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, 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., www.plantcell.org; 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.

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

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