Photosynthesis and Environments: Photoinhibition and Repair Mechanisms in Plants

Photoinhibition is the inhibition of photosynthesis by excessive light resulting in the reduction of plant growth. Exposure to additional stress factors during exposure to light increases the potential for photoinhibitory effects. Reversible photoinhibition is indicative of a protective mechanism aimed at dissipating excess light energy, while irreversible photoinhibition indicates damage to the photosynthetic systems. The present review summarizes the physiological mechanisms of photoinhibition and discusses the interaction between light and other stress factors. In addition, some of the features and strategies that help plants avoid or restrict the occurrence of photoinhibition are analyzed. Most of these defense mechanisms are associated with the dissipation of excessive energy such as heat. Therefore, these mechanisms would regulate the carbon available to the plant by the output ratio of ATP/NADPH to the stressful environmental conditions. Understanding these mechanisms can help avoid plant cell death and increase plant productivity.     

高等植物光合作用的光抑制研究进展

光抑制是目前高等植物光合作用研究中的热点,近些年来无论是对其本质的认识,还是机理研究都已取得很大进展。本文首先简要回顾了光抑制研究发展的历程,阐明现代光抑制理论包括耗散过剩光能的光保持机制运转和过剩光能对光合机构的破坏两个方面。然后,就叶黄素循环、Mehler反应、光呼吸、LHCII磷酸化、PSII光化学活性下降以及由类胡罗卜素、Cytb 559参与的一些主要光保护机制作了综述,着重论述了其作用机理及研究进展。最后,就现阶段光破坏原初作用位点的认识及光破坏机理的最新研究成果作了总结。     

The desert green algae Chlorella ohadii thrives at excessively high light intensities by exceptionally enhancing the mechanisms that protect photosynthesis from photoinhibition

Although light is the driving force of photosynthesis, excessive light can be harmful. One of the main processes that limits photosynthesis is photoinhibition, the process of light-induced photodamage. When the absorbed light exceeds the amount that is dissipated by photosynthetic electron flow and other processes, damaging radicals are formed that mostly inactivate photosystem II (PSII). Damaged PSII must be replaced by a newly repaired complex in order to preserve full photosynthetic activity. Chlorella ohadii is a green microalga, isolated from biological desert soil crusts, that thrives under extreme high light and is highly resistant to photoinhibition. Therefore, C. ohadii is an ideal model for studying the molecular mechanisms underlying protection against photoinhibition. Comparison of the thylakoids of C. ohadii cells that were grown under low light versus extreme high light intensities found that the alga employs all three known photoinhibition protection mechanisms: (i) massive reduction of the PSII antenna size; (ii) accumulation of protective carotenoids; and (iii) very rapid repair of photodamaged reaction center proteins. This work elucidated the molecular mechanisms of photoinhibition resistance in one of the most light-tolerant photosynthetic organisms, and shows how photoinhibition protection mechanisms evolved to marginal conditions, enabling photosynthesis-dependent life in severe habitats.     

Leaf movements and photoinhibition in relation to water stress in field-grown beans

Photoinhibition in plants depends on the extent of light energy being absorbed in excess of what can be used in photochemistry and is expected to increase as environmental constraints limit CO2 assimilation. Water stress induces the closure of stomata, limiting carbon availability at the carboxylation sites in the chloroplasts and, therefore, resulting in an excessive excitation of the photosynthetic apparatus, particularly photosystem II (PSII). Mechanisms have evolved in plants in order to protect against photoinhibition, such as non-photochemical energy dissipation, chlorophyll concentration changes, chloroplast movements, increases in the capacity for scavenging the active oxygen species, and leaf movement or paraheliotropism, avoiding direct exposure to sun. In beans (Phaseolus vulgaris L.), paraheliotropism seems to be an important feature of the plant to avoid photoinhibition. The extent of the leaf movement is increased as the water potential drops, reducing light interception and maintaining a high proportion of open PSII reaction centres. Photoinhibition in water-stressed beans, measured as the capacity to recover F(v)/F(m), is not higher than in well-watered plants and leaf temperature is maintained below the ambient, despite the closure of stomata. Bean leaves restrained from moving, increase leaf temperature and reduce qP, the content of D1 protein and the capacity to recover F(v)/F(m) after dark adaptation, the extent of such changes being higher in water-stressed plants. Data are presented suggesting that even though protective under water stress, paraheliotropism, by reducing light interception, affects the capacity to maintain high CO2 assimilation rates throughout the day in well-watered plants.     

植物低温光抑制及可能的光保护机制研究进展

综述了近年来有关植物低温光抑制和光保护机制的研究进展。与以往对光抑制的定义不同,现在认为光抑制既包括光对光合作用反应中心的损伤,也包括植物为避免光破坏而形成的生理生化保护机制。该文主要从三个方面展开论述:低温下光抑制发生的原因及光抑制的位点;低温光抑制时可能的光保护机制;低温光抑制下过剩光能的耗散机制。     

The regulation of P700 is an important photoprotective mechanism to NaCl‐salinity in Jatropha curcas

Salinity commonly affects photosynthesis and crop production worldwide. Salt stress disrupts the fine balance between photosynthetic electron transport and the Calvin cycle reactions, leading to over‐reduction and excess energy within the thylakoids. The excess energy triggers reactive oxygen species (ROS) overproduction that causes photoinhibition in both photosystems (PS) I and II. However, the role of PSI photoinhibition and its physiological mechanisms for photoprotection have not yet been fully elucidated. In the present study, we analyzed the effects of 15 consecutive days of 100 mM NaCl in Jatropha curcas plants, primarily focusing on the photosynthetic electron flow at PSI level. We found that J. curcas plants have important photoprotective mechanisms to cope with the harmful effects of salinity. We show that maintaining P700 in an oxidized state is an important photoprotector mechanism, avoiding ROS burst in J. curcas exposed to salinity. In addition, upon photoinhibition of PSI, the highly reduced electron transport chain triggers a significant increase in H₂O₂ content which can lead to the production of hydroxyl radical by Mehler reactions in chloroplast, thereby increasing PSI photoinhibition.     

Chloroplast movement provides photoprotection to plants by redistributing PSII damage within leaves

Plants use light to fix carbon through the process of photosynthesis but light also causes photoinhibition, by damaging photosystem II (PSII). Plants can usually adjust their rate of PSII repair to equal the rate of damage, but under stress conditions or supersaturating light-intensities damage may exceed the rate of repair. Light-induced chloroplast movements are one of the many mechanisms plants have evolved to minimize photoinhibition. We found that chloroplast movements achieve a measure of photoprotection to PSII by altering the distribution of photoinhibition through depth in leaves. When chloroplasts are in the low-light accumulation arrangement a greater proportion of PSII damage occurs near the illuminated surface than for leaves where the chloroplasts are in the high-light avoidance arrangement. According to our findings chloroplast movements can increase the overall efficiency of leaf photosynthesis in at least two ways. The movements alter light profiles within leaves to maximize photosynthetic output and at the same time redistribute PSII damage throughout the leaf to reduce the amount of inhibition received by individual chloroplasts and prevent a decrease in photosynthetic potential.     

Photoinactivation of catalase at low temperature and its relevance to photosynthetic and peroxide metabolism in leaves

Abstract In green as well as in etiolated leaves of rye (Secale cereale L. ev. ‘Halo’), exposed to strong light at low temperature (0.4°C) catalase was inactivated. Other heme-containing enzymes (peroxidases) and various enzymes of photosynthetic, photorespiratory or peroxide metabolism were not photoinactivated. After returning plants from a low to a physiological temperature (22°C), catalase activity recovered within 12 h through new synthesis. The leaf contents of H₂O₂ and organic peroxides were not affected by the photoinactivation of catalse. The content of malondialdehyde generally increased after exposure to a higher light intensity. High-light-induced increases of ascorbate, and particularly of glutathione, were more marked in catalase-deficient than in normal leaves. Photoinactivation of catalase was accompanied by severe inhibition of photosynthesis. Photoinhibition of photosynthesis was not related to the lack of catalase because photosynthesis was not impaired when catalase activity was kept low by growing the plants under non-photorespiratory conditions. Photoinhibition appeared to result from photodamage in primary photochemistry of photosystem II, as indicated by a decrease of the maximal variable fluorescence. Photoinhibition of photosynthesis and of catalase have in common that in both instances proteins are involved that are continuously inactivated in light and, therefore, particularly sensitive to stress conditions that prevent their replacement by repair synthesis.     

Photoinhibition of Photosynthesis: Role of Carotenoids in Photoprotection of Chloroplast Constituents

Exposure of plants to irradiation, in excess to saturate photosynthesis, leads to reduction in photosynthetic capacity without any change in bulk pigment content. This effect is known as photoinhibition. Photoinhibition is followed by destruction of carotenoids (Cars), bleaching of chlorophylls (Chls), and increased lipid peroxidation due to formation of reactive oxygen species if the excess irradiance exposure continues. Photoinhibition of photosystem 2 (PS2) in vivo is often a photoprotective strategy rather than a damaging process. For sustainable maintenance of chloroplast function under high irradiance, the plants develop various photoprotective strategies. Cars perform essential photoprotective roles in chloroplasts by quenching the triplet Chl and scavenging singlet oxygen and other reactive oxygen species. Recently photoprotective role of xanthophylls (zeaxanthin) for dissipation of excess excitation energy under irradiance stress has been emphasised. The inter-conversion of violaxanthin (Vx) into zeaxanthin (Zx) in the light-harvesting complexes (LHC) serves to regulate photon harvesting and subsequent energy dissipation. De-epoxidation of Vx to Zx leads to changes in structure and properties of these xanthophylls which brings about significant structural changes in the LHC complex. This ultimately results in (1) direct quenching of Chl fluorescence by singlet-singlet energy transfer from Chl to Zx, (2) trans-thylakoid membrane mediated, pH-dependent indirect quenching of Chl fluorescence. Apart from these, other processes such as early light-inducible proteins, D1 turnover, and several enzymatic defence mechanisms, operate in the chloroplasts, either for tolerance or to neutralise the harmful effect of high irradiance.     

Photoinhibition of photosynthesis in intact kiwifruit (Actinidia deliciosa) leaves: effect of growth temperature on photoinhibition and recovery

Intact leaves of kiwifruit (Actinidia deliciosa (A. Chev.) C.F. Liang et A.R. Ferguson) from plants grown in a range of controlled temperatures from 15/10 to 30/25°C were exposed to a photon flux density (PFD) of 1500 μmol·m⁻²·s⁻¹ at leaf temperatures between 10 and 25°C. Photoinhibition and recovery were followed at the same temperatures and at a PFD of 20 μmol·m⁻²·s⁻¹, by measuring chlorophyll fluorescence at 77 K and 692 nm, by measuring the photon yield of photosynthetic O₂ evolution and light-saturated net photosynthetic CO₂ uptake. The growth of plants at low temperatures resulted in chronic photoinhibition as evident from reduced fluorescence and photon yields. However, low-temperature-grown plants apparently had a higher capacity to dissipate excess excitation energy than leaves from plants grown at high temperatures. Induced photoinhibition, from exposure to a PFD above that during growth, was less severe in low-temperature-grown plants, particularly at high exposure temperatures. Net changes in the instantaneous fluorescence,F ₀, indicated that little or no photoinhibition occurred when low-temperature-grown plants were exposed to high-light at high temperatures. In contrast, high-temperature-grown plants were highly susceptible to photoinhibitory damage at all exposure temperatures. These data indicate acclimation in photosynthesis and changes in the capacity to dissipate excess excitation energy occurred in kiwifruit leaves with changes in growth temperature. Both processes contributed to changes in susceptibility to photoinhibition at the different growth temperatures. However, growth temperature also affected the capacity for recovery, with leaves from plants grown at low temperatures having moderate rates of recovery at low temperatures compared with leaves from plants grown at high temperatures which had negligible recovery. This also contributed to the reduced susceptibility to photoinhibition in low-temperature-grown plants. However, extreme photoinhibition resulted in severe reductions in the efficiency and capacity for photosynthesis.     

Photosynthetic Fluorescence Induction and Oxygen Production in Corallinacean Algae Measured on Site

Photoinhibition of photosynthesis was measured in two Mediterranean Corallinaceae, Jania rubens and Corallina mediterranea, using pulse-amplitude modulation (PAM) fluorescence and oxygen production on site. Both algae were found to be adapted to low irradiances of solar radiation and easily inhibited by exposure to excessive radiation. Both algae were impaired even in their natural habitat under overhanging rocks which protected them from direct solar radiation, except for a few hours in the early morning. Recovery from photoinhibition of both the photosynthetic quantum yield, defined as F_v′/F_m′, and oxygen production took several hours and was not complete. Judging from both parameters indicated above, Jania seems to be even more sensitive than Corallina, even though the former alga was found in more exposed habitats.     

The temperature dependance of photoinhibition in the tropical basidiomycete lichen Cora pavonia E. Fries

Summary The response of net photosynthesis (NP) and dark respiration to periods of high insolation exposure was examined in the tropical basidiomycete lichen Cora pavonia. Photoinhibition of NP proved quite dependant on temperature. Rates of light saturated NP were severely impaired immediately after pretreatment high light exposure at temperatures of 10, 20 and 40°C, while similar exposure at 30°C resulted in only minimal photoinhibition. Apparent quantum yield proved an even more sensitive indicator of photoinhibition, reduced in all temperature treatments, although inhibition was again greatest at low and high temperatures. Concurrent exposure to reduced O₂ tensions during high light exposure mitigated some of the deleterious effects of high light exposure at 10 and 20°C, suggesting an interaction of O₂ with the inactivation of photosynthetic function. This represents the first reported instance of light dependant chilling stress in lichens, and may be an important limitation on the distribution of this and other tropical lichen species. This narrow range of temperatures within which thalli of C. pavonia can withstand periods of high insolation exposure coincides with that faced by hydrated thalli during rare periods of high insolation exposure within the cloud/shroud zone on La Soufrière, and points to the necessity of considering periods of atypical or unusual climatic events when interpreting patterns of net photosynthetic response, both in tropical and in north temperate lichen species.     

May photoinhibition be a consequence, rather than a cause, of limited plant productivity?

Photoinhibition in leaves in response to high and/or excess light, consisting of a decrease in photosynthesis and/or photosynthetic efficiency, is frequently equated to photodamage and often invoked as being responsible for decreased plant growth and productivity. However, a review of the literature reveals that photoinhibited leaves characterized for foliar carbohydrate levels were invariably found to possess high levels of sugars and starch. We propose that photoinhibition should be placed in the context of whole-plant source–sink regulation of photosynthesis. Photoinhibition may represent downregulation of the photosynthetic apparatus in response to excess light when (1) more sugar is produced in leaves than can be utilized by the rest of the plant and/or (2) more light energy is harvested than can be utilized by the chloroplast for the fixation of carbon dioxide into sugars.     

Photoinhibition as a control on photosynthesis and production of Sphagnum mosses

The effect of high light intensity on photosynthesis and growth of Sphagnum moss species from Alaskan arctic tundra was studied under field and laboratory conditions. Field experiments consisted of experimental shading of mosses at sites normally exposed to full ambient irradiance, and removal of the vascular plant canopy from above mosses in tundra water track habitats. Moss growth was then monitored in the experimental plots and in adjacent control areas for 50 days from late June to early August 1988. In shaded plots total moss growth was 2–3 times higher than that measured in control plots, while significant reductions in moss growth were found in canopy removal plots. The possibility that photoinhibition of photosynthesis might occur under high-light conditions and affect growth was studied under controlled laboratory conditions with mosses collected from the arctic study site, as well as from a temperate location in the Sierra Nevada, California. After 2 days of high-light treatment (800 mol photons m^–2 s^–1) in a controlled environmental chamber, moss photosynthetic capacity was significantly lowered in both arctic and temperate samples, and did not recover during the 14-day experimental period. The observed decrease in photosynthetic capacity was correlated (r ²=0.735, P<0.001) with a decrease in the ratio of variable to maximum chlorophyll fluorescence (F _v/F _m) in arctic and temperate mosses. This relationship indicates photoinhibition of photosynthesis in both arctic and temperate mosses at even moderately high light intensities. It is suggested that susceptibility to photoinhibition and failure to photoacclimate to higher light intensities in Sphagnum spp. may be related to low tissue nitrogen levels in these exclusively ombrotrophic plants. Photoinhibition of photosynthesis leading to lowered annual carbon gain in Sphagnum mosses may be an important factor affecting CO₂ flux at the ecosystem level, given the abundance of these plants in Alaskan tussock tundra.     

Tidal Dependence of Photoinhibition of Photosynthesis in Marine Macrophytes of the South China Sea*

During an expedition in spring 1992 to Hainandao, an island in the tropical zone of the South China Sea, the daily courses of photoinhibition of different brown algal species and of the seagrass Thalassia hemprichii were investigated. Experiments were carried out with the new portable chlorophyll fluorometer PAM 2000 (Walz, Germany). As a measure of photoinhibition Fv/Fm was used and as a measure of the photosynthetic yield ΔF/Fm'. Photoinhibition occurred in all algae floating near the water surface and reached its maximum between noon and the early afternoon. In the evening photosynthesis was always fully recovered. The extent of photoinhibition depended on both the depth of the algae and the course of the irradiance during the day. Algae of the sublittoral zone showed only a low degree of photoinhibition at high fluence rates when they were covered by a water column of more than 1 m, even if the water was clear. The seagrass Thalassia hemprichii grew in the middle and upper intertidal zone and showed a significant photoinhibition at low tide only when it was not water-covered. Apparently, it is able to cope with extreme high light conditions without downregulation of photosynthesis caused by photoinhibition.     

The cost of photoinhibition

Photoinhibition is an inevitable consequence of oxygenic photosynthesis. However, the concept of a 'photoinhibition-proof' plant in which photosystem II (PSII) is immune to photodamage is useful as a benchmark for considering the performances of plants with varying mixes of mechanisms which limit the extent of photodamage and which repair photodamage. Some photodamage is bound to occur, and the energy costs of repair are the direct costs of repair plus the photosynthesis foregone during repair. One mechanism permitting partial avoidance of photodamage is restriction of the number of photons incident on the photosynthetic apparatus per unit time, achieved by phototactic movement of motile algae to places with lower incident photosynthetically active radiation (PAR), by phototactic movement of plastids within cells to positions that minimize the incident PAR and by photonastic relative movements of parts of photolithotrophs attached to a substrate. The other means of avoiding photodamage is dissipating excitation of photosynthetic pigments including state transitions, non-photochemical quenching by one of the xanthophyll cycles or some other process and photochemical quenching by increased electron flow through PSII involving CO? and other acceptors, including the engagement of additional electron transport pathways. These mechanisms inevitably have the potential to decrease the rate of growth. As well as the decreased photosynthetic rates as a result of photodamage and the restrictions on photosynthesis imposed by the repair, avoidance, quenching and scavenging mechanisms, there are also additional energy, nitrogen and phosphorus costs of producing and operating repair, avoidance, quenching and scavenging mechanisms. A comparison is also made between the costs of photoinhibition and those of other plant functions impeded by the occurrence of oxygenic photosynthesis, i.e. the competitive inhibition of the carboxylase activity of ribulose bisphosphate carboxylase-oxygenase by oxygen via the oxygenase activity, and oxygen damage to nitrogenase in diazotrophic organisms.     

Effect of high-light treatments in inducing photoinhibition of photosynthesis in intact leaves of low-light grown Phaseolus vulgaris and Lastreopsis microsora

Photoinhibition studies, using gas-exchange techniques, were conducted with leaflets of Phaseolus vulgaris L. plants that were grown under low photonfluence rates. Comparative measurements were made on attached, intact leaflets and in subsequently isolated chloroplasts. Photoinhibition studies were also conducted with attached fronds of the deep-shade fern Lastreopsis microsora (Endl.) Tindale. Leaflets of lowlight-grown Phaseolus vulgaris and fronds of the shade fern were found to be subject to similar photoinhibition when exposed to photon-fluence rates in excess of those at which they were grown. Photoinhibition following exposure to a photon fluence-rate approximating full sunlight is manifested as a reduction in the capacity for both light-saturated and light-limited carbon uptake and is reflected at the chloroplast level as substantial inhibition of electron flow through photosystem (PS) II, with little effect on PS I. The extent of photoinhibition is markedly dependent on the length of exposure to a high-light regime and on the actual photon-fluence rate maintained during treatment. A greater degree of photoinhibition is evident if carbon metabolism is prevented by the removal of CO₂ than when maximum rates of CO₂ uptake prevail throughout the exposure to a high photonfluence rate. Apparently a certain level of CO₂ turnover is beneficial in providing a sink for photochemically generated energy. When leaf material is exposed to photon-fluence rates well in excess of the rate present during growth apparently the potentials of the various biophysical and photochemical means of dissipating excitation energy are exceeded and photoinhibition of photosynthesis results.Abbreviation PFR photon fluence rate     

Temperature-dependent photoinhibition and recovery of photosynthesis in the green alga Chlamydomonas reinhardtii acclimated to 12 and 27°C

Photoinhibition of photosynthesis and subsequent recovery were studied in cultures of the unicellular green alga Chlamydomonas reinhardtii L. (wt strain 137 c mating type +) acclimated at high (27°C) and low (12°C) temperature, Photoinhibition was assayed by fluorescence kinetics (77K) and oxygen evolution measurements under growth temperature conditions Inhibition of 50% was obtained by exposing cultures acclimated at high temperature to a photosynthetic photon flux density (PPFD) of 1 600 μmol m⁻² S⁻¹ at. 27°C. and cultures acclimated at low temperature to a PPFD of 900 μmol m⁻² s⁻¹ at 12°C When the photoinhibitory conditions were shifted it was revealed that algae acclimated at low temperature had acquired an increased resistance to photoinhibition at both 12 and 27°C. Furthermore, acclimation at low temperature increased the capacity to recover from 50% photoinhibition at both 12 and 27°C Studies of photoinhibition in the presence of the protein synthesis inhibitor, chloramphenicol, revealed that in response to acclimation at low temperature during growth the algae became more dependent on protein synthesis to avoid photoinhibition. It is suggested that acclimation at low temperature rendered C. reinhardtii an increased resistance to photoinhibition by. increasing the rate of turnover of photodamaged proteins in photosystem II (PS II). However, we cannot exclude the possibility that the increased resistance to photoinhibition of C. reinhardtii acclimated at low temperature also involves modifications of the mechanism of photoinhibition.     

A mechanistic model of photoinhibition

A mechanistic model was developed, to simulate the main facets of photoinhibition in phytoplankton. Photoinhibition is modelled as a time dependent decrease in the initial slope of a photosynthesis versus irradiance curve, related to D1 (photosystem II reaction centre protein) damage and non-photochemical quenching. The photoinhibition model was incorporated into an existing ammonium-nitrate nutrition interaction model capable of simulating photoacclimation and aspects of nitrogen uptake and utilization. Hence the current model can simulate the effects of irradiance on photosynthesis from sub-saturating to inhibitory photon flux densities, during growth on different nitrogen sources and under nutrient stress. Model output conforms well to experimental data, allowing the extent of photoinhibition to be predicted under a range of nutrient and light regimes. The ability of the model to recreate the afternoon depression of photosynthesis and the enhancement of photosynthesis during fluctuating light suggests that these two processes are related to photoinhibition. The model may be used to predict changes in biomass and/or carbon fixation under a wide range of oceanographic situations, and it may also help to explain the progression to dominance of certain algal species, and bloom formation under defined irradiance and nutrient conditions.     

Photooxidative stress in plants

The light-dependent generation of active oxygen species is termed photooxidative stress. This can occur in two ways: (1) the donation of energy or electrons directly to oxygen as a result of photosynthetic activity; (2) exposure of tissues to ultraviolet irradiation. The light-dependent destruction of catalase compounds the problem. Although generally detrimental to metabolism, superoxide and hydrogen peroxide may serve useful functions if rigorously controlled and compartmentalised. During photosynthesis the formation of active oxygen species is minimised by a number of complex and refined regulatory mechanisms. When produced, active oxygen species are eliminated rapidly by efficient antioxidative systems. The chloroplast is able to use the production and destruction of hydrogen peroxide to regulate the thermal dissipation of excess excitation energy. This is an intrinsic feature of the regulation of photosynthetic electron transport. Photoinhibition and photooxidation only usually occur when plants are exposed to stress. Active oxygen species are part of the alarm-signalling processes in plants. These serve to modify metabolism and gene expression so that the plant can respond to adverse environmental conditions, invading organisms and ultraviolet irradiation. The capacity of the antioxidative defense system is often increased at such times but if the response is not sufficient, radical production will exceed scavenging and ultimately lead to the disruption of metabolism. Oxidative damage arises in high light principally when the latter is in synergy with additional stress factors such as chilling temperatures or pollution. Environmental stress can modify the photooxidative processes in various ways ranging from direct involvement in light-induced free radical formation to the inhibition of metabolism that renders previously optimal light levels excessive. It is in just such situations that the capacity for the production of active oxygen species can exceed that for scavenging by the antioxidative defense systems. The advent of plant transformation, however, may have placed within our grasp the possibility of engineering greater stress tolerance in plants by enhancement of the antioxidative defence system.