Plant Salinity Stress: Many Unanswered Questions Remain

Abstract

Salinity is a major threat to modern agriculture causing inhibition and impairment of crop growth and development. Here, we not only review recent advances in salinity stress research in plants but also revisit some basic perennial questions that still remain unanswered. In this review, we analyze the physiological, biochemical, and molecular aspects of Na⁺ and Cl^- uptake, sequestration, and transport associated with salinity. We discuss the role and importance of symplastic versus apoplastic pathways for ion uptake and critically evaluate the role of different types of membrane transporters in Na⁺ and Cl^- uptake and intercellular and intracellular ion distribution. Our incomplete knowledge regarding possible mechanisms of salinity sensing by plants is evaluated. Furthermore, a critical evaluation of the mechanisms of ion toxicity leads us to believe that, in contrast to currently held ideas, toxicity only plays a minor role in the cytosol and may be more prevalent in the vacuole. Lastly, the multiple roles of K⁺ in plant salinity stress are discussed.

Keywords: ion uptake; mechanisms of salt tolerance; membrane transporters; role of K+; salt stress; symplastic and apoplastic pathway; transport of Na+ and Cl−.

Figure 1

Schematic representation of possible transport pathways for Na⁺ and Cl⁻ uptake and their cellular and long-distance distribution. Red arrows represent Na⁺ and Cl⁻ entry sites and route through cell walls – apoplastic bypass flow. Black arrows represent Na⁺ and Cl⁻ entry sites and cytoplasmic route through plasma membrane-symplastic pathway. Various transporters (AKT, HKT2, NSCC, PIP2;1, NHA, LCT1, HAK5) may be involved in Na⁺ uptake and movement through the plasma membrane. Compartmentalization of Na+ in vacuoles is mediated by tonoplast transporters (CCX, NHX). The further Na⁺ redistribution over long distances may rely on members of several membrane transporter families (NSCC, HKT, NHA, CHX). Cl⁻ entry to the root cells through the plasma membrane may be mediated by Cl⁻/H⁺ co-transporter NRT. Vacuolar Cl⁻ sequestration may possibly be performed by two anion tonoplast transporters (ALMT and CLC). Cl⁻ membrane transport over long distances may be conducted by membrane transporters from different protein families (NPF, SLASH, ALMT, NPF, CCC). AKT, Arabidopsis K⁺ transporter; HKT, High-affinity K⁺ transporter Type; NSCC, Nonselective cation channels; PIP 2,1, Plasma membrane intrinsic protein (Aquaporin); NHA, Na⁺/H⁺ antiporter (SOS1); LCT1, Low-affinity cation transporter; HAK, High-affinity K⁺ uptake transporter; CHX, cation/H⁺ exchanger; NHX, Na⁺/H⁺ exchanger; NRT, Nitrate transporter; ALMT, Aluminum-activated malate transporter; CLC, Chloride channel; NPF, Nitrate transporter 1/peptide transporter; CCC, Cation/chloride cotransporter; SLASH, Anion channel associated homolog 1.

Figure 2

Schematic overview of early components involved in salt sensing. High external Na⁺ concentration leads to elevation of intracellular Ca²⁺, phosphatidic acid (PA), and cGMP. Cld PA can activate NHA (SOS1) in an independent manner. The main target of Ca²⁺ is CIBL4 (SOS3). The CIBL4 is capable to form the complex with CBL-interacting serine/threonine-protein kinase 24 (CIPK24, SOS2). The CIBL4-CIPK24 complex activates NHA (SOS1) and inhibits Na⁺ uptake by HKT2. CIPK24 together with SCaBP (SOS3 like protein) is involved in activation of the V-ATPase. CIPK24 participates in the activation of vacuolar transporters such as CAX and NHX. The rise in cytosolic Ca²⁺ concentration could trigger interaction of RSA1-RITF1. RSA1-RITF1 complex activates promoter of SOS1 gene. PA is involved in activation of mitogen-activated protein kinase 6 (MPK6). MPK6 can directly phosphorylate SOS1. The Ca²⁺-dependent kinase (CDPK3) and cytosolic Ca²⁺ lead to activation of vacuolar two-pore K⁺ channels (TPKs) and subsequent K⁺ release from vacuole. Due to the plasma membrane localization, SOS5 protein is considered to be potential candidate for extracellular Na⁺ sensing and helps maintain of cell wall integrity and architecture. Annexin1 (ANN1) is capable to sense the high concentrations of extracellular Na⁺ by mediating ROS-activated Ca²⁺ influx through the plasma membrane of plant cells. The rise of cGMP leads to inhibition of Na⁺ uptake, possibly via cyclic nucleotide–gated ion channels (CNGSs) and glutamate receptor (GLRs). PIP2;1, CNGCs, and GLRs could be blocked by exogenous Ca²⁺. The ROS production leads to K⁺ leak via activation of outward K⁺ channels – KOR (guard cells outward K⁺ channel, GORK) and NSCC. The intracellular accumulation of ROS at high levels can trigger programmed cell death (PCD).