Unravelling GSNOR-Mediated S-Nitrosylation and Multiple Developmental Programs in Tomato Plants

Nitric oxide (NO) impacts multiple developmental events and stress responses in plants. S-nitrosylation, regulated by S-nitrosoglutathione reductase (GSNOR), is considered as an important route for NO bioactivity. However, genetic evidence for GSNOR-mediated plant development and S-nitrosylation remains elusive in crop species. Genetic and site-specific nitrosoproteomic approach was used to obtain GSNOR-mediated phenotype and S-nitrosylated network. Knockdown of GSNOR increased the endogenous NO level and S-nitrosylation, resulting in higher germination rate, inhibition of root and hypocotyl growth, decreased photosynthesis, reduced plant growth, altered plant architecture, dysplastic pollen grains, and low fructification rate and fruit yield. For nitrosoproteomic analysis, 395 endogenously S-nitrosylated proteins with 554 S-nitrosylation sites were identified within a wide range of biological processes, especially for energy metabolism. Physiological and exogenous energy-support testing were consistent with the omic result, suggesting that GSNOR-mediated S-nitrosylation of energy metabolism plays key roles in impacting plant growth and development. Taken together, GSNOR is actively involved in the regulation of multiple developmental processes related to agronomically important traits. In addition, our results provide valuable resources and new clues for the study of S-nitrosylation-regulated metabolism in plants.