Ion Changes and Signaling under Salt Stress in Wheat and Other Important Crops

Abstract

High concentrations of sodium (Na⁺), chloride (Cl^-), calcium (Ca²⁺), and sulphate (SO₄^2-) are frequently found in saline soils. Crop plants cannot successfully develop and produce because salt stress impairs the uptake of Ca²⁺, potassium (K⁺), and water into plant cells. Different intracellular and extracellular ionic concentrations change with salinity, including those of Ca²⁺, K⁺, and protons. These cations serve as stress signaling molecules in addition to being essential for ionic homeostasis and nutrition. Maintaining an appropriate K⁺:Na⁺ ratio is one crucial plant mechanism for salt tolerance, which is a complicated trait. Another important mechanism is the ability for fast extrusion of Na⁺ from the cytosol. Ca²⁺ is established as a ubiquitous secondary messenger, which transmits various stress signals into metabolic alterations that cause adaptive responses. When plants are under stress, the cytosolic-free Ca²⁺ concentration can rise to 10 times or more from its resting level of 50-100 nanomolar. Reactive oxygen species (ROS) are linked to the Ca²⁺ alterations and are produced by stress. Depending on the type, frequency, and intensity of the stress, the cytosolic Ca²⁺ signals oscillate, are transient, or persist for a longer period and exhibit specific "signatures". Both the influx and efflux of Ca²⁺ affect the length and amplitude of the signal. According to several reports, under stress Ca²⁺ alterations can occur not only in the cytoplasm of the cell but also in the cell walls, nucleus, and other cell organelles and the Ca²⁺ waves propagate through the whole plant. Here, we will focus on how wheat and other important crops absorb Na⁺, K⁺, and Cl^- when plants are under salt stress, as well as how Ca²⁺, K⁺, and pH cause intracellular signaling and homeostasis. Similar mechanisms in the model plant Arabidopsis will also be considered. Knowledge of these processes is important for understanding how plants react to salinity stress and for the development of tolerant crops.

Keywords: cereals; chloride; cytosolic Ca2+, K+, Na+, pH; salt stress; signaling; wheat.

Figure 1

Na⁺ influx into a root cell or mesophyll cell in the leaf causes an efflux of K⁺ from the cell by GORKs or NSCCs by Na⁺-induced membrane depolarization. The depolarization might activate the H⁺ATPase in the plasma membrane, pumping out protons that can be used for the Na⁺/H⁺ antiporter (SOS1). Na⁺ can also leak into the vacuole by SVs or FVs. Under high salinity stress, most Na⁺ is transported via NSCCs and HKTs into cells, and also by HAKs. GORK, outwards-rectifying K⁺ channel; HAK, high-affinity K⁺ channel; NSCC, nonselective cation channel; SV, slow vacuolar channel; FV, fast vacuolar channel.

Figure 2

Protoplasts from rice mesophyll in transmitted light (a), and labelled with Fura 2 (b), labelled with SBFI (c), protoplasts from rice root labelled with SBFI (d), from wheat root in transmitted light (e), and labelled with SBFI (f). Fluorescence emission was measured at 530–550 nm.

Figure 3

Chloride transport in the root, leaf, and stem of a plant via channels and transporters. SLAH, anion-channel-associated homolog; ALMT, aluminum-activated malate transporter; CCC, cation/chloride cotransporter; CLC, chloride channels; NRT, nitrate transporter; NPF, nitrate transporter 1/peptide transporter; SALT3, salt-tolerance-associated gene on chromosome 3; SLAC, slow anion channel; NAXT1, nitrate excretion transporter1, MSL10, mechano-sensitive ion channel 10; X-IRAC, inwardly-rectifying anion channel. For Cl⁻, various transporters, including NRT, NPF, SLAH, ALMT, and CCC, are involved in uptake and transport over long distances. Cl⁻ influx in the vacuole also involves ALMT and CLC.

Figure 4

Ca²⁺ transport by channels, antiporters, and ATPase-mediated pumps in a plant cell. ACA, autoinhibited Ca²⁺ATPase; CAX, Ca²⁺ exchanger; CNGC, cyclic-nucleotide-gated channel; DACC, depolarization-activated cation channel; ECA, ER-type Ca²⁺ATPase; FACC, fast-activating cation channel; GLR, glutamate-receptor-like channel; HACC, hyperpolarization-activated cation channel; InsP₃R, inositol 1,4,5-trisphosphate receptor-like channel; MLC, mechanosensitive-like channel; NSCC, nonselective cation channel; RyR, cyclic ADP-ribose (cADPR)-activator ryanodine receptor-like channel; SV, slow-activating vacuolar channel.

Figure 5

Simplified model of a cyclic nucleotide-gated channel (adapted from Demidchik et al. [269], with modification). The figure shows one subunit of the tetrameric channel with three CaM-Ca²⁺ (calmodulin-Ca²⁺)-binding sites. NT and CT, N- and C-terminal CaM-binding sites; IQ, isoleucine-glutamine domain, where CaM is bound; CNBD, cyclic-nucleotide-binding domain; P, part of the pore domain.

Figure 6

A possible model of SOS1 structure and its role in Na⁺-stress tolerance (adopted from Xie et al. [286]. SOS1, the salt overly sensitive 1 Na⁺/H⁺ antiporter, is composed of 12 transmembrane domains and transports Na⁺ out of the cell cytosol and protons into the cytosol. Na⁺ is proposed to bind to GIPC, a glycosyl inositol phosphoryl ceramide, a sphingolipid in the PM, and might also be transported into the cytosol by this lipid. The binding of Na⁺ to the lipid induces a transient efflux of Ca²⁺ into the cytosol, either via the sphingolipid molecule or by unknown Ca²⁺ channels. Ca²⁺ can be sensed by SOS3, a calcineurin B-like protein 10, and Ca²⁺-binding protein 8, SCABP8. These proteins can bind to and activate SOS2 and transport SOS2 to the serine phosphoryl domain 1136–1138 of SOS1 and activate this antiporter by phosphorylation: 749–925 activation area, 998–1146 C-terminal, 925–997 non-conservative area.

Figure 7

A simplified model of the CBL-CIPK network leading to ionic and pH homeostasis and ROS, reactive oxygen species, signaling. (i) Salt-stress-induced Ca²⁺ signals are sensed by CBL4 and CBL10, which combine with CIPK24 and CIPK8 to form CBL4/CIPK24 and CBL10/CIPK8, respectively, which activate the Na⁺/H⁺ antiporter in the PM and the Na⁺, K⁺/H⁺ antiporter in the tonoplast, respectively. This leads to less Na⁺ in the cytosol. (ii) ROS-induced Ca²⁺ signals are sensed by CBL1, which combines with CIPK26 and activates RBOHF, the respiratory burst oxidase homolog F, which produces ROS by Ca²⁺ binding to its EF-hand motif. (iii) K⁺ homeostasis is obtained by two mechanisms: In Arabidopsis, CBL1 combines with CIPK23 and activates AKT1 and HAK5, Arabidopsis K transporter1 and high-affinity K transporter, respectively, and CBL4 combines with CIPK6 and activates AKT2, K transporter 2. (iv) pH homeostasis (by H⁺) is obtained by binding between CBL7 and CIPK11, which activates AHA2, the PM H⁺ATPase, responsible for cytosolic pH homeostasis around 7.5 under normoxia.