Ion Transport at the Plant Plasma Membrane


Membrane transport plays a fundamental role in virtually every aspect of homeostasis, signalling, growth and development in plants. At the plasma membrane, the boundary with the outside world, ion and solute fluxes underpin inorganic mineral nutrient uptake, they trigger rapid changes in second messengers such as cytosolic‐free Ca2+ concentrations, and they power the osmotic gradients that drive cell expansion, to name just a few roles. Our understanding of the transporters – the ion pumps that generate an H+ electrochemical driving force, H+ ion‐coupled symport and antiport systems, and ion channels – now, more than ever, builds on developments in molecular genetics, protein chemistry and crystallography to gain insights into the fine structure and mechanics of these remarkable enzymes. Even so, it is the interface with the biophysical detail of ion transport that drives scientific enquiry in the field and will continue to be essential in informing both the most fundamental research as well as efforts to apply the knowledge gained in resolving some of the dilemmas that face society today.

Keywords: membrane ion flux; membrane voltage; H+‐coupled solute transport; K+ and Ca2+ channels; inorganic mineral nutrition

Figure 1.

An overview of the proton and charge circuit of the plant plasma membrane. (a) The energy of ATP hydrolysis is used to drive H+ out of the cell, generating an electrochemical driving force of membrane voltage and [H+] gradients directed back into the cell. This driving force energizes H+‐coupled transport for uncharged (S) and charged (M+ and X) solutes. Coupled transport contributes return pathways for H+ flux and, with the exception of electroneutral ion exchange (e.g. H+–M+ exchange), charges movement back across the membrane. Ion channels for Ca2+, Cl and K+ (above) contribute to the charge circuit, but not the H+ circuit across the membrane. (b) Transport of many anions requires coupling with two H+ to overcome the opposing electrical barrier of moving a negatively charged ion into the (inside‐negative) cell. Charge balance via the H+‐ATPase in this case must result in a net decrease in cytosolic pH. (c) H+‐coupled K+ uptake in Neurospora and Arabidopsis requires export of two H+ to balance charge. The overall effect is 1:1 exchange of H+ export with K+ uptake and an overall rise in cytosolic pH. (d) H+‐coupled antiport of Na+ is electroneutral and provides a pathway for H+ return across the membrane but not for charge flux. Figure a–c redrawn with permission from John Wiley & Sons (Blatt, );Figure d: Copyright Mike Blatt.

Figure 2.

Interaction of H+‐coupled K+ symport and the H+‐ATPase in Neurospora. (a) Membrane depolarization (Vm) on adding 50 μM K+ outside (↑, addition; ↓, subtraction) is accompanied by a progressive rise in cytosolic pH (pHi) as the symport enables K+/H+ exchange that engages the H+‐ATPase. pH values and membrane voltages (in mV) as indicated. (b) Voltage trace of metabolic blockade with cyanide and salicylhydroxamic acid (SHAM). Here NaCl was added as a control for the effects of Na+ added with the cyanide. 50 μM K+ was added at the times indicated by the horizontal bars (numbered 1–7). Voltage clamp scans were run at times indicated by the carats (above). (c) Metabolic blockade of the H+‐ATPase with cyanide suppresses membrane depolarization by the H+–K+ symport through its kinetic dependence on voltage. Current–voltage curves (left) and current–difference curves (right) correspond to the K+ additions in (b) as numbered. Note that under voltage clamp current through the H+–K+ symport is clearly unaffected at any one voltage. Figure a: Copyright Mike Blatt. After Blatt and Slayman ; Figure b and c: After: J Membr Biol, 98, (1987), 169–189, Potassium‐proton symport in Neurospora: kinetic control by pH and membrane potential, Blatt, et al., Figure 5 and 6. With kind permission of Springer Science and Business Media.

Figure 3.

The KAT1 K+ channel is clustered in a small number of microdomains of 0.5–1 μm over the plasma membrane surface. Images are three‐dimensional reconstructions from confocal image stacks of tobacco epidermal (left) and guard cells (right) expressing a KAT1 fusion construct tagged with GFP. GFP fluorescence is pseudocolour coded in green. Chloroplast fluorescence is shown in red. Scale bars, 10 μm. Figure (left): Reproduced from Sutter et al.,; Copyright American Society of Plant Biologists; right: Copyright Mike Blatt.

Figure 4.

Cytosolic pH (pHi) affects the activities of the inward‐ and outward‐rectifying K+ channels in guard cells so that raising pHi suppresses the inward‐rectifier and enhances the outward‐rectifier K+ channels. (a) Experimental time course includes periods of loading with the pH‐sensitive dye BCECF (diagonal‐filled bar) and subsequent exposures to the weak acid butyrate (open bars with concentrations indicated in mM). Fluorescence at 535 nm (left‐hand scale) on excitation with either 440 nm (f440) or 490 nm (f490) light was used to determine and calibrate the fluorescence ratio R490/440 (right‐hand scale). Butyrate was used to acid‐load the cytosol and drive pHi from a resting value near 7.5 to near 6.7 in 30 mM butyrate and 8.0 on butyrate washout. Voltage clamp measurements (b) were carried out at the time points indicated (a, b, …, g). Time scale, 5 min. (b) K+ currents recorded concurrently under voltage clamp at the times cross‐referenced by letter in (a). The corresponding K+ channel components are indicated by the first set of traces, and the voltage clamp cycles are indicated above. Scale: vertical, 300 mV or 50 μA cm−2; horizontal, 1 s. Figure a and b: After Grabov and Blatt , Figure , with kind permission of Springer Science and Business Media.

Figure 5.

KAT1 K+ channels recycle to plasma membrane‐localized microdomains. Three‐dimensional reconstructions from confocal image stacks (for clarity, omitting upper and lower surfaces) of tobacco guard cells expressing KAT1 tagged with a photoactivatable GFP (paGFP) and pretreated with 20 μM ABA for 60 min. Image sets taken (a) before and (b) after photoactivation (±pa) at the start of ABA washout, and (c) after a further 7 h continuous superfusion with buffer – ABA. Images are (left to right) overlay, GFP (green) and chloroplast (red) channels. Brightfield image overlay included in (a). Nuclei (n) are labelled in (b). Chloroplasts within the stomatal pore in (c) are the consequence of cell debris accumulating during continuous perfusion. Scale bar, 20 μm. Because only those KAT1 channels photoactivated after 1 h in ABA will fluoresce, the GFP signal recovered at the plasma membrane after 7 h must have come from the channels sequestered in the endomembrane pool. Reproduced from Sutter et al. with kind permission of Cell Press.



Amtmann A and Blatt MR (2007) Regulation of ion transporters. In: Yeo AR and Flowers T (eds) Plant Solute Transport, pp. 99–132. Oxford: Blackwells.

Armengaud P, Breitling R and Amtmann A (2004) The potassium‐dependent transcriptome of Arabidopsis reveals a prominent role of jasmonic acid in nutrient signaling. Plant Physiology 136: 2556–2576.

Beilby M and Walker NA (1981) Chloride transport in Chara. I: kinetics and current‐voltage curves for a probable proton symport. Journal of Experimental Botany 32: 43–54.

Bernstein J (1902) Untersuchungen zur Thermodynamik der bioelektrischen Ströme. Pflügers Archive 92: 521–562.

Blatt MR (2004) Membrane Transport in Plants. Oxford: Blackwell. Annual Plant Reviews, Vol. 15. Roberts J, Imaseki H, McManus M, Robinson DG and Rose J.

Blatt MR, Garcia‐Mata C and Sokolovski S (2007) Membrane transport and Ca2+ oscillations in guard cells. In: Mancuso S and Shabala S (eds) Rhythms in Plants, pp. 115–134. Berlin: Springer.

Blatt MR and Gradmann D (1997) K+‐sensitive gating of the K+ outward rectifier in Vicia guard cells. The Journal of Membrane Biology 158: 241–256.

Blatt MR and Slayman CL (1987) Role of “active” potassium transport in the regulation of cytoplasmic pH by nonanimal cells. Proceedings of the National Academy of Sciences of the USA 84: 2737–2741.

Blatt MR, Rodriguez‐Navarro A and Slayman CL (1987) Potassium‐proton symport in Neurospora: kinetic control by pH and membrane potential. The Journal of Membrane Biology 98: 169–189.

Brezeale JF (1906) The relation of sodium to potassium in soil and solution cultures. Journal of the American Chemical Society 28: 1013–1025.

Clint GM and MacRobbie EAC (1987) Sodium efflux from perfused giant algal cells. Planta 171: 247–253.

Cole KS and Curtis HJ (1938) Electrical impedance of Nitella during activity. The Journal of General Physiology 22: 37–64.

DeWeer P, Gadsby DC and Rakowski RF (1988) Voltage dependence of the Na‐K pump. Annual Review of Physiology 50: 225–241.

Dreyer I, MullerRober B and Kohler B (2004) Voltage‐gated ion channels. In: Blatt MR (ed.) Membrane Transport in Plants, pp. 150–192. Oxford: Blackwell.

Felle H (1981) Steriospecificity and electrogenicity of amino acid transport in Riccia fluitans. Planta 152: 505–512.

Filleur S and Niel‐Vedele F (1999) Expression analysis of a high‐affinity nitrate transporter isolated from Arabidopsis thaliana by differential display. Planta 207: 461–469.

Gaffey CT and Mullins LJ (1958) Ion fluxes during the action potential in Chara. Journal of Physiology 144: 505–524.

Gelli A and Blumwald E (1997) Hyperpolarization‐activated Ca2+‐permeable channels in the plasma membrane of tomato cells. The Journal of Membrane Biology 155: 35–45.

Glass ADM, Shaff JE and Kochian LV (1992) Studies of the uptake of nitrate in barley. 4. Electrophysiology. Plant Physiology 99: 456–463.

Goldman DE (1943) Potential, impedance and rectification in membranes. The Journal of General Physiology 27: 37–60.

Grabov A and Blatt MR (1997) Parallel control of the inward‐rectifier K+ channel by cytosolic‐free Ca2+ and pH in Vicia guard cells. Planta 201: 84–95.

Hager A, Debus G, Edel H‐G, Stansky H and Serrano R (1991) Auxin induces exocytosis and the rapid synthesis of a high‐turnover pool of plasma membrane H+‐ATPase. Planta 185: 627–537.

Hamilton DWA, Hills A, Kohler B and Blatt MR (2000) Ca2+ channels at the plasma membrane of stomatal guard cells are activated by hyperpolarization and abscisic acid. Proceedings of the National Academy of Sciences of the USA 97: 4967–4972.

Hetherington AM and Brownlee C (2004) The generation of Ca2+ signals in plants. Annual Review of Plant Biology 55: 401–427.

Higinbotham N, Etherton B and Foster RJ (1967) Mineral ion contents and cell transmembrane electropotentials of pea and oat seedling tissue. Plant Physiology 42: 37–46.

Hille B (2001) Ionic Channels of Excitable Membranes. Sunderland, MA: Sinauer Press. pp. 1–813.

Hirsch RE, Lewis BD, Spalding EP and Sussman MR (1998) A role for the AKT1 potassium channel in plant nutrition. Science 280: 918–921.

Hodgkin AL, Huxley AF and Katz B (1952) Measurement of current‐voltage relations in the membrane of the giant axon of Loligo. Journal of Physiology 116: 424–448.

Homann U and Thiel G (2002) The number of K+ channels in the plasma membrane of guard cell protoplasts changes in parallel with the surface area. Proceedings of the National Academy of Sciences of the USA 99: 10215–10220.

Hosy E, Vavasseur A, Mouline K et al. (2003) The Arabidopsis outward K+ channel GORK is involved in regulation of stomatal movements and plant transpiration. Proceedings of the National Academy of Sciences of the USA 100: 5549–5554.

Johansson I, Wulfetange K, Poree F et al. (2006) External K+ modulates the activity of the Arabidopsis potassium channel SKOR via an unusual mechanism. The Plant Journal 46: 269–281.

Kitasato H (1968) The influence of H+ on the membrane potential and ion fluxes of Nitella clavata. The Journal of General Physiology 52: 60–87.

von Leibig J (1840) Die Chemie in ihrer Anwendung auf Agrikultur und Physiologie. Leipzig: Wilhelm Engelmann. pp. 1–835.

Lejay L, Gansel X, Cerezo M et al. (2003) Regulation of root ion transporters by photosynthesis: functional importance and relation with hexokinase. Plant Cell 15: 2218–2232.

Ling G and Gerard RW (1949) The normal membrane potential of frog sartorius fibers. Journal of Cellular and Comparative Physiology 34: 383–396.

Lopez‐Marques RL, Schiott M, Jakobsen MK and Palmgren MG (2004) Structure, function and regulation of primary H+ and Ca2+ pumps. In: Blatt MR (ed.) Membrane Transport in Plants, pp. 72–104. Oxford: Blackwell.

Loque D and von Wiren N (2004) Regulatory levels for the transport of ammonium in plant roots. Journal of Experimental Botany 55: 1293–1305.

Maathuis F and Sanders D (1994) Mechanism of high‐affinity potassium uptake in roots of Arabidopsis thaliana. Proceedings of the National Academy of Sciences of the USA 91: 9272–9276.

MacRobbie EAC (2000) ABA activates multiple Ca2+ fluxes in stomatal guard cells, triggering vacuolar K+(Rb+) release. Proceedings of the National Academy of Sciences of the USA 97: 12361–12368.

Meharg AA and Blatt MR (1995) Nitrate transport in root hairs of Arabidopsis thaliana: kinetic control by membrane voltage and pH. The Journal of Membrane Biology 145: 49–66.

Mitchell P (1969) Chemiosmotic coupling and energy transduction. Theoretical and Experimental Biophysics 2: 159–216.

Nakamura RL, Mckendree WL, Hirsch RE et al. (1995) Expression of an Arabidopsis potassium channel gene in guard cells. Plant Physiology 109: 371–374.

Osterhout WJV (1931) Physiological studies of single plant cells. Biological Reviews 6: 369–411.

Paciorek T, Zazimalova E, Ruthardt N et al. (2005) Auxin inhibits endocytosis and promotes its own efflux from cells. Nature 435: 1251–1256.

Pfeffer W (1877) Osmotische Untersuchungen. Leipzig: Wilhelm Engelmann. pp. 1–236.

Qiu QS, Guo Y, Dietrich MA, Schumaker KS and Zhu JK (2002) Regulation of SOS1, a plasma membrane Na+/H+ exchanger in Arabidopsis thaliana, by SOS2 and SOS3. Proceedings of the National Academy of Sciences of the USA 99: 8436–8441.

Rodriguez‐Navarro A, Blatt MR and Slayman CL (1986) A potassium‐proton symport in Neurospora crassa. The Journal of General Physiology 87: 649–674.

Slayman CL (1965) Electrical properties of Neurospora crassa. Respiration and the intracellular potential. The Journal of General Physiology 49: 93–116.

Slayman CL, Long WS and Lu CYH (1973) The relationship between ATP and an electrogenic pump in the plasma membrane of Neurospora crassa. The Journal of Membrane Biology 14: 303–338.

Slayman CL and Slayman CW (1974) Depolarization of the plasma membrane of Neurospora during active transport of glucose: evidence for a proton‐dependent cotransport system. Proceedings of the National Academy of Sciences of the USA 71: 1935–1939.

Spanswick RM (1970) Electrophysiological techniques and the magnitudes of the membrane potentials and resistances of Nitella translucens. Journal of Experimental Botany 21: 617–627.

Spanswick RM (1981) Electrogenic ion pumps. Annual Review of Plant Physiology and Plant Molecular Biology 32: 267–281.

Sutter JU, Campanoni P, Blatt MR and Paneque M (2006a) Setting SNAREs in a different wood. Traffic 7: 627–638.

Sutter JU, Campanoni P, Tyrrell M and Blatt MR (2006b) Selective mobility and sensitivity to SNAREs is exhibited by the Arabidopsis KAT1 K+ channel at the plasma membrane. Plant Cell 18: 935–954.

Sutter JU, Sieben C, Hartel A et al. (2007) Abscisic acid triggers the endocytosis of the Arabidopsis KAT1 K+ channel and its recycling to the plasma membrane. Current Biology 17: 1396–1402.

Takano J, Miwa K, Yuan LX, von Wiren N and Fujiwara T (2005) Endocytosis and degradation of BOR1, a boron transporter of Arabidopsis thaliana, regulated by boron availability. Proceedings of the National Academy of Sciences of the. USA 102: 12276–12281.

Tanford C (1983) Mechanism of free energy coupling in active transport. Annual Review of Biochemistry 52: 379–409.

Vidmar JJ, Zhuo D, Siddiqi MY et al. (2000) Regulation of high‐affinity nitrate transporter genes and high‐affinity nitrate influx by nitrogen pools in roots of barley. Plant Physiology 123: 307–318.

Willmer C and Fricker MD (1996) Stomata. London: Chapman and Hall. pp. 1–375.

Xu J, Li HD, Chen LQ et al. (2006) A protein kinase, interacting with two calcineurin B‐like proteins, regulates K+ transporter AKT1 in Arabidopsis. Cell 125: 1347–1360.

Further Reading

Ashley MK, Grant M and Grabov A (2006) Plant responses to potassium deficiencies: a role for transport proteins. Journal of Experimental Botany 57: 425–436.

Blatt MR, Leigh RA and Sanders D (1994) Membrane Transport in Plants and Fungi: Molecular Mechanisms and Control. Cambridge: Company of Biologists.

Broadley MR and White PJ (2005) Plant Nutritional Genomics. Oxford: Blackwells.

Marschner H (1995) Mineral Nutrition of Higher Plants. New York: Academic Press.

Yeo AR and Flowers T (2007) Plant Solute Transport. Oxford: Blackwells.

Contact Editor close
Submit a note to the editor about this article by filling in the form below.

* Required Field

How to Cite close
Blatt, Michael R(Dec 2008) Ion Transport at the Plant Plasma Membrane. In: eLS. John Wiley & Sons Ltd, Chichester. [doi: 10.1002/9780470015902.a0001307.pub2]