Melatonin relieves the S-nitrosylation of plasma membrane H+-ATPase 2 to enhance saline-alkali tolerance in tomato

Abstract

Abstract Soil salinity-alkalinity is a global problem with special relevance to land resources. Although melatonin confers multiple tolerances to plants, its role in saline-alkali tolerance remains unclear. Here, we found that excess nitric oxide (NO) accumulation accounts for saline-alkali stress by genetically manipulating the NO metabolic enzyme of S-nitrosoglutathione reductase (GSNOR). A caffeic acid O-methyltransferase (COMT) was identified to enhance melatonin synthesis and NO scavenging to improve saline-alkali tolerance. As a target protein participating in saline-alkali tolerance, plasma membrane H+-ATPase 2 (HA2) was identified to be S-nitrosylated at Cys206. Further, the S-nitrosylation of HA2 was induced by saline-alkali stress, and was aggravated by GSNOR-knockdown, but was alleviated by COMT-overexpression. The S-nitrosylation of HA2 at Cys206 suppressed its interaction with 14-3-3 protein 1 (TFT1), culminating in the inhibition of its enzymatic activity and saline-alkali tolerance. Under physiological status, melatonin and NO jointly act as a redox switch of HA2 to regulate root H+ and Na+ efflux to affect saline-alkali tolerance. Thus, the COMT-, GSNOR-, and HA2-transgenic grafting significantly improved tomato productivity in natural saline-alkali soil. Together, this study unravels the molecular basis of the melatonin-NO-HA2 module and provides effective solution to agricultural applications.