Nitric oxide in co-ordination with nitrogen reverses cadmium-inhibited photosynthetic activity by interacting with ethylene synthesis, strengthening the antioxidant system, and nitrogen and sulfur assimilation in mustard (Brassica juncea L.)

Abstract

Nitric oxide (NO) is a gaseous signaling molecule with known prominent roles in plant development and abiotic stress acclimation. This study reports that NO plus nitrogen (N) conspicuously alleviated cadmium (Cd)-inhibited photosynthetic activity by interacting with ethylene synthesis, and modifying the mechanisms of antioxidant enzymes, N and sulfur (S) assimilation in mustard (Brassica juncea L.) cv. Giriraj plants. The application of 100 µM sodium nitroprusside (SNP; NO donor) and 200 mg N kg−1 soil (as ammonium nitrate) to 200 mg Cd kg−1 soil-grown plants reduced oxidative stress (superoxide radical, hydrogen peroxide, and thiobarbituric acid reactive species content) and cell death through enhanced synthesis of metal chelators (non-protein thiols and phytochelatins) and limited Cd translocation. The reduced cellular ROS was also related to NO and N-mediated enhancement of S and N-assimilation, and antioxidants. The NO and N-mediated higher expression of psbA and psbB genes of D1 protein of PSII resulted into higher photosynthetic performance even under higher Cd regimes. Further, NO and N in the presence of aminoethoxyvinylglycine (AVG, ethylene biosynthesis inhibitor) under Cd stress showed reduced growth and photosynthetic attributes, with greater oxidative stress, substantiating ethylene involvement in NO and N-mediated reversal of Cd-inhibited photosynthesis. The principal component analysis showed a positive correlation between the treatment SNP + N + Cd and NO production, antioxidant enzymes, glutathione and metal chelators which resulted in higher N and S-assimilation, and better growth and photosynthetic capacity under Cd stress. The results indicate that NO-mediated alleviation of Cd toxicity and protection of photosynthetic activity were more conspicuous with N availability through the coordination with ethylene synthesis. The outcome of the study may be utilized in maintaining and managing hostile soils polluted with potentially toxic metals like Cd.