PHYSIOLOGIA PLANTARUM 119: 355–364. 2003 Copyright # Physiologia Plantarum 2003 Printed in Denmark – all rights reserved Redox sensing and signalling associated with reactive oxygen in chloroplasts, peroxisomes and mitochondria Christine H. Foyera,* and Graham Noctorb aCrop Performance and Improvement Division, Rothamsted Research, Harpenden, Hertfordshire AL5 2JQ, UK bInstitut de Biotechnologie des Plantes, Baˆtiment 630, Universite´ Paris XI, 91405 Orsay Cedex, France *Corresponding author, e-mail: [email protected] Received 4 February 2003; revised 19 May 2003 Chloroplasts and mitochondria are the powerhouses of photo- electron transport processes with the inherent generation of synthetic cells. The oxidation-reduction (redox) cascades of superoxide, hydrogen peroxide and singlet oxygen provides a the photosynthetic and respiratory electron transport chains repertoire of additional extremely powerful signals. Accumu- not only provide the driving forces for metabolism but also lating evidence implicates the major redox buffers of plant generate redox signals, which participate in and regulate every cells, ascorbate and glutathione, in redox signal transduction. aspect of plant biology from gene expression and translation The network of redox signals from energy-generating organ- to enzyme chemistry. Plastoquinone, thioredoxin and reactive elles orchestrates metabolism to adjust energy production to oxygen have all been shown to have signalling functions. utilization, interfacing with hormone signalling to respond to Moreover, the intrinsic involvement of molecular oxygen in environmental change at every stage of plant development. Introduction All living organisms are oxidation–reduction (redox) transduction arose around this central core. These sig- systems. They use anabolic, reductive processes to store nals exert control on nearly every aspect of plant biology energy and catabolic, oxidative processes to release it. from chemistry to development, growth and eventual Through photosynthesis, plants set this global wheel in death. Controlled production of reactive oxygen species motion. By harnessing light energy to drive biochemistry, (ROS) acts as a second messenger, alongside other medi- photosynthetic organisms have perfected the art of redox ators such as calcium, not only in plant responses to control. Redox signals are the most fundamental forms pathogens but also in hormone signalling (Pei et al. of information monitored by photosynthetic organisms 2000). Recent developments have greatly increased our (Noctor and Foyer 1998). These types of signals may understanding of how systems in organelles involved in well belong to the earliest evolved controls since photosynthesis sense redox changes, particularly those they prevent uncontrolled ‘boom and bust’ scenarios in linked to reactive oxygen in order to regulate whole cell energy availability, utilization and exchange. More redox homeostasis. complex aspects of redox control of physiology through regulation of gene expression developed with the The key role of reactive oxygen species and evolution of higher plants. It is now widely accepted antioxidants in plant redox homeostasis that redox signals are key regulators of plant meta- bolism, morphology and development, and it may even Photosynthetic and respiratory electron transport chains be that all intermediates and other systems of signal are the primary energy-transducing processes in eukaryotic organisms. The evolution of oxygenic photosynthesis, Abbreviations – ABA, abscissic acid; APX, ascorbate peroxidase; DHA, dehydroascorbate; GPX, glutathione peroxidase; GRX, glutaredoxin; GSH, reduced glutathione; GSSG, glutathione disulphide; GST, glutathione S-transferase; LHC, light-harvesting complex; M-POX, Mehler-peroxidase; (i)NOS, (inducible) nitric oxide synthase; PQ, plastoquinone; PRX, peroxiredoxin; PSI, photosystem I; PSII, photosystem II; ROS, reactive oxygen species; TRX, thioredoxin. Physiol. Plant. 119, 2003 355 an event that occurred two billion years ago, provided ensure control of the cellular redox state rather than to abundant oxygen and facilitated the elaboration of reac- facilitate the complete elimination of H2O2 (Foyer and tions involving O2, particularly aerobic respiration. Almost Noctor 2000). The antioxidative system determines the all life is based on the essential energy exchange reactions of lifetime of H2O2 in planta. Plant cells are strongly redox photosynthesis and respiration. The evolution of photosys- buffered and contain very large quantities of the soluble tem II first allowed use of the very high electrochemical hydrophilic antioxidants, ascorbate (10–100 mM) and potential (Em7 ¼ 1 815 mV) of the O2/H2O redox couple. glutathione (0.2–10 mM) (Noctor and Foyer 1998, Oxygenic photosynthesis and aerobic respiration today deal Hartmann et al. 2003). Most of their intracellular com- with concerted, four-electron exchange between water and partments hence have the capacity to deal with even very oxygen, without release of reactive, partially reduced inter- high fluxes of H2O2 production. Rapid compartment- mediates. However, many processes in plants (and in other specific differences in redox state (and hence signalling) organisms) catalyse only partial reduction of oxygen, and so that influence the operation of many fundamental pro- generate superoxide, H2O2, and hydroxyl radicals (Noctor cesses in plants, can be achieved by modifying ROS and Foyer 1998, Mittler 2002). In addition, a reaction (particularly H2O2) production or by repression or potentially common in the thylakoid pigment beds involves activation of antioxidant defences. Recent evidence sug- photodynamic energy transfer to ground-state triplet O2 gests that glutathione and ascorbate are key components and leads to the formation of highly reactive singlet O2. of redox signalling in plants (Baier et al. 2000, Noctor Redox signals are involved in all aspects of plant et al. 2000, Horling et al. 2003). Specific compartment- biology. They are particularly important in defence based signalling and regulation of gene expression can be responses and cross-tolerance phenomena, enabling a achieved via differential compartment-based changes in general acclimation of plants to stressful conditions. either the absolute concentrations of ascorbate and glu- H2O2 has long been recognized as a signal-transducing tathione or the ascorbate/dehydroascorbate and GSH/ molecule in the activation of defence responses in GSSG ratios, which are very high and stable in the plants. It mediates intra- and extra-cellular communica- absence of stress (Noctor et al. 2000). tion during plant reactions to pathogens and several Three factors are particularly significant in governing studies have suggested a role in systemic acquired resis- the importance of H2O2 in signalling redox status in a tance. The hypersensitive response (HR) is a widespread given compartment. The first is the absolute rate of H2O2 phenomenon that is responsible for the activation and production. Figure 1 shows rates of H2O2 production in establishment of plant immunity to disease. HR is an different compartments during photosynthesis at moder- example of plant programmed cell death as it leads ately high light and optimal temperatures. Photosynth- to rapid, localized cell death at infection sites. This esis produces superoxide as result of direct electron contributes to the limitation of the growth and spread transfer to oxygen, from which H2O2 is produced and of the invading pathogen. One of the earliest events in metabolized through the Mehler-peroxidase (M-POX) the HR is the rapid accumulation of ROS through the reaction. Assuming, however, that the M-POX reaction activation of enzyme systems, some of which are similar is not a sink for more than 10% of photosynthetic elec- to neutrophil NADPH oxidase (Keller et al. 1998). The tron flow, H2O2 is probably produced even faster in the oxidative burst is a central component of an integrated peroxisomes, at least in C3 plants, by virtue of the glycol- HR signalling system, whose function is rapid amplifica- late oxidase reaction. The second important factor is the tion of the signal. Other signalling components involved rate of scavenging by detoxifying systems. These two fac- 21 in HR are salicylic acid (SA) and cytosolic Ca .H2O2 tors are likely to be the main determinants of H2O2 con- 21 has a strong regulatory influence on fluxes through Ca centration. Third, the probability of reaction of H2O2 with channels and on Ca21 concentrations in different cellular signalling components is probably a key determinant of compartments. During HR, H2O2 is required to trigger signalling intensity. As we discuss below, early components localized host cell death but it seems that NO is in redox signalling are likely to include antioxidants and/or also needed to induce an efficient cell death response antioxidative enzymes. The influence of a given compart- (Delledonne et al. 1998). Further evidence that the ment in redox signalling may differ as a function of how H2O2 cascade interacts closely with other signalling well primed each compartment is with sensing components, systems comes from studies on hormone-mediated the nature of the signal that these components sense (e.g. stomatal movement (Pei et al. 2000), cell growth (Rodriguez H2O2 or other ROS, electron transport components, et al. 2002) and tropic responses (Joo et al. 2001). Such organic peroxides), and to what extent sensing components studies show that H2O2 is a common