Peroxisomes as redox-signaling nodes in intracellular communication and stress responses

Redox compartmentalization in organelles is an effective evolutionary strategy (Box 1; Jones and Go, 2010). From an evolutionary perspective, peroxisomes, originating from the endoplasmic reticulum (ER), were selected to house a range of metabolic pathways involving the production of certain reactive oxygen species (ROS) such as H2O2 to avoid toxicity to other organelles such as mitochondria (Gabaldon, 2018). Peroxisomes play a diverse range of roles in cell functionality and in the perception of and responses to changes in their environment (Sandalio and Romero-Puertas, 2015; Lismont et al., 2019). The range of functions associated with plant peroxisomes has increased considerably over the last two decades (Table 1). As most of these pathways produce ROS and nitric oxide (NO), disturbances in these metabolic processes trigger transitory changes in ROS/reactive nitrogen species (RNS) production. These changes regulate peroxisomal metabolism, leading to peroxisome-dependent signaling and organelle crosstalk, which triggers specific cell responses (Sandalio and Romero-Puertas, 2015). The biosynthesis of phytohormones jasmonic acid (JA), auxin IAA, and salicylic acid (SA) associated with the b-oxidation pathway contributes to the complex role of peroxisomes in development and stress responses (Kao et al., 2018; Figure 2A). Peroxisomes dynamically regulate their number, shape, and protein content in response to changing environmental conditions and remain in close contact with other subcellular compartments such as mitochondria and chloroplasts (Sandalio and Romero-Puertas, 2015; Shai et al., 2016; Sandalio et al., 2020). Peroxisomes play a key role in the evolution of the metabolic networks of photosynthetic organisms by connecting oxidative and biosynthetic pathways operating in different compartments. This review updates our knowledge of peroxisomal redox homeostasis and the role of ROS and NO in the functionality, biogenesis and abundance of these organelles, as well as their role as redox hubs in metabolic regulation, signaling, and organelle crosstalk.