The Key Targets of NO-Mediated Post-Translation Modification (PTM) Highlighting the Dynamic Metabolism of ROS and RNS in Peroxisomes

Abstract

Nitric oxide (NO) has been firmly established as a key signaling molecule in plants, playing a significant role in regulating growth, development and stress responses. Given the imperative of sustainable agriculture and the urgent need to meet the escalating global demand for food, it is imperative to safeguard crop plants from the effects of climate fluctuations. Plants respond to environmental challenges by producing redox molecules, including reactive oxygen species (ROS) and reactive nitrogen species (RNS), which regulate cellular, physiological, and molecular processes. Nitric oxide (NO) plays a crucial role in plant stress tolerance, acting as a signaling molecule or free radical. NO is involved in various developmental processes in plants through diverse mechanisms. Exogenous NO supplementation can alleviate the toxicity of abiotic stresses and enhance plant resistance. In this review we summarize the studies regarding the production of NO in peroxisomes, and how its molecule and its derived products, (ONOO^-) and S-nitrosoglutathione (GSNO) affect ROS metabolism in peroxisomes. Peroxisomal antioxidant enzymes including catalase (CAT), are key targets of NO-mediated post-translational modification (PTM) highlighting the dynamic metabolism of ROS and RNS in peroxisomes.

Keywords: H2O2; S-nitrosoglutathione (GSNO); nitric oxide (NO); peroxynitrite (ONOO−), post-translational modification (PTM); reactive nitrogen species (RNS).

Figure 1

A proposed model for the function of the ascorbate glutathione cycle in leaf peroxisomes is derived from various experimental observations. These include studies on enzyme activity latency within intact organelles, solubilization assays using 0.2 M KCl, characterization of peroxisomal membrane polypeptides (PMPs) from pea leaves, and investigations into the NADH-dependent monodehydroascorbate reductase (MDHAR) activity in peroxisomal membranes from castor bean endosperm. The model integrates components such as ascorbate (ASC) in its reduced (ASC) and oxidized (dehydroascorbate, DHA) forms, monodehydroascorbate reductase (MDHAR), glutathione reductase (GR), reduced glutathione (GSH), oxidized glutathione (GSSG), ascorbate peroxidase (APX), and xanthine oxidase (XOD).

Figure 2

The key components involved in the process of importing the peroxisomal protein that is responsible for generating nitric oxide (NO) into the peroxisome.

Figure 3

Outline of the nitric oxide (NO)-mediated post-translational modifications alternative reactions by Trx. Proteins are represented with letter “P.” (A) The initial stage involves a nucleophilic attack on the SNO by the catalytic cysteine, which releases nitric oxide (NO) and creates a mixed disulfide intermediate. This intermediate is then reduced by the resolving thiol of Trx. (B) In the alternative reaction, the process begins with the same initial step, where NO is transferred to the catalytic thiol, resulting in the release of the reduced peptide. Following this, the bound SNO is reduced by the resolving cysteine, which subsequently releases NO.

Figure 4

The intricate interplay between nitric oxide (NO) metabolism and antioxidant enzymes within plant peroxisomes involves several key components. Peroxisomal xanthine oxidoreductase (XOR) activity generates uric acid and superoxide radicals (O₂^•−), while an _L-arginine-dependent nitric oxide synthase (NOS)-like activity produces NO. NO can react with O₂^•− to form ONOO⁻, a potent oxidant capable of inducing PTMs like tyrosine nitration. Additionally, NO can combine with GSH to yield GSNO, serving as a NO donor for S-nitrosation reactions. Uric acid, known for its ability to scavenge ONOO⁻, may contribute to a regulatory mechanism within peroxisomes. These interactions influence the activity of key peroxisomal enzymes, including CAT, CuZnSOD, and MDAR, potentially leading to their inhibition.