Salicylic acid improves salinity tolerance in Arabidopsis by restoring membrane potential and preventing salt-induced K+ loss via a GORK channel

Abstract

Despite numerous reports implicating salicylic acid (SA) in plant salinity responses, the specific ionic mechanisms of SA-mediated adaptation to salt stress remain elusive. To address this issue, a non-invasive microelectrode ion flux estimation technique was used to study kinetics of NaCl-induced net ion fluxes in Arabidopsis thaliana in response to various SA concentrations and incubation times. NaCl-induced K+ efflux and H+ influx from the mature root zone were both significantly decreased in roots pretreated with 10–500 μM SA, with strongest effect being observed in the 10–50 μM SA range. Considering temporal dynamics (0–8-h SA pretreatment), the 1-h pretreatment was most effective in enhancing K+ retention in the cytosol. The pharmacological, membrane potential, and shoot K+ and Na+ accumulation data were all consistent with the model in which the SA pretreatment enhanced activity of H+-ATPase, decreased NaCl-induced membrane depolarization, and minimized NaCl-induced K+ leakage from the cell within the first hour of salt stress. In long-term treatments, SA increased shoot K+ and decreased shoot Na+ accumulation. The short-term NaCl-induced K+ efflux was smallest in the gork1-1 mutant, followed by the rbohD mutant, and was highest in the wild type. Most significantly, the SA pretreatment decreased the NaCl-induced K+ efflux from rbohD and the wild type to the level of gork1-1, whereas no effect was observed in gork1-1. These data provide the first direct evidence that the SA pretreatment ameliorates salinity stress by counteracting NaCl-induced membrane depolarization and by decreasing K+ efflux via GORK channels.

Exogenous salicylic acid improves photosynthesis and growth through increase in ascorbate-glutathione metabolism and S assimilation in mustard under salt stress

“…The results are consistent with the other studies showing that application of SA decreased Na C concentration in roots and shoots of Zea mays seedlings and resulted in an increase of nutrients content. 23,24 Jayakannan et al 25 have also shown that SA pretreatment in Arabidopsis did not decrease Na C entry into roots, but reduced Na C accumulation in the shoot. Application of SA has been shown to influence plant growth by promoting protective reactions involving photosynthetic pigments and membrane integrity.…”

Global plant-responding mechanisms to salt stress: physiological and molecular levels and implications in biotechnology

“…Ion homeostasis, especially the optimum K + /Na + ratio, is crucial for plant salt stress. Discoveries achieved by non-invasive microelectrode ion flux estimation (MIFE) techniques (Shabala et al, 1997) revealed that SA pretreatment can enhance K + retention, increase H + -ATPase activity and reduce K + loss under salt stress (Jayakannan et al, 2013). Generally speaking, the potential mechanism of SA to enhance salt tolerance lies in improving photosynthesis, enhancing antioxidant protection and maintaining the optimum K + /Na + ratio (Horváth et al, 2007;Jayakannan et al, 2013;Nazar et al, 2011).…”

An Arabidopsis Soil-Salinity–Tolerance Mutation Confers Ethylene-Mediated Enhancement of Sodium/Potassium Homeostasis

“…Liu et al, 2000;Qiu et al, 2002;Quan et al, 2007) are also involved in the signaling pathways by which Na + is eventually transported back out of the root, while the HIGH-AFFINITY K + TRANSPORTER1 (HKT1) gene product (HKT1) can retrieve Na + from the transpiration stream xylem sap before it reaches the shoot (Mäser et al, 2002;Sunarpi et al, 2005;Møller et al, 2009). High salinity also causes strong depolarization of the electrical potential difference across the plasma membrane, leading to tissue K + loss via outward-rectifying K + channels Jayakannan et al, 2013), in turn impairing metabolic processes. Therefore, the ability of plants to retain tissue K concentration correlates with plant salinity tolerance (Maathuis and Amtmann, 1999;Chen et al, 2005;Cuin et al, 2008;Munns and Tester, 2008).…”

“…For example, salt increases abscisic acid (ABA) levels and activates ABA-dependent signaling pathways (Zhu, 2002), in turn regulating transcriptome-level salt stress responses and physiological adaptation to salt stress (Xiong et al, 2001). Salicylic acid can prevent salinity-induced K loss, thus promoting Arabidopsis salinity tolerance (Jayakannan et al, 2013). Kinetin can inhibit K release into the xylem (Collins and Kerrigan, 1974;Hong and Sucoff, 1976), increase K + channel-mediated root K uptake (Shabala et al, 2009), and thus alleviate the negative impact of salinity on plants (Tounekti et al, 2011).…”