Plant peroxisomes: A nitro-oxidative cocktail

Abstract

Although peroxisomes are very simple organelles, research on different species has provided us with an understanding of their importance in terms of cell viability. In addition to the significant role played by plant peroxisomes in the metabolism of reactive oxygen species (ROS), data gathered over the last two decades show that these organelles are an endogenous source of nitric oxide (NO) and related molecules called reactive nitrogen species (RNS). Molecules such as NO and H₂O₂ act as retrograde signals among the different cellular compartments, thus facilitating integral cellular adaptation to physiological and environmental changes. However, under nitro-oxidative conditions, part of this network can be overloaded, possibly leading to cellular damage and even cell death. This review aims to update our knowledge of the ROS/RNS metabolism, whose important role in plant peroxisomes is still underestimated. However, this pioneering approach, in which key elements such as β-oxidation, superoxide dismutase (SOD) and NO have been mainly described in relation to plant peroxisomes, could also be used to explore peroxisomes from other organisms.

Keywords: Hydrogen peroxide; Nitric oxide; Peroxisomes; Peroxynitrite; Reactive nitrogen species; Reactive oxygen species.

Graphical abstract

Fig. 1

Images illustrating CLSM in vivo detection of nitric oxide (NO) and peroxynitrite (green), peroxisomes (red) and chloroplasts (blue) in guard cells of transgenic Arabidopsis seedlings expressing CFP-PTS1. A and E, fluorescence punctates (red) attributable to CFP-PTS1, indicating the localization of peroxisomes in guard cells. B and F, fluorescence punctates (green) attributable to the detection in the same guard cells of nitric oxide and peroxynitrite, respectively. C and G, chlorophyll autofluorescence (blue) attributable to the detection of chloroplasts. D and H, merged images for corresponding panels.

Fig. 2

Model of NO and H₂O₂ metabolism in plant peroxisomes.L-Arginine nitric oxide synthase (NOS)-like activity generates NO which can react with reduced glutathione (GSH) in the presence of O₂ to form S-nitrosoglutathione (GSNO). This metabolite can interact with SH-containing proteins by a process of S-nitrosylation affecting their function. NO can also react with superoxide radicals (O₂^·-) to generate peroxynitrate (ONOO^-) which can mediate a process of tyrosine nitration of proteins. Alternatively, either NO or GSNO can be released to the cytosol to participate in signaling cascades, although the S-nitrosoglutathione reductase (GSNOR) could modulate the GSNO release. Hydrogen peroxide (H₂O₂) is produced by different biochemical pathways. Additionally, the superoxide radical (O₂^·-) generated by some enzymes such as xanthine oxidase (XOD) which is part of purine metabolism can dismutate into H₂O₂ by the enzyme superoxide dismutase (SOD). The level of peroxisomal H₂O₂ is controlled either by catalase located in the matrix or by the membrane bound ascorbate peroxidase (APX), and its release to the cytosol could be through putative aquaporins.