Nitric Oxide- and Sulfur-Mediated Reversal of Cadmium-Inhibited Photosynthetic Performance Involves Hydrogen Sulfide and Regulation of Nitrogen, Sulfur, and Antioxidant Metabolism in Mustard

Abstract

This study aimed to test the role of hydrogen sulfide (H2S) in the responses regarding the nitric oxide- (NO) and sulfur (S)-mediated improvement in photosynthesis and growth under cadmium (Cd) stress in mustard (Brassica juncea L. cv. Giriraj), and integrate the mechanisms of S, nitrogen (N), and antioxidant metabolism. The plants grown with Cd (200 mg Cd kg−1 soil) exhibited reduced assimilation of S and N and diminished photosynthetic performance, which was associated with higher Cd accumulation-induced excess reactive oxygen species (ROS) production. The application of 100 μM of sodium nitroprusside (SNP, a NO donor) together with a more prominent concentration of S resulted in increased photosynthetic S- and N-use efficiency, production of non-protein thiols and phytochelatins, efficiency of enzymatic (superoxide dismutase, ascorbate peroxidase, and glutathione reductase), non-enzymatic antioxidants (ascorbate and glutathione) limiting Cd accumulation and, thus, reduced oxidative stress (superoxide radical, hydrogen peroxide, and thiobarbituric acid reactive species content). The benefit of NO together with S was manifested through a modulation in H2S production. The use of 100 μM of hypotaurine (HT; H2S scavenger) or 100 μM of cPTIO (2-4-carboxyphenyl-4,4,5,5-tetramethylimidazoline-1-oxyl-3-oxide) in plants treated with NO plus S reversed the action of NO plus S, with a higher reduction in photosynthesis and growth with the use of HT, suggesting that H2S plays a significant role in the NO- and S-mediated alleviation of Cd stress. The interplay of NO and ES with H2S may be used in augmenting the photosynthesis and growth of Cd-grown mustard plants.