Oxidative stress: antagonistic signaling for acclimation or cell death?

Severe environmental stress imposed on plant tissues induces changes in oxygen (O2) metabolism that cause oxidative stress. Oxidative stress occurs when reactive oxygen species (ROS) are not rapidly scavenged and the rate of repair of damaged cell components fails to keep pace with the rate of damage. If this situation persists, irreversible damage results in a loss of physiological competence and eventual cell death. However, ROS production in leaves resulting from moderate environmental stresses, within the adaptive range of the plant, also has important local and systemic signaling roles. In these circumstances, ROS production induces defense mechanisms that protect the plant but do not result in oxidative stress. We shall illustrate ROS involvement in signaling in both of these situations by considering the role of chloroplasts in initiating cellular responses to environmental perturbations, choosing examples where this organelle interacts with specific signaling pathways. It is perhaps helpful to use a stress-strain response diagram, commonly used in mechanics, to illustrate the possible relationships between increasing imposition of environmental stress, physiological perturbations, ROS production, oxidative stress, and cell death (Fig. 1). Moderate environmental stresses on leaves can result in increased rates of ROS production and physiological changes that are reversible when the stress is removed. With increasing stress, the rate of ROS production increases and oxidative stress and irreversible damage occur, which, if sufficiently great, eventually lead to cell death. Identification of the factors that set the threshold at which a cell or tissue makes the transition from successful acclimation/ resistance to oxidative stress-induced cell death is critical. However, such outcomes should not be regarded as a success (for acclimation) or a failure (for death). This may be so from a cellular perspective, but at the level of the organ or organism the processes of cell death and acclimation are inextricably linked, and both are essential for a successful response to environmental change. This may explain why many studies show that oxidative stress-induced cell death is under genetic control and not simply a consequence of ROS toxicity. Plant cells have evolved the ability to actively move up or down the curve shown in Figure 1 by regulating the balance between acclimation and cell death responses.