Melatonin confers saline-alkali tolerance in tomato by alleviating nitrosative damage and S-nitrosylation of H+-ATPase 2.

Soil salinization and alkalization disrupt redox homeostasis, impairing plant survival and crop production. Disruption of redox homeostasis can cause accumulation of reactive nitrogen species, such as nitric oxide (NO), which causes nitrosative damage in which the properties of biomacromolecules are altered. It is unclear whether melatonin regulates NO homeostasis, thereby affecting plant saline-alkali tolerance. In tomato (Solanum lycopersicum), excess NO caused by saline-alkali stress resulted in nitrosative damage, which was alleviated by S-nitrosoglutathione reductase (GSNOR). Moreover, saline-alkali stress-triggered NO stimulated caffeic acid O-methyltransferase (COMT) transcription and melatonin biosynthesis to scavenge excess NO and alleviate nitrosative damage at the proteome level. Under saline-alkali stress, plasma membrane-localized H+-ATPase 2 (HA2) was S-nitrosylated at Cys206, impairing its interaction with 14-3-3 protein 1 (TFT1). HA2 S-nitrosylation resulted in reduced HA activity, H+ efflux, and saline-alkali tolerance. Conversely, COMT-generated melatonin alleviated HA2 S-nitrosylation, recovering its function and tomato saline-alkali tolerance. Therefore, we propose that melatonin and NO are redox switches of HA2 S-nitrosylation for saline-alkali tolerance. Under natural saline-alkali conditions, tomato productivity was improved by grafting with COMT-, GSNOR-, or HA2-overexpression rootstocks, or by generating nonnitrosylated HA2C206S mutants. By establishing the melatonin-NO-HA2 module, this study illuminates a molecular function of melatonin and suggests possible genetic engineering strategies to improve agriculture.