Mechanisms of Plant Responses and Adaptation to Soil Salinity

Abstract

Soil salinity is a major environmental stress that restricts the growth and yield of crops. Understanding the physiological, metabolic, and biochemical responses of plants to salt stress and mining the salt tolerance-associated genetic resource in nature will be extremely important for us to cultivate salt-tolerant crops. In this review, we provide a comprehensive summary of the mechanisms of salt stress responses in plants, including salt stress-triggered physiological responses, oxidative stress, salt stress sensing and signaling pathways, organellar stress, ion homeostasis, hormonal and gene expression regulation, metabolic changes, as well as salt tolerance mechanisms in halophytes. Important questions regarding salt tolerance that need to be addressed in the future are discussed.

Keywords: halophyte; hormones; ion homeostasis; osmotic stress; oxidative stress; salt stress; salt stress sensing.

Figure 1

Salt Stress Signaling Pathways The SOS signaling pathway, consisting of SOS3/SOS3-like calcium-binding protein 8 (SCaBP8), SOS2, and SOS1, is important for sensing salt-induced Ca²⁺ signals and in the regulation of ion homeostasis by extruding excessive Na⁺ out of cells. 14-3-3, GI, and ABI2 negatively regulate the kinase activity of SOS2. Ca²⁺-mediated binding of PKS5 with 14-3-3 releases the inhibition on SOS2. GIPCs act as putative salt stress sensors that directly bind to Na⁺ and trigger Ca²⁺ influx via an unknown Ca²⁺ channel. GIPCs-mediated Ca²⁺ influx is required for the activation of the SOS signaling pathway. RbohD/F are involved in the production of ROS at the plasma membrane, and ROS can activate the ANN1-mediated Ca²⁺ signaling pathway. AKT1, which is regulated by SCaBP8, mediates the influx of K⁺ to the cytosol under salt stress. MAP kinase cascades, including MAPKKK20, MKK2, MKK4, MPK3, MPK4, and MPK6, are involved in the relay of salt stress signals. Salt stress-induced accumulation of ABA activates subclass III SNF1-related protein kinase 2s (SnRK2s) via the PYR/PYLs-PP2Cs-mediated regulatory module. Subclass I SnRK2s are activated via an ABA-independent pathway under osmotic stress. Activated MPKs and SnRK2s transduce signals to downstream transcription factors, including ABFs, zips, MYBs, NACs, WRKYs, and AP2/ERFs, in the nucleus to induce the expression of stress-responsive genes. In the apoplast, cell wall-localized leucine-rich repeat extensins LRX3, LRX4, and LRX5, together with secreted peptides RALF22/23 and receptor-like kinase FER, function as a module to sense salt stress-induced cell wall changes. FER, RALFs, and LLG1 form a complex at the plasma membrane to trigger Ca²⁺ signaling and consequently activate the cell wall repair pathway. FER also inhibits the activity of AHA2 to regulate apoplastic pH. In the vacuole, NHXs, CAX1, TPK1, and H⁺-ATPase are involved in the regulation of ion homeostasis under high salinity. The dashed lines indicate that the negative regulatory roles are released under salt stress.

Figure 2

The Biological Functions of Phytohormones in the Regulation of Salt Stress Response in Plants ABA is a major hormone involved in the regulation of salt stress response, including the regulation of stomatal closure, ion homeostasis, salt stress-responsive gene expression, and metabolic changes. JA is required for the inhibition of root elongation and activation of antioxidative enzymes upon exposure to high salinity. Salt stress reduces the accumulation of endogenous bioactive GAs, leading to inhibition of plant growth and root elongation, delay of flowering, and promotion of survival under high salinity. The effect of ethylene on salt stress tolerance acts in a species- or gene-specific manner. The components involved in ethylene biosynthesis or signaling transduction either positively or negatively regulate ion homeostasis and seed germination, but ethylene induces detoxifying machineries and promotes survival under salt stress. SA participates in the accumulation of osmoprotectants, induction of antioxidative enzymes, and improvement of ion homeostasis under salt stress.

Figure 3

Major Transporters Mediating Na⁺ Homeostasis in Salinized Root Tissues The major pathways for Na⁺ uptake in the root epidermis are glutamate receptor-like (GLRs) channels or cyclic nucleotide-gated (CNGCs) non-selective cation channels and HKT2 high-affinity K⁺ transporters. Other possible pathways for Na⁺ uptake may involve AKT1 Shaker-type K⁺ channels, HAK5 high-affinity K⁺ transporters, the low-affinity cation transporter LCT1, and PIP2;1 aquaporins. The uptake of Na⁺ is counterbalanced by active Na⁺ extrusion via SOS1 Na⁺/H⁺ exchangers. Vacuolar Na⁺ sequestration is conferred by tonoplast-based Na⁺/H⁺ exchangers from the NHX family fueled by either H⁺-ATPase or H⁺-PPase pumps. Another component of vacuolar Na⁺ sequestration is efficient control over tonoplast slow- (SV) and fast- (FV) activating ion channels that may allow Na⁺ to leak back to the cytosol. Passive Na⁺ loading into the xylem is mediated by non-selective cation channels (NSCCs), and its active loading requires operation of cotransporters such as SOS1, CCC (cation-chloride cotransporters), and HKT2 (K⁺/Na⁺ symporter). Na⁺ withdrawal from the xylem is achieved by HKT1 high-affinity K⁺ transporters. Salinity-induced K⁺ loss from the root epidermis is mediated by NSCCs and depolarization-activated outward-rectifying GORK K⁺ channels.

Figure 4

A Proposed Model for the Mechanism of Salt Sequestration in Epidermal Bladder Cells Left part of figure shows the morphology of an epidermal cell (EC), stalk cell (SC), and epidermal bladder cell (EBC). Right part of the figure presents ion transport systems in the EC, SC, and EBC. SOS1 (Na⁺/H⁺ plasma membrane exchanger) and HKT1 (high-affinity potassium transporter) transport Na⁺, while SLAH (Cl⁻ permeable anion channel) and NRT (Cl⁻/H⁺ co-transporter) transport Cl⁻ from EC to EBC. In the EBC, NHX1 (tonoplast-based Na⁺/H⁺ exchanger) and CLC (anion channel) are required for the sequestration of excessive Na⁺ and Cl⁻ in the vacuole. Plasma membrane-localized H⁺-ATPase and vacuolar ATPase (V-ATPase) are essential for the generation of proton gradients and membrane potential that drive the transport of Na⁺ and Cl⁻ from the EC to the vacuole of the EBC.