Shedding light on NO homeostasis: Light as a key regulator of glutathione and nitric oxide metabolisms during seedling deetiolation

Abstract

Despite the significant impacts of light on nitric oxide (NO) levels in plants, the mechanism underlying the influence of this environmental factor on NO metabolism remains poorly understood. A critical mechanism controlling NO levels in plant cells relies on the S-nitrosylation of glutathione (GSH), giving rise to S-nitrosoglutathione (GSNO), which can be either stored or degraded depending on the cellular context. Here, we demonstrate that a strict balance is maintained between NO generation and scavenging during tomato (Solanum lycopersicum) seedling deetiolation. Given the absence of accurate methods in the literature to estimate NO scavenging in planta, we first developed a simple, robust system to continuously monitor the global in vivo NO scavenging by plant tissues. Then, using photomorphogenic tomato mutants, we demonstrated that the light-evoked de-etiolation is associated with a dramatic rise in NO content followed by a progressive increment in NO scavenging capacity of the tissues. Light-driven increments in NO scavenging rates coincided with pronounced rises in S-nitrosothiol content and GSNO reductase (GSNOR) activity, thereby suggesting that GSNO formation and subsequent removal via GSNOR might be key for controlling NO levels during seedling deetiolation. Accordingly, treatments with thiol-blocking compounds further indicated that thiol nitrosylation might be critically involved in the NO scavenging mechanism responsible for maintaining NO homeostasis during deetiolation. The impacts of both light and NO on the transcriptional profile of glutathione metabolic genes also revealed an independent but coordinated action of these signals on the regulation of key components of glutathione and GSNO metabolisms. Altogether, these data indicated that GSNO formation and subsequent removal might facilitate maintaining NO homeostasis during light-driven seedling deetiolation.