Exogenous nitric oxide alleviates sulfur deficiency-induced oxidative damage in tomato seedlings

Despite numerous reports on the role of nitric oxide (NO) in regulating plants growth and mitigating different environmental stresses, its participation in sulfur (S) -metabolism remains largely unknown. Therefore, we studied the role of NO in S acquisition and S-assimilation in tomato seedlings under low S-stress conditions by supplying NO to the leaves of S-sufficient and S-deficient seedlings. S-starved plants exhibited a substantial decreased in plant growth attributes, photosynthetic pigment chlorophyll (Chl) and other photosynthetic parameters, and activity of enzymes involved in Chl biosynthesis (δ-aminolevulinic acid dehydratase), and photosynthetic processes (carbonic anhydrase and RuBisco). Also, S-deficiency enhanced reactive oxygen species (ROS) (superoxide and hydrogen peroxide) and lipid peroxidation (malondialdehyde) levels in tomato seedlings. Contrarily, foliar supplementation of NO to S-deficient seedlings resulted in considerably reduced ROS formation in leaves and roots, which alleviated low S-stress-induced lipid peroxidation. However, exogenous NO enhanced proline accumulation by increasing proline metabolizing enzyme (Δ1-pyrroline-5-carboxylate synthetase) activity and also increased NO, hydrogen sulfide (a gasotransmitter small signaling molecule) and S uptake, and content of S-containing compounds (cysteine and reduced glutathione). Under S-limited conditions, NO improved S utilization efficiency of plants by upregulating the activity of S-assimilating enzymes (ATP sulfurylase, adenosine 5-phosphosulfate reductase, sulfide reductase and O-acetylserine (thiol) lyase). Under S-deprived conditions, improved S-assimilation of seedlings receiving NO resulted in improved redox homeostasis and ascorbate content through increased NO and S uptake. Application of 2-(4-carboxyphenyl)-4,4,5,5-tetramethylimidazoline-1-oxy l-3-oxide (an NO scavenger) invalidated the effect of NO and again caused low S-stress-induced oxidative damage, confirming the beneficial role of NO in seedlings under S-deprived conditions. Thus, exogenous NO enhanced the tolerance of tomato seedlings to limit S-triggered oxidative stress and improved photosynthetic performance and S assimilation.