Ion Transport at the Plant Plasma Membrane

Abstract

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, genomics, 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.

Key Concepts

  • Study of ion transport is the key for our understanding of mineral nutrition in plants.
  • Ion transporters and their biophysical properties form the basis for understanding of the membrane potentials.
  • Plasma membrane H+‐ATPase of plants and the Na+/K+‐ATPase of animals are both members of the P‐type membrane ATPase superfamily.
  • The transport of many solutes is coupled by H+ across plasma membrane of plant cells.
  • Ion channels carry much larger current than pumps and cotransporters on a unit protein basis.
  • Membrane vesicle traffic regulates ion transport by controlling the population and availability of transporters at the membrane and, in some cases, by direct binding with ion transporters.
  • Plasma membrane ion transporters have coevolved with the evolution of land plants.

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 energises 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. (a–c) Redrawn from 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 with permission from Wiley. (d) H+‐coupled antiport of Na+ is electroneutral and provides a pathway for H+ return across the membrane but not for charge flux. Courtesy of Michael Blatt.
Figure 2. Interaction of H+‐coupled K+ symport and the H+‐ATPase in Neurospora. (a) Membrane depolarisation (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 depolarisation 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. Reproduced with permission of Springer Nature from 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.
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 (a) and guard cells (b) 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. (a) Reproduced from Sutter et al. 2006b, www.plantcell.org.
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–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. Reproduced with permission of Springer Nature from 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.
Figure 5. KAT1 K+ channels recycle to plasma membrane‐localised 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. Reprinted from 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 with permission from Elsevier.
Figure 6. Similarity heat map for the evolution of membrane transporters in different species. The GENESIS simulation environment was used to estimate the similarities among protein families. Candidate protein sequences were selected by BLASTP software searches that satisfied the criteria of E value <10−5. Coloured squares indicate protein sequence similarity from zero (yellow) to 100% (red). Grey squares indicate that no proteins were found that satisfied the selection criteria. KATs represent the AKTs/KATs/GORKs proteins. ABCC, ATP‐binding cassette C transporter; ACA, autoinhibited Ca2+‐ATPase; AHA, Arabidopsis plasma membrane H+‐ATPase; AKT, Arabidopsis inwardly rectifying K+ channel; ALMT, aluminium‐activated malate transporter; CAX, cation proton exchanger; CLC, chloride channel; CNGC, cyclic nucleotide gated channel; GORK, guard cell outwardly rectifying K+ channel; GLR, Glu receptor‐like Ca2+ channel; HAK, high‐affinity K+ transporter; HKT, high affinity K+/Na+ transporter; KAT, guard cell inwardly rectifying K+ channel; NHX, Na+/H+ antiporter; TPK, tonoplast K+ channel; PIP, plasma membrane intrinsic protein; SLAC, slow anion channel; SnRK2, SNF1‐related protein kinase2; SUC, Suc transporter; TPC, two‐pore channel; TPK, two‐pore channel, a guard cell membrane transporter. Reprinted from Cai S, Chen G, Wang Y et al. (2017) Evolutionary conservation of ABA signaling for stomatal closure. Plant Physiology 174: 732–747 with permission from The American Society of Plant Biologists.
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References

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

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.

Armstrong F, Leung J, Grabov A, et al. (1995) Sensitivity to abscisic acid of guard‐cell K+ channels is suppressed by abi1‐1, a mutant Arabidopsis gene encoding a putative protein phosphatase. Proceedings of the National Academy of Sciences United States of America 92: 9520–9524.

Bayle V, Arrighi JF, Creff A, et al. (2011) Arabidopsis thaliana high‐affinity phosphate transporters exhibit multiple levels of posttranslational regulation. The Plant Cell 23: 1523–1535.

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 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 United States of America 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.

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 (2004) In: Roberts J, Imaseki H, McManus M, Robinson DG and Rose J (eds) Membrane Transport in Plants. Annual Plant Reviews, vol. 15. Oxford, UK: Blackwell.

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.

Bouguyon E, Brun F, Meynard D, et al. (2015) Multiple mechanisms of nitrate sensing by Arabidopsis nitrate transceptor NRT1.1. Nature Plants 1: 15015.

Brearley J, Venis MA and Blatt MR (1997) The effect of elevated CO2 concentrations on K+ and anion channels of Vicia faba L. guard cells. Planta 203: 145–154.

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

Cai S, Chen G, Wang Y, et al. (2017) Evolutionary conservation of ABA signaling for stomatal closure. Plant Physiology 174: 732–747.

Chen ZH, Hills A, Lim CK and Blatt MR (2010) Dynamic regulation of guard cell anion channels by cytosolic free Ca2+ concentration and protein phosphorylation. The Plant Journal 61: 816–825.

Chen ZH, Chen G, Dai F, et al. (2017) Molecular evolution of grass stomata. Trends in Plant Science 22: 124–139.

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

Colcombet J, Lelièvre F, Thomine S, et al. (2005) Distinct pH regulation of slow and rapid anion channels at the plasma membrane of Arabidopsis thaliana hypocotyl cells. Journal of Experimental Botany 56: 1897–1903.

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 and Blatt MR (2009) What makes a gate? The ins and outs of Kv‐like K+ channels in plants. Trends in Plant Science 14: 383–390.

Dreyer I, Porée F, Schneider A, et al. (2004) Assembly of plant Shaker‐like Kout channels requires two distinct sites of the channel α‐subunit. Biophysical Journal 87: 858–872.

Falhof J, Pedersen JT, Fuglsang AT and Palmgren M (2016) Plasma membrane H+‐ATPase regulation in the center of plant physiology. Molecular Plant 9: 323–337.

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.

Flowers TJ, Galal HK and Bromham L (2010) Evolution of halophytes: multiple origins of salt tolerance in land plants. Functional Plant Biology 37: 604–612.

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

Geiger D, Scherzer S, Mumm P, et al. (2010) Guard cell anion channel SLAC1 is regulated by CDPK protein kinases with distinct Ca2+ affinities. Proceedings of the National Academy of Sciences United States of America 107: 8023–8028.

Geiger D, Maierhofer T, AL‐Rasheid KA, et al. (2011) Stomatal closure by fast abscisic acid signaling is mediated by the guard cell anion channel SLAH3 and the receptor RCAR1. Science Signaling 4: ra32.

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.

Gonzalez E, Solano R, Rubio V, et al. (2005) Phosphate transporter traffic facilitator1 is a plant‐specific SEC12‐related protein that enables the endoplasmic reticulum exit of a high‐affinity phosphate transporter in Arabidopsis. The Plant Cell 17: 3500–3512.

González W, Riedelsberger J, Morales‐Navarro SE, et al. (2012) The pH sensor of the plant K+‐uptake channel KAT1 is built from a sensory cloud rather than from single key amino acids. Biochemical Journal 442: 57–63.

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.

Grabov A, Leung J, Giraudat J and Blatt MR (1997) Alteration of anion channel kinetics in wild‐type and abi1‐1 transgenic Nicotiana benthamiana guard cells by abscisic acid. The Plant Journal 12: 203–213.

Grabov A and Blatt MR (1998) Membrane voltage initiates Ca2+ waves and potentiates Ca2+ increases with abscisic acid in stomatal guard cells. Proceedings of the National Academy of Sciences United States of America 95: 4778–4783.

Grefen C, Chen Z, Honsbein A, et al. (2010) A novel motif essential for SNARE interaction with the K+ channel KC1 and channel gating in Arabidopsis. The Plant Cell 22: 3076–3092.

Grefen C, Karnik R, Larson E, et al. (2015) A vesicle‐trafficking protein commandeers Kv channel voltage sensors for voltage‐dependent secretion. Nature Plants 1: 15108.

Hachez C, Laloux T, Reinhardt H, et al. (2014) Arabidopsis SNAREs SYP61 and SYP121 coordinate the trafficking of plasma membrane aquaporin PIP2; 7 to modulate the cell membrane water permeability. The Plant Cell 26: 3132–3147.

Hamamoto S, Horie T, Hauser F, et al. (2015) HKT transporters mediate salt stress resistance in plants: from structure and function to the field. Current Opinion in Biotechnology 32: 113–120.

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 United States of America 97: 4967–4972.

Hamilton DW, Hills A and Blatt MR (2001) Extracellular Ba2+ and voltage interact to gate Ca2+ channels at the plasma membrane of stomatal guard cells. FEBS Letters 491: 99–103.

Haruta M, Burch HL, Nelson RB, et al. (2010) Molecular characterization of mutant Arabidopsis plants with reduced plasma membrane proton pump activity. Journal of Biological Chemistry 285: 17918–17929.

Held K, Pascaud F, Eckert C, et al. (2011) Calcium‐dependent modulation and plasma membrane targeting of the AKT2 potassium channel by the CBL4/CIPK6 calcium sensor/protein kinase complex. Cell Research 21: 1116.

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, pp. 1–813. Sunderland, MA: Sinauer Press.

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 United States of America 99: 10215–10220.

Honsbein A, Sokolovski S, Grefen C, et al. (2009) A tripartite SNARE‐K+ channel complex mediates in channel‐dependent K+ nutrition in Arabidopsis. The Plant Cell 21: 2859–2877.

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 United States of America 100: 5549–5554.

Jezek M and Blatt MR (2017) The membrane transport system of the guard cell and its integration for stomatal dynamics. Plant Physiology 174: 487–519.

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.

Karnik R, Waghmare S, Zhang B, et al. (2017) Commandeering channel voltage sensors for secretion, cell turgor, and volume control. Trends in Plant Science 22: 81–95.

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.

Labro AJ, Lacroix JJ, Villalba‐Galea CA, Snyders DJ and Bezanilla F (2012) Molecular mechanism for depolarization‐induced modulation of Kv channel closure. The Journal of General Physiology 140: 481–493.

Lefoulon C, Karnik R, Honsbein A, et al. (2014) Voltage-sensor transitions of the inward‐rectifying K+ channel KAT1 indicate a latching mechanism biased by hydration within the voltage sensor. Plant Physiology 166: 960–975.

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

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.

Leube MP, Grill E and Amrhein N (1998) ABI1 of Arabidopsis is a protein serine/threonine phosphatase highly regulated by the proton and magnesium ion concentration. FEBS Letters 424: 100–104.

Leung J, Bouvier‐Durand M, Morris PC, et al. (1994) Arabidopsis ABA response gene ABI1: features of a calcium‐modulated protein phosphatase. Science 264: 1448–1452.

Lind C, Dreyer I, López‐Sanjurjo EJ, et al. (2015) Stomatal guard cells co‐opted an ancient ABA‐dependent desiccation survival system to regulate stomatal closure. Current Biology 25 (7): 928–935.

Linder B and Raschke K (1992) A slow anion channel in guard cells, activating at large hyperpolarization, may be principal for stomatal closing. FEBS Letters 313: 27–30.

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, UK: 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 United States of America 91: 9272–9276.

Maurel C, Verdoucq L, Luu DT, et al. (2008) Plant aquaporins: membrane channels with multiple integrated functions. Annual Reviews of Plant Biology 59: 595–624.

McAdam SA, Brodribb TJ, Banks JA, et al. (2016) Abscisic acid controlled sex before transpiration in vascular plants. Proceedings of the National Academy of Sciences United States of America 113: 12862–12867.

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.

Meyer S, Mumm P, Imes D, et al. (2010) AtALMT12 represents an R‐type anion channel required for stomatal movement in Arabidopsis guard cells. The Plant Journal 63: 1054–1062.

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.

Negi J, Matsuda O, Nagasawa T, et al. (2008) CO2 regulator SLAC1 and its homologues are essential for anion homeostasis in plant cells. Nature 452: 483.

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

Park SY, Fung P, Nishimura N, et al. (2009) Abscisic acid inhibits type 2C protein phosphatases via the PYR/PYL family of START proteins. Science 324: 1068–1671.

Parker JL and Newstead S (2014) Molecular basis of nitrate uptake by the plant nitrate transporter NRT1.1. Nature 507: 68–72.

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

Platten JD, Cotsaftis O, Berthomieu P, et al. (2006) Nomenclature for HKT transporters, key determinants of plant salinity tolerance. Trends in Plant Science 11: 372–374.

Pornsiriwong W, Estavillo GM, Chan KX, et al. (2017) A chloroplast retrograde signal, 3′‐phosphoadenosine 5′‐phosphate, acts as a secondary messenger in abscisic acid signaling in stomatal closure and germination. eLife 6: e23361.

Qiu QS, Guo Y, Dietrich MA, et al. (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 United States of America 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.

Ruszala EM, Beerling DJ, Franks PJ, et al. (2011) Land plants acquired active stomatal control early in their evolutionary history. Current Biology 21: 1030–1035.

Schroeder JI and Keller BU (1992) Two types of anion channel currents in guard cells with distinct voltage regulation. Proceedings of the National Academy of Sciences United States of America 89: 5025–5029.

Siegel RS, Xue SW, Murata Y, et al. (2009) Calcium elevation‐dependent and attenuated resting calcium‐dependent abscisic acid induction of stomatal closure and abscisic acid‐induced enhancement of calcium sensitivities of S‐type anion and inward‐rectifying K+ channels in Arabidopsis guard cells. Plant Journal 59: 207–220.

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 United States of America 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.

Sun J, Bankston JR, Payandeh J, et al. (2014) Crystal structure of the plant dual‐affinity nitrate transporter NRT1.1. Nature 507: 73–77.

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.

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

Tang RJ, Liu H, Yang Y, et al. (2012) Tonoplast calcium sensors CBL2 and CBL3 control plant growth and ion homeostasis through regulating V‐ATPase activity in Arabidopsis. Cell Research 22: 1650.

Ueno K, Kinoshita T, Inoue SI, Emi T and Shimazaki KI (2005) Biochemical characterization of plasma membrane H+‐ATPase activation in guard cell protoplasts of Arabidopsis thaliana in response to blue light. Plant and Cell Physiology 46: 955–963.

Vahisalu T, Kollist H, Wang YF, et al. (2008) SLAC1 is required for plant guard cell S‐type anion channel function in stomatal signalling. Nature 452: 487.

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.

de Vries J, Stanton A, Archibald JM and Gould SB (2016) Streptophyte terrestrialization in light of plastid evolution. Trends in Plant Science 21: 467–476.

Wang Y and Blatt MR (2011) Anion channel sensitivity to cytosolic organic acids implicates a central role for oxaloacetate in integrating ion flux with metabolism in stomatal guard cells. Biochemical Journal 439: 161–170.

Wang Y, Papanatsiou M, Eisenach C, et al. (2012) Systems dynamic modeling of a guard cell Cl− channel mutant uncovers an emergent homeostatic network regulating stomatal transpiration. Plant Physiology 160: 1956–1967.

Wang Y, Chen ZH, Zhang B, Hills A and Blatt MR (2013) PYR/PYL/RCAR abscisic acid receptors regulate K+ and Cl− channels through reactive oxygen species‐mediated activation of Ca2+ channels at the plasma membrane of intact Arabidopsis guard cells. Plant Physiology 163: 566–577.

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

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.

Zhang B, Karnik R, Waghmare S, et al. (2017) VAMP721 conformations unmask an extended motif for K+ channel binding and gating control. Plant Physiology 173: 536–551.

Zhang B, Karnik R, Wang Y, et al. (2015) The Arabidopsis R‐SNARE VAMP721 interacts with KAT1 and KC1 K+ channels to moderate K+ current at the plasma membrane. The Plant Cell 27: 1697–1717.

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, UK: Company of Biologists.

Broadley MR and White PJ (2005) Plant Nutritional Genomics. Oxford, UK: Blackwell.

van Hooren M and Munnik T (2017) Plant plasma membrane. Encyclopedia of Life Sciences. DOI: 10.1002/9780470015902.a0001672.pub3.

Lau OS (2017) Stomata. Encyclopedia of Life Sciences. DOI: 10.1002/9780470015902.a0002075.pub3.

Marchant DB, Soltis DE and Soltis PS (2016) Genome evolution in plants. Encyclopedia of Life Sciences. DOI: 10.1002/9780470015902.a0026814.

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

McAinsh MR and Taylor JE (2017) Cell signalling mechanisms in plants. Encyclopedia of Life Sciences. DOI: 10.1002/9780470015902.a0026507.

Yeo AR and Flowers T (2007) Plant Solute Transport. Oxford, UK: Blackwell.

Zhu J‐K (2007) Plant salt stress. Encyclopedia of Life Sciences. DOI: 10.1002/9780470015902.a0001300.pub2.

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Wang, Yizhou, Blatt, Michael R, and Chen, Zhong‐Hua(Jul 2018) Ion Transport at the Plant Plasma Membrane. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0001307.pub3]