Understanding Oxidative Stress and Antioxidant Functions to Enhance Photosynthesis
Year: 2010
Type: article
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, such as at high light intensities, the rate of repair is also rapid (Ohad et al., 1984), so a high level of PSII activity can be maintained. It is widely accepted that efficient regulation of PET serves to minimize the production of singlet oxygen at PSII as well as the generation of superoxide and hydrogen peroxide (H2O2), which occurs predominantly on the reducing side of PSI (Genty and Harbinson, 1996). Within this context, reversible decreases in the efficiencies of both photosystems are intrinsic to the regulation of light use by photosynthesis (Genty and Harbinson, 1996). Inherent limitations on the capacity for electron transport through the cytochrome b 6/f complex favor overreduction of PSII, which exacerbates PSII turnover (Genty and Harbinson, 1996; Vass and Cser, 2009). Of the strategies that can be employed to protect PSII under conditions of limiting PET capacity, the most important is nonphotochemical quenching (NPQ), which dissipates the excitation energy of chlorophyll a molecules safely as heat (Niyogi et al., 1998). The majority of electron flow follows a linear, noncyclic route from water through PSII, the cytochrome b 6/f complex and PSI to NADP, leading to the generation of both NADPH and ATP. However, the operation of a cyclic electron flow pathway around PSI provides a mechanism whereby ATP production can be increased relative to NADPH. The operation of cyclic electron flow is also considered to prevent overreduction of the acceptor side of PSI (Munekage et al., 2008). This is important because superoxide and H2O2 are generated by PET components on the acceptor side of PSI. Cyclic electron flow may also help to limit singlet oxygen production at PSII because it enhances protonation in the lumen, which triggers protective NPQ mechanisms (Rumeau et al., 2007). The exact contribution of the linear and cyclic pathways to overall electron flow depends on cell type and environmental conditions. However, in C3 leaves under optimal growth conditions, the major function of cyclic electron flow around PSI is considered to be the augmentation of ATP production relative to NADPH in order to balance the energy budget of the chloroplast. While many fundamental questions remain concerning the components involved in cyclic electron flow and the extent to which this pathway operates in C3 plants, there is a general consensus of opinion that cyclic electron flow is an essential component of the repertoire of chloroplast mechanisms that serve to coordinate energy metabolism and balance redox status. A further mechanism of regulation for photosynthesis that prevents overreduction of the PSI acceptor side and the chloroplast stroma is the “malate valve” system, which transfers reducing equivalents to the cytosol (Scheibe et al., 2005). This pathway, which is activated by the thioredoxin (TRX)-regulated activation of chloroplastic NADP-dependent malate dehydrogenase, is an essential component for the stromal redox homeostasis network because it allows the export of excess reducing power and thus relieves electron pressure in the chloroplast. In this way, the regulation of metabolite distribution can be used to balance cellular redox status in order to achieve metabolic and photosynthetic control. However, to date, little attention has been paid to how the regulated distribution of other metabolites, particularly antioxidants, may alter the stromal redox homeostasis network and affect the regulation of photosynthesis. Photosynthesis is an important source of cellular oxidants (Foyer and Noctor, 2003). Even under optimal conditions, the calculated rate of H2O2 formation by the PET chain in the chloroplasts during photosynthesis in C3 leaves is nearly as high (4 μmol m–2 s–1) as the amount produced in the peroxisomes as a result of the glycolate oxidation in the photorespiratory pathway (10 μmol m–2 s–1; Foyer and Noctor, 2003). While it is often stated that the amount of H2O2 in chloroplasts can increase by several orders of magnitude during stress, such notions must be viewed with caution because of the inherent complexities of obtaining accurate measurements of H2O2 contents in intact tissues and isolated organelles (Queval et al., 2008). Current methods do not allow accurate estimations of the H2O2 concentration of the stroma under either optimal or stress conditions. Regardless of any uncertainties about absolute values for H2O2 levels in photosynthetic tissues, it has long been recognized that H2O2 is a potent inhibitor of photosynthesis, because even at low concentrations (10 μm) it can inhibit CO2 fixation by 50% because of the oxidation of the thiol-modulated enzymes of the Calvin cycle. Therefore, the balance between ROS production and ROS scavenging in chloroplasts is delicate and must be strictly controlled. AsA and GSH are the most abundant and best characterized water-soluble antioxidants in plants, and they accumulate to millimolar concentrations in chloroplasts. Although these metabolites scavenge ROS separately, they have long been considered to function together in the AsA-GSH cycle (Foyer and Halliwell, 1976) and the water-water cycle (Asada, 1999) to metabolize H2O2 (Fig. 1) and to dissipate excess excitation energy in chloroplasts. AsA-dependent (AsA-GSH cycle; right) and TRX-dependent (TRX/GPX; left) pathways of H2O2 removal in chloroplasts. Fd, Ferredoxin; FNR, ferredoxin NADPH reductase; FTR, ferredoxin thioredoxin reductase; MDAR, MDA reductase. The reduction of ground-state molecular oxygen to superoxide on the acceptor side of PSI in the Mehler reaction is the first step of a series of reactions that together has been called “the water-water cycle” (Asada, 1999). This incorporates superoxide dismutase (SOD), ascorbate peroxidase (APX), and the AsA-GSH cycle (Fig. 1) in a mechanism that builds up the transthylakoid proton gradient and facilitates ATP formation at the expense of NADPH and reductant (Asada, 1999). APX utilizes AsA as a specific electron donor to reduce H2O2 to water with the concomitant generation of monodehydroascorbate (MDA), a univalent oxidant of AsA. While MDA is spontaneously converted to AsA and dehydroascorbate (DHA), it is also rapidly reduced to AsA by the action of a NAD(P)H-dependent MDA reductase. DHA reductase (DHAR) utilizes GSH to reduce DHA and thereby regenerate AsA. GSH is then regenerated from oxidized glutathione, also called glutathione disulfide (GSSG), by the action of glutathione reductase (GR) using NAD(P)H. While different APX and SOD isoforms are located in the stroma and thylakoid membrane, the chloroplastic GR and DHAR enzymes are localized in the stroma. A characteristic property of APX, particularly the chloroplastic APX forms, is their susceptibility to oxidative inactivation in the absence of AsA (Ishikawa and Shigeoka, 2008). Under low AsA concentrations (less that 20 μm), the activity of chloroplastic APXs is rapidly lost in the presence of H2O2, with a half-inactivation time of less 30 In the and APXs only activity more The chloroplastic APXs are the for inactivation chloroplast AsA accumulation is of chloroplast AsA and inactivation of chloroplast have been considered as limitations of photosynthetic in stress conditions (Ishikawa and Shigeoka, and thus potential for In to the AsA-GSH other that are important in chloroplast ROS are particularly and glutathione peroxidase and which function together with and in the chloroplasts The mechanism used by to reduce H2O2 of a by that can a of electron such as and AsA. can use both GSH and as reducing and they can as well as H2O2 et al., is a more efficient GSH and their high rates of TRX-dependent peroxidase plant have been to the protein et al., In the system, the of reduced is to the PET chain through either or While the rates of plant and their for H2O2 are low with APX, the and pathways an pathway to the water-water cycle in the light (Fig. particularly the AsA-GSH cycle is However, are also efficient for the chloroplast The of which the may be as important as H2O2 in of maintaining optimal photosynthetic in the AsA-GSH cycle and the pathways may be important in and serve Our is that the pathways are to specific in defense metabolism and that their relative importance to the environmental conditions. The that chloroplastic MDA and APXs are enhanced in with et al., that regulatory mechanisms between the so that pathway may be enhanced to for in the other of interactions between the AsA-GSH pathway and the between the pathways of the chloroplasts. The AsA-GSH pathway has a for H2O2 and the chloroplast APX has activities but the have a reactive such as values for the efficiencies for plant with H2O2 between and with a of with In the for AsA-dependent H2O2 reduction is (Asada, 1999). is an important plant signaling rapidly with the superoxide to It is that is produced in where it may signaling Moreover, in to the in not to be to plants, which to function even in the presence of high levels of this A key feature of the regulation of metabolism is its reaction with GSH to which can then with other to et al., 2005). serves as a of and also as signaling protein can both protein function and activity et al., While the AsA-GSH cycle operates largely within the it is also to the of a which is in its reduced by AsA. and are the most abundant of antioxidants in chloroplasts and is to high concentrations in where it serves to prevent by removal of singlet oxygen and (Krieger-Liszkay et al., 2008). The are reduced to by AsA and the action of the AsA-GSH cycle. The that are in a accumulation of AsA and In plants, which accumulate have AsA and GSH levels et al., 2005). further of the that between chloroplast antioxidants, which for Moreover, these data not only the high of between the chloroplast antioxidant pathways but also that there are of control. However, the pathways for AsA et al., GSH and and and are now well remains to be how the and accumulation of these essential antioxidants is and regulated in a The that control the intracellular of metabolites between the different of the cell and the antioxidant transport systems are of importance to the overall regulation of photosynthesis and its operation a of environmental conditions. While recent have witnessed an increase in understanding of the of ROS in the signaling systems that coordinate antioxidant gene expression, little information is to date on how the low-M r antioxidants in this control. A of molecular genetics and have been used to the of to stress and have been the to protect photosynthesis by of component antioxidant and an that enhancing the capacity of the water-water cycle through the of and can the of to stress et al., the of chloroplast antioxidant has to be of the most of plant from stress (Ishikawa and Shigeoka, et al., 2009). studies that that an of antioxidant capacity to photosynthesis the that there is not an excess capacity for ROS in the chloroplasts. such that the capacity for ROS in the chloroplasts is with regard to ROS production. This is the susceptibility of the photosynthetic processes to oxidative However, that ROS generated in photosynthesis in a redox signaling then the importance of regulation of both ROS abundance and the of the ROS signal The data that ROS pathways are not in that all the ROS from the cellular there to be a level of between ROS and processes that allows a of ROS to in the cellular This coordinate regulation allows in the ROS to during stress, for signaling The of the ROS signaling on the relative rates of ROS production and the of which can be with regard to activation and gene In this context, the balance between oxidant production and removal by the antioxidant system the and of the ROS as in In the oxidation of pathways of gene expression, oxidation of other such as in the PSII reaction center further a mechanism that more rapid of PSI and PSII to environmental conditions. to specific is a and generally accepted mechanism of for A of the interactions between cellular redox and photosynthesis within the context of plant stress responses and interactions with signaling oxidation can to either cell death or enhanced on the of the oxidative signal and the of the signaling pathway that is Within the context of the “oxidative damage” the of photosynthesis during stress that has been by enhancing the chloroplast antioxidant network provides that it is to harmful reactions by enhanced oxidative et al., and thylakoid APX in the chloroplasts enhanced to high light and a that is to stress (Ishikawa and Shigeoka, 2008). a gene an in the in a greatly enhanced to stress et al., In this the enhanced in of for the inactivation of chloroplastic APXs by The physiological significance of the high susceptibility of chloroplastic APXs to inactivation by ROS remains a only the potential for increased damage. However, from a signaling the inactivation of chloroplastic APXs may have a regulatory in redox signaling pathways under conditions of high ROS production or oxidative of useful from into the chloroplasts of has also to be at enhancing to the of are to reduce using NADPH as an electron but not GSH and The of in chloroplasts in a of photoinhibition and an increased to stress et al., Moreover, the of a which is with in chloroplasts enhanced to a of et al., 2008). are considered to prevent electron and thus to the stress by reducing the of ROS formation et al., 2008). The described the importance of the enzymes in chloroplasts and the of enhanced antioxidants and other defense as a mechanism for photosynthesis in stress metabolites can also serve protective in chloroplasts. such as and which often accumulate to high can also as antioxidants and function as in plant However, they from and as such molecules are generally as a result of oxidation and be and key enzymes in the of and increased levels of these and enhanced to enhanced oxidation by to and stress et al., 2008). Thus, these can function to protect plant from oxidative damage et al., 2008). it is well established that the enhanced of an the of to of stress and 2008). While not scavenge ROS H2O2 that ROS-scavenging enzymes and thus oxidation. The accumulation of to be more in the chloroplasts in the its to protect the photosynthetic and 2008). now to important for oxidative and signaling in the regulation of photosynthesis, with antioxidants such as AsA and GSH signaling (Foyer and Noctor, 2009). While of the antioxidant network has that of antioxidant components has a negative on photosynthesis, a of studies have demonstrated that concerning ROS and antioxidants are and in of either or APX has a general negative that are in both and APX a less the et al., Thus, whether the and action of ROS and antioxidants associated with photosynthesis are often most described within the of damage or these metabolites are of the more complex cellular system that cell in of cell death or enhancing to to the of and et al., it is now well established that singlet oxygen generated by photosynthesis triggers a pathway that leads to cell death (Fig. However, it has only more recently been that generated H2O2 also cell death through a pathway that et al., and is by and Noctor, of these signaling pathways thus provides a mechanism to protect photosynthesis and from the cell death by generated ROS. While superoxide production in the Mehler reaction is of crucial importance to the chloroplast redox system, the production of H2O2 during the glycolate reaction of is often the most in of overall oxidant production in C3 (Foyer and Noctor, 2003). the high rates of H2O2 generation in the peroxisomes of C3 in that are in the major do not accumulate the is greatly increased and there is a low (Queval et al., 2009). This has to the that many of the responses of plant to enhanced in gene by generated H2O2, are through in the GSH by H2O2 (Queval et al., Moreover, the both and APX, the both and GR have a more the et al., This may the that GR and GSH in H2O2 metabolism as described as well as in the AsA-GSH While AsA and GSH in these antioxidants have and specific in photosynthesis and associated redox signaling (Foyer and Noctor, 2009). In to the AsA-GSH AsA has several other important in photosynthesis. It is a for an required for NPQ and it in the regulation of it can the of both and chloroplast photosynthetic components et al., 2003). the many of AsA in the regulation of photosynthesis, it is that and an of photosynthesis when to high light et al., The chloroplast and GSH pools have interactions with the photosynthetic and also in signaling pathways that photosynthesis to to environmental acclimation to high light is to in antioxidants and decreases in that are to in gene (Foyer and Noctor, 2009). Moreover, ROS and GSH are considered to as in the pathways for high light stress and signal et al., The stress signaling pathways also with signaling pathways in light a mechanism that to H2O2 generation in et al., and signaling pathways in the regulation of and at the level of information flow from the chloroplast to the in order to coordinate and gene expression, in a process called signaling et al., 2009). In has been to be important in the regulation of in to environmental and et al., 2007). While remains to be the of the between the different signaling it is that of control is through the abundance of redox metabolites, as in between different pathways involving oxidants and antioxidants not only serves as a mechanism of control but also provides a of redox information that with different of such as that are generated by chloroplasts and that are for the of photosynthetic in the et al., 2009). of chlorophyll that ROS by action are considered to be important in signaling et al., 2009). of current understanding of the of singlet oxygen signaling in signaling pathways has been by the analysis of that are in the control of which can be from the type by the and et al., in the gene of the relative to the type that the pathway of singlet control of gene different from that of H2O2 et al., 2007). Moreover, singlet oxygen generation in the activated a of signaling pathways involved in and stress but this process to be to the action of H2O2 on gene et al., 2007). analysis of the that the inactivation of a protein called to singlet stress responses and the extent of of gene et al., A called has also been in singlet control of gene et al., 2007). function in signaling pathways in the chloroplasts and control singlet in order to the accumulation of chlorophyll and particularly in stress et al., 2007). In enhancing the activities of antioxidant enzymes the accumulation of low-M r antioxidants by to a of through more efficient removal of ROS. Thus, by ROS removal more the photosynthetic processes are to environmental systems have evolved not to ROS but to allow these to within the cellular The of ROS in environmental conditions serves to limit the capacity of photosynthesis in situations where and energy-utilizing processes are not well high or enhanced antioxidant capacity can be considered to be generally because it photosynthesis to overreduction in the PET and in such as enhanced water-water cycle it can even help While there is little information to date concerning how increased antioxidant capacity signaling pathways from the chloroplasts to the with enhanced antioxidants often and stress date, of plant antioxidant have been largely to a of The of redox signaling pathways to both ROS and antioxidants more useful molecular for the of of with protective that the photosynthetic system less to and
Source: PLANT PHYSIOLOGY
Authors: Christine H. Foyer, Shigeru Shigeoka
Institutions: University of Leeds, Kindai University
Language: English
Subfield: Molecular Biology
Domain: Life Sciences
Open Access status: green
OpenAlex ID: W1991064860