Understanding Oxidative Stress and Antioxidant Functions to Enhance Photosynthesis

Abstract

Photosynthesis is a well-established source of reactive oxygen species (ROS) in plants. The photosynthetic electron transport chain (PET) operates in an aerobic environment; thus, regulatory systems are required to minimize ROS production. Moreover, an efficient antioxidant network is also essential in order to process ROS effectively and to maintain intracellular ROS pools at low levels. The importance of the antioxidant network in maintaining high rates of photosynthesis has been demonstrated in many studies using molecular genetics approaches to either disable antioxidant enzymes or boost their activities or alter the abundance of low-M r molecular antioxidants such as ascorbate (AsA) and reduced glutathione (GSH). However, such studies have often failed to take into account the photosynthetic production of reductants and oxidants within the context of cellular redox homeostasis and redox signaling. Our understanding of the interactions of redox signaling pathways with photosynthesis has greatly increased in recent years, and this provides new opportunities for enhancing photosynthesis particularly under conditions that favor cellular oxidation. Here, we consider current concepts of oxidative stress and oxidative signaling in relation to photosynthesis, and we discuss whether ROS-scavenging systems have evolved to be “leaky” in order that ROS can function as a useful signaling system. The field of redox biology has recently witnessed a dramatic reappraisal of the importance of ROS. Due to the reactivity of ROS and because they are unavoidable by-products of oxygenic photosynthesis, only the more negative aspects of ROS generation are often considered in relation to observations. Thus, light-driven ROS production is generally described as harmful because it has the potential to cause irreversible damage to photosynthetic components. It is generally often suggested that ROS production should be minimized at all costs. However, despite their potential for causing harmful oxidations, it is now well established that ROS are also powerful signaling molecules that are involved in the control of plant growth and development as well as priming acclimatory responses to stress stimuli (Jones, 2006; Foyer and Noctor, 2005a, 2005b, 2009). In many studies involving photosynthetic ROS generation, the signaling function of these powerful metabolites is largely ignored, and interpretations are all too frequently based solely on the notion that ROS exert their principal effects through chemical toxicity and their abilities to cause damage. Within this context, the term “oxidative stress” has become largely synonymous with “oxidative damage” to cellular components, particularly in situations where oxidative inactivation exceeds that of repair or replacement. Furthermore, it is often suggested that the accumulation of damaged cellular components and associated loss of function leads to cell death, but the mechanisms that cause cell death in this case are generally vague or undefined. Relatively few studies to date have considered photosynthetic ROS generation in the context of the light-driven production of powerful signaling molecules, whose abundance provides essential information to the cell concerning imbalances between energy-generating and energy-utilizing processes in the PET system. Within this context, increased ROS production leading to enhanced oxidation in high light may be considered to be a powerful signal that not only decreases PSII activity but also stimulates gene expression, particularly with regard to acclimation and defense genes. While concepts of ROS function in signaling or damage in photosynthesis are largely irrelevant to the description of the basic biochemical mechanisms by which ROS oxidize cellular components, the philosophical choice between “damage” and “signaling” in data analysis remains crucial to the evaluation of the physiological significance of these mechanisms. Oxygenic photosynthesis is a dynamic and flexible process that powers life on earth, in which water oxidation on the lumen side of PSII is an indispensable step. The light-driven PET system drives electrons from water through to NADP, generating the proton gradient that facilitates ATP synthesis. Intriguingly, a key feature of PSII is its vulnerability to light-induced damage, which is considered to be a consequence of the production of singlet oxygen (Vass and Cser, 2009) in the PSII reaction center, leading to irreversible oxidation of the D1 protein (Krieger-Liszkay et al., 2008). This sensitivity means that the PSII reaction center has to be rebuilt about once every 30 min even under relatively low irradiances. The damage and repair process thus occurs under all light intensities. A limitation of the PET system only occurs when the rate of damage exceeds that of repair, and this makes a major contribution to the processes called photoinhibition (Vass and Aro, 2008). In many circumstances where the rate of damage is fast, su