Defining robust redox signalling within the context of the plant cell

Over the last 25 years, the concept that the reactive oxygen species (ROS) and the reactive nitrogen species (RNS) are key signalling molecules that facilitate a plethora of adaptive metabolic, molecular genetic and epigenetic responses has become established in the literature (Foyer & Noctor 2005). However, the notion that cells exploit highly reactive and potentially harmful species to drive life-promoting changes in gene expression still rests uneasily on the shoulders of earlier ideas such as oxidant-induced damage and cell death, as well as the ever-popular free radical theory of ageing. However, high reactivity, and hence characteristic instability, may be crucial to the success of ROS and RNS as versatile signalling molecules. Successful signalling cascades may be fundamentally dependent on the high abundance of reactive but relatively short-lived interacting molecules that can either directly or indirectly (e.g. through thiol intermediates) alter protein structure or function via at least partially reversible mechanisms. In fact, ROS and RNS may be viewed as a paradigm for successful intercellular and intracellular molecular communication. Environmentally and developmentally triggered redox cues intermesh tightly with hormonal signals to afford plants the flexibility required to respond to a wide range of conditions. In this way, redox-driven metabolism, once considered a routine housekeeping function that merely provided the backdrop to sophisticated signalling networks, is now recognized as a cornerstone of cellular control modules. This startling paradigm shift has arisen despite a significant and ongoing vacuum in our knowledge of the underpinning mechanisms. A set of discrete locations defines specificity in redox signalling in different compartments of the plant cell. Independent control and buffering permit redox-sensitive signal transduction to occur in locations such as the thylakoid lumen and the apoplast/cell wall and across the membranes that separate these compartments from the highly redox-buffered spaces such as the stroma and cytosol. In these locations, a potent antioxidative system dictates a much higher threshold for the transmission of ROS signals. The synthesis of many important plant hormones, such as abscisic acid, jasmonic acid, salicylic acid and strigolactones, begins in the chloroplast. It is perhaps not fortuitous that the key steps in the synthesis of hormones that regulate plant growth and defence are located in close proximity to the signal-transducing photosynthetic electron transport system. This is undoubtedly important to allow synergistic co-activation of non-specific stress-responsive pathways that cross biotic–abiotic stress boundaries. Such interactions enable plants to maximize productivity under optimal conditions while regulating growth and development in stress conditions. The present volume is firmly anchored within the context of current concepts that ROS, RNS and redox processes are at the heart of integrated signalling networks. The content includes two papers on ROS interactions with hormones in seed germination (El-Maarouf-Bouteau et al. 2014; Oracz & Karpinski 2014), one on the role of auxin signalling in counteracting hydrogen peroxide-induced cell death (Kerchev et al. 2014) and a stimulating discussion of the interactions between the oxidative signals generated by ozone exposure and plant responses through the hormone signalling network (Vainonen & Kangasjarvi 2014). While Scharfenberg et al. (2014) focus on the role of proteins that regulate iron availability, key factors in oxidative stress, the possible mechanisms of ROS-dependent signalling are explored in relation to exposure to cryptogein (Kulik et al. 2014) and ultraviolet light (Wituszynska et al. 2014). Two authoritative and timely reports focus on the general mechanisms of redox control involving, on the one hand, regulation at the translational level in response to paraquat treatment (Benina et al. 2014) and, on the other hand, the expression of thiol-regulating proteins in plants (Belin et al. 2014). The roles of the two major redox buffers, ascorbate and glutathione, are not overlooked. While Sultana et al. (2014) describe the influence of ascorbate content on the cell wall glycoproteome, an emerging area of study, Schnaubelt et al. (2014) report on the importance of glutathione-mediated gene expression in the regulation of the cell cycle and its interactions with auxin-mediated processes. Future progress in this area will depend on the exploitation of new technologies to overcome current bottlenecks. It will also be crucial to incorporate an innovative vision of the nexus of control that places redox processes at the heart of plant cell function. It is our hope that the present special issue will make a useful contribution to this goal.