Summary: Agriculture is expanding into regions that are affected by salinity. This review considers the energetic costs of salinity tolerance in crop plants and provides a framework for a quantitative assessment of costs. Different sources of energy, and modifications of root system architecture that would maximize water vs ion uptake are addressed. Energy requirements for transport of salt (NaCl) to leaf vacuoles for osmotic adjustment could be small if there are no substantial leaks back across plasma membrane and tonoplast in root and leaf. The coupling ratio of the H⁺‐ATPase also is a critical component. One proposed leak, that of Na⁺ influx across the plasma membrane through certain aquaporin channels, might be coupled to water flow, thus conserving energy. For the tonoplast, control of two types of cation channels is required for energy efficiency. Transporters controlling the Na⁺ and Cl⁻ concentrations in mitochondria and chloroplasts are largely unknown and could be a major energy cost. The complexity of the system will require a sophisticated modelling approach to identify critical transporters, apoplastic barriers and root structures. This modelling approach will inform experimentation and allow a quantitative assessment of the energy costs of NaCl tolerance to guide breeding and engineering of molecular components.

Summary: P‐type H⁺ ATPases mediate active H⁺ efflux from plant cells. They generate a proton motive force across the plasma membrane, providing the free energy to drive the transport of other solutes, partly by coupling to H⁺ influx. Wegner & Shabala (2020) recently suggested that passive H⁺ influx can exceed pump‐driven efflux due to ‘active buffering’, that is, cytosolic H⁺ scavenging and apoplastic H⁺ generation by metabolism (‘biochemical pH clamp’). Charge balance is provided by K⁺ efflux or anion influx. Here, this hypothesis is extended to net H⁺ efflux: even though H⁺ pumping is faster than backflow via symporters and antiporters, a progressive increase in the transmembrane pH gradient is avoided. Cytosolic H⁺ release is associated with bicarbonate formation from CO₂. Bicarbonate serves as substrate for the PEPCase, catalyzing the reaction from phosphoenolpyruvate to oxaloacetate, which is subsequently reduced to malate. Organic anions such as malate and citrate are released across the plasma membrane and are (partly) protonated in the apoplast, thus limiting pump‐induced acidification. Moreover, a ‘biophysical pH clamp’ is introduced, that is, adjustment of apoplastic/cytosolic pH involving net H⁺ fluxes across the plasma membrane, while the gradient between compartments is maintained. The clamps are not mutually exclusive but are likely to coexist.

Summary: Solute uptake and release by plant cells are frequently energized by coupling to H⁺ influx supported by the proton motive force (pmf). The pmf results from a stable pH difference between the apoplast and the cytosol, with bulk values ranging from 4.9 to 5.8 and from 7.1 to 7.5, respectively, in combination with a negative electrical membrane potential. The P‐type H⁺ ATPases pumping H⁺ from the cytosol into the apoplast at the expense of ATP hydrolysis are generally viewed as the only pmf source, exclusively linking membrane transport to energy metabolism. However, recent evidence suggests that pump activity may be insufficient to energize transport, particularly under stress conditions. Indeed, cytosolic H⁺ scavenging and apoplastic H⁺ generation by metabolism (denoted as ‘active’ buffering in contrast to the readily exhausted ‘passive’ matrix buffering) also stabilize the pH gradient. In the cytosol, H⁺ scavenging is mainly associated with malate decarboxylation catalyzed by malic enzyme, and via the GABA shunt of the tricarboxylic acid (TCA) cycle involving glutamate decarboxylation. In the apoplast, formation of bicarbonate from CO₂, the end‐product of respiration, generates H⁺ at pH ≥ 6. Membrane potential is stabilized by K⁺ release and/or by anion uptake via ion channels. Finally, thermodynamic aspects of active buffering are discussed.

A series of recent publications has launched a debate on trans-membrane water secretion into root xylem vessels against a water potential gradient, energised by a cotransport with salts (e.g. KCl) that follow their chemical potential gradient. Cation–chloride–cotransporter -type transporters that function in this way in mammalian epithelia were detected in root stelar cells bordering on xylem vessels. Using literature data on barley (Hordeum vulgare L.) seedlings, one study confirmed that K+ and Cl– gradients across stelar cell membranes favour salt efflux. Moreover, the energetic costs of putative water secretion into the xylem (required for maintaining ionic gradients) would amount to just 0.12% of the energy captured by photosynthetic C assimilation if transpirational water flow relied exclusively on this mechanism. Here, a detailed thermodynamic analysis of water secretion into xylem vessels is undertaken, including an approach that exploits its analogy to a desalinisation process. Water backflow due to the passive hydraulic conductivity of stelar cell membranes is also considered. By comparing free energy consumption by putative water secretion with (i) the free energy pool provided by root respiration and (ii) stelar ATPase activity, the feasibility of this mechanism is confirmed but is shown to depend critically on the plant’s energy status.

Current concepts of plant membrane transport are based on the assumption that water and solutes move across membranes via separate pathways. According to this view, coupling between the fluxes is more or less exclusively constituted via the osmotic force that solutes exert on water transport. This view is questioned here, and experimental evidence for a cotransport of water and solutes is reviewed. The overview starts with ion channels that provide pathways for both ion and water transport, as exemplified for maxi K⁺ channels from cytoplasmic droplets of Chara corallina. Aquaporins are usually considered to be selective for water (just allowing for slippage of some other small, neutral molecules). Recently, however, a “dual function” aquaporin has been characterized from Arabidopsis thaliana (AtPIP2.1) that translocates water and at the same time conducts cations, preferentially Na⁺. By analogy with mammalian physiology, other candidates for solute-water flux coupling are cation-chloride cotransporters of the CCC type, and transporters of sugars and amino acids. The last part is dedicated to possible physiological functions that could rely on solute-water cotransport. Among these are the generation of root pressure, refilling of embolized xylem vessels, fast turgor-driven movements of leaves, cell elongation (growth), osmoregulation and adjustment of buoyancy in marine algae. This review will hopefully initiate further research in the field.