Salicylic acid alleviates decreases in photosynthesis under salt stress by enhancing nitrogen and sulfur assimilation and antioxidant metabolism differentially in two mungbean cultivars

Abstract

Salicylic acid (SA) is known to affect photosynthesis under normal conditions and induces tolerance in plants to biotic and abiotic stresses through influencing physiological processes. In this study, physiological processes were compared in salt-tolerant (Pusa Vishal) and salt-sensitive (T44) cultivars of mungbean and examined how much these processes were induced by SA treatment to alleviate decrease in photosynthesis under salt stress. Cultivar T44 accumulated higher leaf Na⁺ and Cl⁻ content and exhibited greater oxidative stress than Pusa Vishal. Activity of antioxidant enzymes, ascorbate peroxidase (APX) and glutathione reductase (GR) was greater in Pusa Vishal than T44. Contrarily, activity of superoxide dismutase (SOD) was greater in T44. The greater accumulation of leaf nitrogen and sulfur through higher activity of their assimilating enzymes, nitrate reductase (NR) and ATP-sulfurylase (ATPS) increased reduced glutathione (GSH) content more conspicuously in Pusa Vishal than T44. Application of 0.5 mM SA increased nitrogen and sulfur assimilation, GSH content and activity of APX and GR. This resulted in the increase in photosynthesis under non-saline condition and alleviated the decrease in photosynthesis under salt stress. It also helped in restricting Na⁺ and Cl⁻ content in leaf, and maintaining higher efficiency of PSII, photosynthetic N-use efficiency (NUE) and water relations in Pusa Vishal. However, application of 1.0 mM SA resulted in inhibitory effects. The effect of SA was more pronounced in Pusa Vishal than T44. These results indicate that SA application alleviates the salt-induced decrease in photosynthesis mainly through inducing the activity of NR and ATPS, and increasing antioxidant metabolism to a greater extent in Pusa Vishal than T44.

Introduction

Salt stress is a major abiotic stress that causes detrimental effects on plant growth and productivity mainly through changes at physiological, biochemical and molecular level (Tester and Devenport, 2003, Khan et al., 2009, Syeed et al., 2010). The physiological processes that are primarily adversely affected by salt stress include ion toxicity, osmotic stress, nutrient deficiency and oxidative stress (Flowers, 2004). Salt stress may negatively affect photosynthesis by causing excess accumulation of leaf Na⁺ and Cl⁻, stomatal closure and oxidative stress resulting in the formation of reactive oxygen species (ROS). Excessive amounts of ROS can enhance membrane lipid peroxidation and electrolyte leakage (Gunes et al., 2007) and damage chloroplast, inhibit photochemical reactions and decrease photosynthesis (Steduto et al., 2000). ROS are toxic by-products of stress metabolism, but also play an important role as important signal transduction molecules in stress signaling and regulation of acclimation responses (Miller et al., 2010). As an adaptation response, plants activate several mechanisms to counteract the adverse effects of salt-induced ROS in plants. These mechanisms include ion homeostasis, detoxification of ROS and the use of available resources which directly influence photosynthesis. One of the defense mechanisms of plants includes the up-regulation of reduced glutathione (GSH), a low molecular weight antioxidant. GSH plays essential roles within plant metabolism and stress tolerance to ROS (Szalai et al., 2009). The potential of GSH as antioxidant is related to the activity of glutathione reductase (GR), which catalyzes the regeneration of GSH from oxidized glutathione (GSSG). Nitrogen (N) and sulfur (S) are constituents of GSH. Therefore, the activity of nitrate reductase (NR) and ATP-sulfurylase (ATPS), the enzymes involved in N and S assimilation may influence GSH content in plant cell. Plants containing high activities of antioxidant enzymes have shown considerable resistance to oxidative damage caused by ROS (Khan et al., 2007, Gapinska et al., 2008, Frary et al., 2010, Syeed et al., 2010). These mechanisms of ion homeostasis, GSH synthesis and antioxidant enzymes may be influenced by plant growth regulators under salt stress.

Salicylic acid (SA) is a naturally occurring plant hormone, influences various physiological and biochemical functions in plants, acts as an important signaling molecule and has diverse effects on tolerance to biotic and abiotic stress (Arfan et al., 2007, Syeed et al., 2010, Wang et al., 2010). Its role in plant tolerance to abiotic stresses such as ozone, UV-B, heat, heavy metal and osmotic stress (El-Tayeb, 2005, Wang et al., 2010) has been reported. In contrast, it has also been shown that high concentration of SA increases oxidative damage generated by NaCl in Arabidopsis (Borsani et al., 2001) and decreases drought tolerance in Zea mays (Nemeth et al., 2002). These reports show that SA has contrasting effects in inducing stress tolerance that may depend upon the species or concentration of SA applied. Therefore, it is critical to identify the physiological processes of plants differing in salt sensitivity, and examine how much these processes are induced by SA application in tolerant and sensitive types to alleviate the decrease in photosynthesis under salt stress. One of the objectives of the reported research was to compare the physiological processes in Pusa Vishal (salt-tolerant) and T44 (salt-sensitive) cultivars of mungbean. The other objective was to study the effectiveness of SA application in modulating these processes and alleviating decrease in photosynthesis under salt stress. The cultivars, Pusa Vishal and T44 have been shown to differ in sensitivity to salt stress (Khan and Syeed, 2003).