Tomato Root Growth Inhibition by Salinity and Cadmium is Mediated by S-Nitrosative Modifications of ROS Metabolic Enzymes Controlled by S-Nitrosoglutathione Reductase

Abstract

S-nitrosoglutathione reductase (GSNOR) exerts crucial roles in the homeostasis of nitric oxide (NO) and reactive nitrogen species (RNS) in plant cells through indirect control of S-nitrosation, an important protein post-translational modification in signaling pathways of NO. Using cultivated and wild tomato species, we studied GSNOR function in interactions of key enzymes of reactive oxygen species (ROS) metabolism with RNS mediated by protein S-nitrosation during tomato root growth and responses to salinity and cadmium. Application of a GSNOR inhibitor N6022 increased both NO and S-nitrosothiol levels and stimulated root growth in both genotypes. Moreover, N6022 treatment, as well as S-nitrosoglutathione (GSNO) application, caused intensive S-nitrosation of important enzymes of ROS metabolism, NADPH oxidase (NADPHox) and ascorbate peroxidase (APX). Under abiotic stress, activities of APX and NADPHox were modulated by S-nitrosation. Increased production of H2O2 and subsequent oxidative stress were observed in wild Solanum habrochaites, together with increased GSNOR activity and reduced S-nitrosothiols. An opposite effect occurred in cultivated S. lycopersicum, where reduced GSNOR activity and intensive S-nitrosation resulted in reduced ROS levels by abiotic stress. These data suggest stress-triggered disruption of ROS homeostasis, mediated by modulation of RNS and S-nitrosation of NADPHox and APX, underlies tomato root growth inhibition by salinity and cadmium stress.

Brassinosteroid enhances salt tolerance via S‐nitrosoglutathione reductase and nitric oxide signaling pathway in mangrove Kandelia obovata

“…Recently, Wang et al (2017) have shown that Al‐induced NO production may mediate Al toxicity by activating NADPH oxidase to increase ROS generation in soybean roots. Likewise, several studies have revealed that GSNOR exerts an important role in ROS homeostasis under abiotic stresses (Gong et al, 2015; Jedelská et al, 2019; Rustérucci et al, 2007). In the present study, the gene expressions of RbohD and RbohF were depressed by NO scavenger cPTIO treatment, but were increased by GSNOR inhibitor N6022 which eliminated the ROS decrease caused by EBR (Figure 6).…”

Protein S-nitrosation differentially modulates tomato responses to infection by hemi-biotrophic oomycetes of Phytophthora spp.

“…Previously, we observed that the activity of APX was significantly increased in the roots of both Solanum spp. genotypes cultivated in agar medium supplemented with GSNO or GSNOR inhibitor N6022, which was associated with increased S-nitrosation of APX 40 . In this study, the increase of GSNOR activity induced by salinity and cadmium stress in S. habrochaites and subsequent lower levels of S-nitrosothiols resulted in decreased S-nitrosation status and decreased APX activity, in contrast to stress-induced down-regulated GSNOR activity in S. lycopersicum cv.…”

“…Previously, we observed that the activity of APX was significantly increased in the roots of both Solanum spp. genotypes cultivated in agar medium supplemented with GSNO or GSNOR inhibitor N6022, which was associated with increased S-nitrosation of APX 40 .…”

Research on the Mechanisms of Plant Enrichment and Detoxification of Cadmium

“…These enzymes include superoxide dismutase (SOD), catalase (CAT), peroxidase (POD), glutathione peroxidase (GSH-Px), and ascorbate peroxidase (APX). Cd induces ROS production by stimulating NADPH oxidase activity, replacing essential cations at specific binding sites, and inhibiting enzyme activity [ 147 ].…”