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Review
, 116 (4), 475-85

Peroxisomes Sense and Respond to Environmental Cues by Regulating ROS and RNS Signalling Networks

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Review

Peroxisomes Sense and Respond to Environmental Cues by Regulating ROS and RNS Signalling Networks

L M Sandalio et al. Ann Bot.

Abstract

Background: Peroxisomes are highly dynamic, metabolically active organelles that used to be regarded as a sink for H2O2 generated in different organelles. However, peroxisomes are now considered to have a more complex function, containing different metabolic pathways, and they are an important source of reactive oxygen species (ROS), nitric oxide (NO) and reactive nitrogen species (RNS). Over-accumulation of ROS and RNS can give rise oxidative and nitrosative stress, but when produced at low concentrations they can act as signalling molecules.

Scope: This review focuses on the production of ROS and RNS in peroxisomes and their regulation by antioxidants. ROS production is associated with metabolic pathways such as photorespiration and fatty acid β-oxidation, and disturbances in any of these processes can be perceived by the cell as an alarm that triggers defence responses. Genetic and pharmacological studies have shown that photorespiratory H2O2 can affect nuclear gene expression, regulating the response to pathogen infection and light intensity. Proteomic studies have shown that peroxisomal proteins are targets for oxidative modification, S-nitrosylation and nitration and have highlighted the importance of these modifications in regulating peroxisomal metabolism and signalling networks. The morphology, size, number and speed of movement of peroxisomes can also change in response to oxidative stress, meaning that an ROS/redox receptor is required. Information available on the production and detection of NO/RNS in peroxisomes is more limited. Peroxisomal homeostasis is critical for maintaining the cellular redox balance and is regulated by ROS, peroxisomal proteases and autophagic processes.

Conclusions: Peroxisomes play a key role in many aspects of plant development and acclimation to stress conditions. These organelles can sense ROS/redox changes in the cell and thus trigger rapid and specific responses to environmental cues involving changes in peroxisomal dynamics as well as ROS- and NO-dependent signalling networks, although the mechanisms involved have not yet been established. Peroxisomes can therefore be regarded as a highly important decision-making platform in the cell, where ROS and RNS play a determining role.

Keywords: Antioxidants; RNS; ROS; arabidopsis; autophagy; nitric oxide; nitrosative stress; oxidative stress; peroxisomes; photorespiration; reactive nitrogen species; reactive oxygen species; signalling; β-oxidation.

Figures

F<sc>ig</sc>. 1.
Fig. 1.
Electron micrograph of arabidopsis leaves showing a close relationship between chloroplasts, mitochondria and peroxisomes. Schemes showing H2O2 production in the reaction of glycolate oxidase (GOX) during photorespiration involving chloroplasts, peroxisomes and mitochondria (yellow) and H2O2 production associated with acyl CoA oxidase (ACX) activity from fatty acid β-oxidation (blue; chloroplasts and peroxisomes). C, chloroplast; ER, endoplasmic reticulum; M, mitochondria; P, peroxisome; pg, plastoglobuli; V, vacuole. Scale bar = 1 µm.
F<sc>ig</sc>. 2.
Fig. 2.
Schematic overview of the signalling networks involving ROS and RNS in peroxisomes. H2O2 and O2.– are produced in different metabolic pathways and in a small electron transport chain associated with the membrane and their steady state is regulated by SODs, catalase, the ASC–GSH cycle and probably peroxiredoxin (PRX). ROS, particularly H2O2, can diffuse to the cytosol were they can alter redox homeostasis and regulate gene transcription in the nucleus, giving rise to acclimatization or cell death depending on the stimuli. Light can regulate photorespiratory peroxisome-dependent changes in cytosolic redox homeostasis that cause SA-dependent lesions and induction of pathogenesis-related proteins. This process is dependent on SA and can also be regulated by PP2A-B’γ and Phy A. In addition, peroxisomes are a source of hormones, such as JA and IAA, that participate in the network regulating cell responses to stress (i.e. IAA, which negatively regulates light-dependent cell death). NO is produced in peroxisomes by a NOS-like activity, although other sources can also be involved, such as xanthine oxidase (XOD) and polyamines. ONOO and GSNO are produced in peroxisomes by reaction of NO with O2.– and GSH, respectively, and can also act as signal molecules regulating gene expression and protein activity throughout post-translational modifications (PTMs) such as nitration and S-nitrosylation. Oxidized peptides may also regulate gene expression and autophagy in order to control homeostasis and peroxisomal quality. Peroxisomal ROS promote cross-talk with mitochondria and chloroplasts, probably through changes in the redox state of each organelle. ATGs, autophagy-related genes; CAT, catalase; Cyt P450, cytochrome P450 reductase; GST, glutathione-S-transferase; HSPs, heat shock proteins; IAA, indoleacetic acid; JA, jasmonic acid; MDAR, monodehydroascorbate reductase; NADPH-DH, NADPH dehydrogenases; NOS-L, NO synthase-like activity; ONOO, peroxynitrite; PRX, peroxiredoxin; PEX, peroxins; Phy A, phytochrome A; PP2A-B’γ, 2A protein phosphatase subunit; PRs, pathogenesis-related proteins; SAOX, sarcosin oxidase; SO, sulphite oxidase; TFs, transcription factors; UO, urate oxidase.

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