, which is consistent with this channel activity underlying the macroscopic inward currents in stelar protoplasts (although ion channel activity other than that shown in Figure 2C may also contribute to the macroscopic TD inward current). The channel had a unitary conductance of 10 pS (15:123 mm K⁺, outside:cytosol) (Fig. 2D), similar to that reported for the inward K⁺ channel in the cortex of maize when recorded in similar solutions (Roberts and Tester, 1995).

Effects of Water Stress and ABA on K⁺ Channel Activity in Maize Roots

View larger version (26K): [in this window] [in a new window]   Figure 3. Mean current density of the whole-cell TD inward and outward currents in protoplasts from the cortex and stele of maize roots that were either well watered (WW), water stressed (WS), or pretreated with ABA. Open and hatched bars represent values from cortical and stelar protoplasts, respectively. Error bars denote the se. Positive values represent outward current density and negative values represent inward current density. The number of replicates is shown in parentheses for each determination of mean current density. Inset, As for the main figure except that the mean current density of whole-cell instantaneously activating outward current is shown from cortical and stelar protoplasts. Current densities were calculated at +45 and 175 mV (for outward and inward current, respectively).

ABA pretreatment of maize roots also had no significant effect on K⁺ channel activity in the cortex. Student's t tests indicated that the TD inward K⁺ current in cortical protoplasts from ABA-pretreated roots was not significantly different from that observed in well-watered (t = 0.269) and water-stressed roots (t = 0.21) (Fig. 3). Likewise, the TD outward current in cortical protoplasts was unaffected by ABA pretreatment compared with that in well-watered (t = 0.36) and water-stressed roots (t = 0.23) (Fig. 3).

More conspicuous was the effect of ABA pretreatment on K⁺ channel activity in stelar protoplasts. ABA pretreatment significantly increased the magnitude of the TD inward current in root stelar cells (Fig. 3) compared with well-watered (t = 0.033) and water-stressed (t = 0.038) plants. The magnitude of the TD outward current in the stele was also significantly reduced by ABA pretreatment compared with that observed in well-watered roots (t = 0.002), but it was not significantly different from that observed in water-stressed roots (t = 0.103).

In addition to the TD outward current, an instantaneously activating outward current was also observed in both the cortical and stelar protoplasts. Although the identity of this current is not known, it is noteworthy that this current was not significantly affected by either water stress or ABA pretreatment of roots (Fig. 3, inset). Furthermore, there was no effect of drought or ABA on the voltage dependence of current activation, so the current densities shown in Figure 3 represent effects of treatments on membrane conductance.

In addition to pretreating roots with ABA, the direct effects of ABA on the plasma membrane currents in stelar protoplasts from well-watered roots were also investigated. In 6 of 11 protoplasts addition of 20 µm external ABA irreversibly reduced the magnitude of the outward current by 47.5 ± 8% (n = 6) (Fig. 4). This effect occurred between 2 and 20 min after the addition of ABA; it was not caused by nonspecific "rundown," because outward currents were stable before addition of ABA (data not shown) and "rundown" of outward currents was not observed in untreated stelar cells. No effect of ABA was observed on the inward current in root stelar (or cortical) protoplasts (data not shown). Furthermore, addition of ABA (for up to 1 h) did not induce an inward current in stelar protoplasts, which did not exhibit the inward current before the addition of ABA (data not shown).

View larger version (11K): [in this window] [in a new window]   Figure 4. The effect of external ABA on the outward current from protoplasts from the stele of maize roots grown in well-watered conditions. A standard bath solution was used. Holding potential was 75 mV and voltage pulses ranged from +65 to 75 mV (in 20-mV steps at intervals of 30 s). A, Before addition of ABA. B, Five minutes after addition of 20 µm external ABA. C, Current-voltage relationship of the time-dependent component of outward currents from stelar protoplasts before () and after () the addition of 20 µm external ABA. Values shown are the mean currents from six independent experiments and the error bars denote the se. Currents were normalized with respect to the current at +65 mV before the addition of ABA for each independent experiment.

	DISCUSSION

Top Abstract Introduction Methods Results Discussion References

Similar inward and outward K⁺ channels exist in both the cortex and stele of maize roots with respect to their selectivity, activation kinetics, and single-channel conductance. However, although the same channel types appear to be present in both the cortex and stele of maize roots, the channels are regulated differently. This could reflect the fact that either different signal transduction pathways exist in the cortical and stelar cells or that the channels themselves are different with respect to their sensitivity to signaling compounds.

Physiological Significance of the Regulation of K⁺ Channel Activity by Water Stress and ABA

Cortex

Stele

Root stelar cells regulate the ionic composition of the transpiration stream (Clarkson, 1993). The outward K⁺ channels in these cells represent a pathway for the efflux of K⁺ from the root symplasm into the xylem apoplast (Wegner and Raschke, 1994; Roberts and Tester, 1995). The inward K⁺ channels may be involved in the reabsorption of K⁺ from the xylem apoplast (Wegner et al., 1994; Wegner and Raschke, 1994). Thus, water stress and ABA modify the permeability of the plasma membrane of root stelar cells in favor of K⁺ influx and against K⁺ efflux. However, the regulation of K⁺ channels by themselves only affects the capacity for passive transport of K⁺. K⁺ transport via ion channels will also depend on membrane potential and cytosolic and extracellular K⁺ concentrations. Thus, plasma membrane hyperpolarization (to generate an electrochemical gradient favoring K⁺ influx) is necessary for increased passive K⁺ uptake via K⁺ channels in stelar cells. ABA is reported to stimulate a transient increase in proton efflux into the xylem apoplast of onion roots (Clarkson and Hanson, 1986), which could indicate that the proton pump is stimulated by ABA. Activation of the proton pump could mediate a membrane hyperpolarization. However, to date there are no measurements of the effects of ABA on the membrane potential of root stelar cells.

Several studies have shown that ABA and water stress promote K⁺ accumulation by root stelar cells. Tracer-flux experiments have shown that ABA reduces K⁺ efflux from the stelar symplasm of maize and barley without any effect on K⁺ uptake by the root cortex (Cram and Pitman, 1972; Schaefer et al., 1975; Pitman and Wellfare, 1978). Although Collins and Kerrigan (1974) showed that ABA promotes ion release from the stele symplasm in maize roots, this contradiction has been explained by Pitman et al. (1974), who showed that ABA inhibits ion efflux in low-salt roots, whereas in high-salt roots ABA promotes ion efflux. In the present study low-salt roots were used. In addition to the flux experiments, a 2-fold increase in the vacuolar K⁺ content of root stelar cells has been reported in water-stressed maize plants relative to that in nonstressed plants (Pritchard et al., 1996). The regulation of the K⁺ channel activity reported in the present study is consistent with both reduced K⁺ transport to the shoot and increased accumulation of K⁺ in the root symplasm.

K⁺ accumulation by the root may be part of an important adaptation of the plant, allowing it to survive drying soils. An early response of plants to water stress is an inhibition of shoot growth while root growth is maintained (Sharp and Davies, 1979; Saab et al., 1990). Thus, ions transported from the root could accumulate in the apoplast of leaves, lowering the extracellular osmotic potential and decreasing the water deficit of leaf cells. Also, ABA promotes the net accumulation of solutes in roots during water stress (Sharp and Davies, 1979; Henson, 1985; Ribaut and Pilet, 1991), which is thought to maintain a water potential favoring the uptake of water and cell turgor pressure necessary for root growth (Morgan, 1984). Although organic compounds are the major constituents of osmoregulation in plant cells during water stress (Morgan, 1984), inorganic ions (e.g. K⁺) would also contribute to osmoregulation.

Mechanism of Regulation of K⁺ Channels in Maize Roots

It is not clear why only 55% of maize root stelar cells exhibiting an outward current respond to extracellular ABA. However, in similar patch-clamp experiments on guard cell protoplasts, ABA regulation of K⁺ currents was observed in only approximately 70% of cells (Lemtiri-Chlieh and MacRobbie, 1994), whereas in intact guard cells (which were impaled with a microelectrode) ABA is reported to regulate the K⁺ currents in nearly all of the cells (Blatt and Armstrong, 1993). In patch-clamp experiments the cytosol from the protoplast is replaced by the pipette solution. Thus, the absence of the ABA-mediated effect during patch-clamp experiments may be attributable to the loss of soluble cytoplasmic factors, which are an integral part of the ABA signal transduction pathway. In experiments in which protoplasts are isolated from ABA-pretreated roots, the ABA-mediated regulation of K⁺ channel activity occurs before the patch-clamp experiment. In these experiments current magnitudes remained stable during whole-cell experiments, indicating that the effects of ABA pretreatment on K⁺ channel activity in intact stelar cells were unaffected by replacement of the cytosol with pipette solution.

Maize root stelar cells from ABA-pretreated plants had increased inward K⁺ channel activity; however, no effect of ABA was observed on inward K⁺ channel activity during a patch-clamp experiment. Hence, it is not known if ABA regulates the activity of the inward K⁺ channel (but is not observed because of the loss of cytoplasmic factors during the patch-clamp experiment; see above) or if ABA regulates the expression of the K⁺ channel protein in the plasma membrane. Schaefer et al. (1975) estimated that protein turned over by 50% at 23°C in approximately 2 h in the root stele. Thus, ABA could rapidly regulate the permeability of the plasma membrane via the expression of the inward K⁺ channel. It may be possible to investigate the expression of the inward K⁺ channel in maize root stelar cells using antibodies raised against the inward K⁺ channel AKT1 (Lagarde et al., 1996).

To summarize, the present study demonstrates that K⁺ channel activity in the stele of maize roots is regulated by water availability and ABA. This regulation may at least in part represent the mechanism by which ABA and water stress modulate K⁺ transport and accumulation in the intact root (Cram and Pitman, 1972; Schaefer et al., 1975; Pitman and Wellfare, 1978; Pritchard et al., 1996). Future investigations will need to focus on determining whether ABA alone is regulating K⁺ channel activity during water stress or whether other factors are involved (e.g. cytokinins and auxins). It will also be of interest to investigate the mechanism of ABA regulation of these ion channels and to determine whether this represents a novel signaling pathway in plant cells.

	FOOTNOTES

   Received June 23, 1997; accepted September 24, 1997.

	ABBREVIATIONS

Abbreviations: pS, picosiemens. TD, time-dependent.

	ACKNOWLEDGMENTS

I thank Mr. P. Freeman for technical assistance and Mark Tester for useful discussions and comments on the manuscript.

	LITERATURE  CITED

Top Abstract Introduction Methods Results Discussion References

Alscher RG, Cummings JR (1990) Stress Responses in Plants: Adaptations and Acclimation Mechanisms. Wiley-Liss, New York

Behl R, Jeschke WD (1981) Influence of abscisic acid on unidirectional fluxes and intracellular compartmentation of K⁺ and Na⁺ in excised barley root segments. Physiol Plant 53: 95-100

Blatt MR, Armstrong F (1993) K⁺ channels of stomatal guard cells: abscisic acid-evoked control of the outward rectifier mediated by cytoplasmic pH. Planta 191: 330-341 [ISI]

Clarkson DT (1993) Roots and the delivery of solutes to the xylem. Philos Trans R Soc Lond B 341: 5-17

Clarkson DT, Hanson JB (1986) Proton fluxes and the activity of a stelar proton pump in onion roots. J Exp Bot 37: 1136-1150 [Abstract/Free Full Text]

Collins JC, Kerrigan AP (1974) The effect of kinetin and ABA on water and ion transport in isolated guard cells. New Phytol 73: 309-314

Cram WJ, Pitman MG (1972) The action of abscisic acid on ion uptake and water flow in plant roots. Aust J Biol Sci 25: 1125-1132

Davies WJ, Metcalfe J, Lodge TA, da Costa AR (1986) Plant growth substances and the regulation of growth under drought. Aust J Plant Physiol 13: 105-125

Edmeades GO, Bolanos J, Laffite HR, Rajaram S, Pfeiffer W, Fischer RA (1989) Traditional approaches to breeding for drought resistance in cereals. In FWG Baker, ed, Drought Resistance in Cereals. ICSU and CABI, Paris and Wallingford, UK, pp 27-52

Findlay GP, Tyerman SD, Garrill A, Skerret M (1994) Pump and K⁺ inward rectifiers in the plasmalemma of wheat root protoplasts. J Membr Biol 139: 103-116 [ISI][Medline]

Gassmann W, Schroeder JI (1994) Inward-rectifying K⁺ channels in root hairs of wheat. A mechanism for aluminum-sensitive low-affinity K⁺ uptake and membrane potential control. Plant Physiol 105: 1399-1408 [Abstract]

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. Pfluegers Arch 391: 85-100 [CrossRef][ISI][Medline]

Henson IE (1985) Solute accumulation and growth in plants of pearl millet (Pennisetum americanum [L] Leeke) exposed to abscisic acid or water stress. J Exp Bot 36: 1889-1899 [Abstract/Free Full Text]

Hodgkin AL, Huxley AF (1952) A quantitative description of membrane current and its implication to conduction and excitation in nerve. J Physiol 144: 505-524

Kochian LV, Xin Zhi J, Lucas WJ (1985) Potassium transport in corn roots. IV. Characterization of the linear component. Plant Physiol 79: 771-776 [Abstract/Free Full Text]

Lagarde D, Mireille B, Lepetit M, Conejero G, Gaymard F, Astruc S, Grignon C (1996) Tissue-specific expression of Arabidopsis AKT1 gene is consistent with a role in K⁺ nutrition. Plant J 9: 195-203 [CrossRef][ISI][Medline]

Lemtiri-Chlieh F, MacRobbie EAC (1994) Role of calcium in the modulation of Vicia guard cell potassium channels by abscisic acid: a patch clamp study. J Membr Biol 137: 99-107 [ISI][Medline]

Li W, Luan S, Schreiber SL, Assmann SM (1994) Evidence for protein phosphatase 1 and 2A regulation of K⁺ channels in two types of leaf cells. Plant Physiol 106: 963-970 [Abstract]

Maathuis FJM, Sanders D (1995) Contrasting roles in ion transport of two K⁺-channel types in root cells of Arabidopsis thaliana. Planta 197: 456-464 [ISI][Medline]

MacRobbie EAC (1992) Calcium and ABA-induced stomatal closure. Philos Trans R Soc Lond B 338: 5-18 [CrossRef]

Morgan JM (1984) Osmoregulation and water stress in higher plants. Annu Rev Plant Physiol 35: 299-319 [CrossRef][ISI]

Neher E (1992) Correction for liquid junction potentials in patch clamp experiments. Methods Enzymol 207: 123-131 [ISI][Medline]

Parker DR, Norvell WA, Chaney RL (1994) GEOCHEM-PC: a chemical speciation program for IBM and compatible computers. In RH Leoppert, S Goldberg, AP Schwab, eds, Chemical Equilibrium Reaction Models. American Society of Agronomy, Madison, WI, pp 253-269

Piñeros M, Tester M (1995) Characterization of a voltage-dependent Ca²⁺-selective channel from wheat roots. Planta 195: 478-488

Pitman MG, Luttge U, Lauchli A, Ball E (1974) Action of abscisic acid on ion transport as affected by root temperature and nutritional status. J Exp Bot 25: 147-155 [Abstract/Free Full Text]

Pitman MG, Wellfare D (1978) Inhibition of ion transport in excised barley roots by abscisic acid: relation to water permeability of the roots. J Exp Bot 29: 1125-1138 [Abstract/Free Full Text]

Pritchard J, Fricke W, Tomos D (1996) Turgor-regulation during extension growth and osmotic stress of maize roots: an example of single cell mapping. Plant Soil 187: 11-21

Ribaut JM, Pilet PE (1991) Effects of water stress on growth, osmotic potential and abscisic acid content of maize roots. Physiol Plant 81: 156-162 [CrossRef]

Ribaut JM, Pilet PE (1994) Water stress and indol-3yl-acetic acid content of maize roots. Planta 193: 502-507

Roberts SK, Tester M (1995) Inward and outward K⁺-selective currents in the plasma membrane of protoplasts from maize root cortex and stele. Plant J 8: 811-825 [ISI]

Roberts SK, Tester M (1997) Permeation of Ca²⁺ and monovalent cations through an outwardly rectifying channel in maize root stelar cells. J Exp Bot 48: 839-846

Saab IN, Sharp RE, Pritchard J, Voetberg G (1990) Increased endogenous abscisic acid maintains primary root growth and inhibits shoot growth of maize seedlings at low water potentials. Plant Physiol 93: 1329-1336 [Abstract/Free Full Text]

Schaefer N, Wildes RA, Pitman MG (1975) Inhibition by p-fluorophenylalanine of protein synthesis and of ion transport across the roots in barley seedlings. Aust J Plant Physiol 2: 61-73

Sharp RE, Davies WJ (1979) Solute regulation and growth by roots and shoots in water-stressed maize plants. Planta 147: 43-49 [CrossRef]

Skerret M, Tyerman SD (1993) A channel that allows inwardly directed fluxes of anions in protoplasts derived from wheat roots. Planta 102: 295-305

Wegner LH, de Boer AH, Raschke K (1994) Properties of the inward rectifier in the plasma membrane of xylem parenchyma cells from barley roots: effects of TEA⁺, Ca²⁺, Ba²⁺, and La³⁺. J Membr Biol 142: 363-379 [ISI][Medline]

Wegner LH, Raschke K (1994) Ion channels in the xylem parenchyma of barley roots. Plant Physiol 105: 799-813 [Abstract]

White PJ (1993) Characterization of a high-conductance, voltage-dependent cation channel from the plasma membrane of rye roots in planar lipid bilayers. Planta 191: 541-551

White PJ, Lemtiri-Chlieh F (1995) Potassium currents across the plasma membrane of protoplasts derived from rye roots: a patch clamp study. J Exp Bot 46: 457-511

Zhang J, Zhang X, Liang J (1995) Exudation rate and hydraulic conductivity of maize roots are enhanced by soil drying and abscisic acid treatment. New Phytol 131: 329-336

Copyright Clearance Center:   0032-0889/98/116/0145/09
 
© 1998 American Society of Plant Physiologists