Consequences of photosystem‐I damage and repair on photosynthesis and carbon use in Arabidopsis thaliana

Natural growth environments commonly include fluctuating conditions that can disrupt the photosynthetic energy balance and induce photoinhibition through inactivation of the photosynthetic apparatus. Photosystem II (PSII) photoinhibition is efficiently reversed by the PSII repair cycle, whereas photoinhibited photosystem I (PSI) recovers much more slowly. In the current study, treatment of the Arabidopsis thaliana mutant proton gradient regulation 5 (pgr5) with excess light was used to compromise PSI functionality in order to investigate the impact of photoinhibition and subsequent recovery on photosynthesis and carbon metabolism. The negative impact of PSI photoinhibition on CO₂ fixation was especially deleterious under low irradiance. Impaired starch accumulation after PSI photoinhibition was reflected in reduced respiration in the dark, but this was not attributed to impaired sugar synthesis. Normal chloroplast and mitochondrial metabolisms were shown to recover despite the persistence of substantial PSI photoinhibition for several days. The results of this study indicate that the recovery of PSI function involves the reorganization of the light‐harvesting antennae, and suggest a pool of surplus PSI that can be recruited to support photosynthesis under demanding conditions.     

Mathematical modelling of the light response curve of photoinhibition of Photosystem II

The light response curves of the acceptor and donor side mechanisms of photoinhibition of Photosystem II were calculated, using Arabidopsis as a model organism. Acceptor-side photoinhibition was modelled as double reduction of Q_A, noting that non-photochemical quenching has the same effect on the quantum yield of Q_A double reduction in closed PSII centres as it has on the quantum yield of electron transport in open centres. The light response curve of acceptor-side photoinhibition in Arabidopsis shows very low efficiency under low intensity light and a relatively constant quantum yield above light saturation of photosynthesis. To calculate the light response curve of donor-side photoinhibition, we built a model describing the concentration of the oxidized primary donor P₆₈₀⁺ during steady-state photosynthesis. The model is based on literature values of rate constants of electron transfer reactions of PSII, and it was fitted with fluorescence parameters measured in the steady state. The modelling analysis showed that the quantum yield of donor-side photoinhibition peaks under moderate light. The deviation of the acceptor and donor side mechanisms from the direct proportionality between photoinhibition and photon flux density suggests that these mechanisms cannot solely account for photoinhibition in vivo, but contribution of a reaction whose quantum yield is independent of light intensity is needed. Furthermore, a simple kinetic calculation suggests that the acceptor-side mechanism may not explain singlet oxygen production by photoinhibited leaves. The theoretical framework described here can be used to estimate the yields of different photoinhibition mechanisms under different wavelengths or light intensities.     

Photoinhibition of photosynthesis without net loss of photosystem II components inPopulus deltoides

The photoinhibition of photosynthesis was investigated on intact attached leaves and isolated thylakoid membranes of Populus deltoides.Our studies demonstrate that in intact leaves photoinhibition takes place under high irradiance which is more pronounced at higher temperatures. No net loss of Dl and other proteins associated with photosystem II (PSII) were observed even after 64 % photoinhibition suggesting that the degradation of polypeptides associated with PSII is not the only key step responsible for photoinhibition as observed by other workers. Electron transport studies in isolated thylakoid membranes suggested water oxidation complex as one of the damaged site during high light exposure. The possible mechanisms of photoinhibition without net loss of D1 protein are discussed.     

田间条件下棉花幼叶光合特性及光保护机制

通过比较棉花(Gossypium hirsutum)幼叶和完全展开叶气体交换参数及叶绿素荧光特性的差异, 探讨高光强下幼叶的光抑制程度及明确光保护机制间的协调机理。在田间自然条件下, 以棉花刚展平的幼嫩叶片(幼叶)和面积已达到最大的完全展开叶片为研究对象, 通过测定不同发育阶段叶片气体交换参数及叶绿素a荧光参数的变化, 并运用Dual-PAM100对不同发育阶段的叶片进行快速光响应曲线的拟合。结果表明: 幼叶和完全展开叶片在光合、荧光特性方面表现出明显的差异。与完全展开叶相比, 较低的叶绿素(Chl)含量和气孔导度(G_s)是幼叶较低净光合速率(P_n)的限制因素, 从而直接导致其光系统II (PSII)实际光化学效率(Φ_PSII)和光化学猝灭系数(q_P)的降低。在1800 μmol·m^-2·s^-1光强以下, 完全展开叶具有较强的围绕PSI循环的电子流(CEF), 有利于合成ATP, 是其具有较高光合能力的原因之一。相同光强下, 幼叶较低的光饱和点(LSP)更易受光抑制, 但其PSII原初光化学效率(F_v/F_m)的日变化幅度显著小于完全展开叶, 说明强光下幼叶通过类胡萝卜素(Car)猝灭单线态氧、光呼吸(P_r)、热耗散(NPQ)以及PSI-CEF等光保护机制能有效地耗散过剩的光能, 从而避免其光合机构发生光抑制。     

Photosynthetic response and recovery of Antarctic marine benthic microalgae exposed to elevated irradiances and temperatures

Exposure to high temperatures affects the photosynthetic processes in marine benthic microalgae by limiting the transport of electrons, thus reducing the ability of the cell to use light. This causes damage to the Photosystem II (PSII) and may lead to photoinhibition. However, the PSII of benthic microalgal communities from Brown Bay, eastern Antarctica, were relatively unaffected by significant changes in temperature. Benthic microalgae exposed to temperatures up to 8°C and an irradiance of 450 μmol photons m⁻² s⁻¹ did not experience any photosynthetic damage or irreversible photoinhibition. The effective quantum yield (∆F/F _m′) at 8°C (0.433 ± 0.042) was higher by comparison to cell incubated at −0.1°C (0.373 ± 0.015) with similar irradiances. Temperatures down to −5°C at a similar irradiance showed a decrease in photosynthesis with decreasing temperature, but no severe photoinhibition as the cells were able to dissipate excess energy via non-photochemical quenching and recover from damage. These responses are consistent with those recorded in past studies on Antarctic benthic microalgae and suggest that short-term temperature change (from −5 to 8°C) will not do irreversible damage to the PSII and will not affect the photosynthesis of the benthic microalgae.     

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.     

Is photoinhibition of zooxanthellae photosynthesis the primary cause of thermal bleaching in corals?

The bleaching of corals in response to increases in temperature has resulted in significant coral reef degradation in many tropical marine ecosystems. This bleaching has frequently been attributed to photoinhibition of photosynthetic electron transport and the consequent photodamage to photosystem II (PSII) and the production of damaging reactive oxygen species (ROS) in the zooxanthellae (Symbiodinium spp.). However, these events may be because of perturbations of other processes occurring within the zooxanthellae or the host cells, and consequently constitute only secondary responses to temperature increase. The processes involved with the onset of photoinhibition of electron transport, photodamage to PSII and pigment bleaching in coral zooxanthellae are reviewed. Consideration is given to how increases in temperature might lead to perturbations of metabolic processes in the zooxanthellae and/or their host cells, which could trigger events leading to bleaching. It is concluded that production of ROS by the thylakoid photosynthetic apparatus in the zooxanthellae plays a major role in the onset of bleaching resulting from photoinhibition of photosynthesis, although it is not clear which particular ROS are involved. It is suggested that hydrogen peroxide generated in the zooxanthellae may have a signalling role in triggering the mechanisms that result in expulsion of zooxanthellae from corals.     

Reversible Redox-Dependent Inactivation of Photosystem II as Photosynthesis Regulation in Chlorella

Inactivation of photosystem II (PSII) in the alga Chlorella pyrenoidosa Chick induced by photoinhibition (high light illumination at an intensity 10 times higher than photosynthesis-saturating light) or by incubation at a supraoptimum temperature (41°C) in darkness, resulted in a decrease in the relative yield of variable fluorescence due to a selective suppression of the slow phase of its rise. This indicates that low-activity PSII complexes, with a low efficiency of Q_A ^– formation are inactivated first. We suppose that the transition of normal PSII complexes to a low-activity state precedes the complete loss of their photochemical activity. The existence of some common stages of PSII inactivation, when induced by photoinhibition or incubation at supraoptimum temperature in darkness, is discussed. We suggest a scheme of the sequential stages in the regulation of photosynthetic light reactions involving a reversible redox-dependent PSII inactivation.     

Acclimation of thermotolerant algae to light and temperature interaction1

Here, we explore the responses of photosynthesis and related cellular processes in the thermotolerant microalga Micractinium sp. acclimated to limiting and saturating irradiances combined with elevated temperatures, using a novel computer-controlled multi-sensor system. This system allows for the monitoring of online values of oxygen exchange during photosynthesis and respiration with high accuracy. Micractinium sp. cells showed maximum growth and net oxygen production rates under the optimal temperature of 25°C regardless of the light acclimation conditions. Our results show that the upper thermal threshold for Micractinium sp. photosynthesis and growth ranges between 35°C and 40°C. This microalga exhibited stable photosynthetic efficiency and effective non-photochemical quenching (NPQ) under saturating light, and was more susceptible to temperature change when acclimated to limiting light levels. These results demonstrate that the acclimation of thermotolerant microalgae to saturating light helps to enhance the thermal tolerance of PSII. This feature results from enhanced heat stability of PSII photochemistry and oxygen evolution.     

Effect of the anthocyanic epidermal layer on Photosystem II and I energy dissipation processes in Tradescantia pallida (Rose) Hunt

The effect of anthocyanic cells of the epidermal layer was investigated on photosynthetic activity of the higher plant Tradescantia pallida. To determine the possible indirect role of anthocyanin in photosynthesis, analysis was done on intact leaves and leaves where anthocyanic epidermal layer was removed. Energy dissipation processes related to Photosystem II (PSII) and Photosystem I (PSI) activity was done using simultaneously Chlorophyll a (Chl a) fluorescence and P700 transmittance signals change. In anthocyanic epidermal-less leaves, PSII photochemical activity was more decreased in dependence to increasing light irradiance exposure. We found that photoinhibition of PSII decreased PSI activity by reducing the electron flow toward PSI, especially under high light intensities. Under those conditions, it resulted in the accumulation of oxidized PSI reaction centers, which was stronger in leaves where the anthocyanic epidermal layer was removed. In conclusion, our results showed that the anthocyanic epidermal layer had a photoprotective effect only on the PSII and not on the PSI of T. pallida leaves, supporting the role of anthocyanin pigments in the regulation of photosynthesis for excess absorbed light irradiance.     

Photoinhibition of Photosynthesis and its Recovery in Red Algae

In different marine red algae (Chondrus crispus, Delesseria sanguinea, Membranoptera alata, Phycodrys rubens, Phyllophora truncata, Polyneura hilliae) photoinhibition of photosynthesis has been investigated by means of both fluorescence and oxygen measurements. Measurements of absolute oxygen production show that photoinhibition causes a decline in the initial slope and in the rate of bending of the fluence rate-response curve (i.e. the photosynthetic efficiency at non-saturating fluence rates), as well as a decline in the photosynthetic capacity (Pm) at saturating fluence rates. Fluorescence data (Fv/Fm) were consistent with the results of oxygen measurements. Under excessive light photoinhibition protects photosynthesis against photo-damage in red algae. However, an increase in the initial fluorescence (Fo) after photoinhibitory treatment indicates that it could not prevent photodamage entirely. Action spectra of photoinhibition demonstrate that the main photoinhibition site in Polyneura hiliae is PS II, because far red light absorbed by PS I was ineffective. The strong increase of Fo in the blue wavelength range and the slight and partial recovery in weak blue light indicate that blue light especially causes photodamage. Recovery of photosynthesis requires dim white light conditions. Experiments with monochromatic light also show a wavelength dependence of recovery. Moreover, the recovery of photosynthesis after a photoinhibitory treatment is strongly temperature dependent, indicating participation of enzymatic processes. The comparison of fluorescence and oxygen measurement of the recovery shows different results in some species. The rate of oxygen production in red control light increased immediately after photoinhibited algae were exposed to weak light conditions. Surprisingly, the ratio of variable to maximum fluorescence (Fv/Fm) of Phyllophora truncata and the maximum fluorescence (Fm) of Polyneura hilliae show first a delay of the recovery under weak light conditions. Thus, in recovery experiments fluorescence and oxygen data are not quite consistent.     

Photoinhibition and photoprotection in senescent leaves of field-grown wheat plants

Photosynthesis, photosystem II (PSII) photochemistry, photoinhibition and the xanthophyll cycle in the senescent flag leaves of wheat (Triticum aestivum L.) plants grown in the field were investigated. Compared to the non-senescent leaves, photosynthetic capacity was significantly reduced in senescent flag leaves. The light intensity at which photosynthesis was saturated also declined significantly. The light response curves of PSII photochemistry indicate that a down-regulation of PSII photochemistry occurred in senescent leaves in particular at high light. The maximal efficiency of PSII photochemistry in senescent flag leaves decreased slightly when measured at predawn but substantially at midday, suggesting that PSII function was largely maintained and photoinhibition occurred in senescent leaves when exposed to high light. At midday, PSII efficiency, photochemical quenching and the efficiency of excitation capture by open PSII centers decreased considerably, while non-photochemical quenching increased significantly. Moreover, compared with the values at early morning, a greater decrease in CO₂ assimilation rate was observed at midday in senescent leaves than in control leaves. The levels of antheraxanthin and zeaxanthin via the de-epoxidation of violaxanthin increased in senescent flag leaves from predawn to midday. An increase in the xanthophyll cycle pigments relative to chlorophyll was observed in senescent flag leaves. The results suggest that the xanthophyll cycle was activated in senescent leaves due to the decrease in CO₂ assimilation capacity and the light intensity for saturation of photosynthesis and that the enhanced formation of antheraxanthin and zeaxanthin at high light may play an important role in the dissipation of excess light energy and help to protect photosynthetic apparatus from photodamage. Our results suggest that the well-known function of the xanthophyll cycle to safely dissipate excess excitation energy is also important for maintaining photosynthetic function during leaf senescence.     

Effects of salt stress on photosynthesis,PSII photochemistry and thermal energy dissipation in leaves of two corn (<Emphasis Type="Italic">Zea mays</Emphasis> L.) varieties

The effect of four different NaCl concentrations (from 0 to 102 mM NaCl) on seedlings leaves of two corn (Zea mays L.) varieties (Aristo and Arper) was investigated through chlorophyll (Chl) a fluorescence parameters, photosynthesis, stomatal conductance, photosynthetic pigments concentration, tissue hydration and ionic accumulation. Salinity treatments showed a decrease in maximal efficiency of PSII photochemistry (F_v/F_m) in dark-adapted leaves. Moreover, the actual PSII efficiency (ϕ_PSII), photochemical quenching coefficient (q_p), proportion of PSII centers effectively reoxidized, and the fraction of light used in PSII photochemistry (%P) were also dropped with increasing salinity in light-adapted leaves. Reductions in these parameters were greater in Aristo than in Arper. The tissue hydration decreased in salt-treated leaves as did the photosynthesis, stomatal conductance (g _s) and photosynthetic pigments concentration essentially at 68 and 102 mM NaCl. In both varieties the reduction of photosynthesis was mainly due to stomatal closure and partially to PSII photoinhibition. The differences between the two varieties indicate that Aristo was more susceptible to salt-stress damage than Arper which revealed a moderate regulation of the leaf ionic accumulation.     

Reaction centre quenching of excess light energy and photoprotection of photosystem II

In addition to the energy dissipation of excess light occurring in PSII antenna via the xanthophyll cycle, there is mounting evidence of a zeaxanthin-independent pathway for non-photochemical quenching based within the PSII reaction centre (reaction centre quenching) that may also play a significant role in photoprotection. It has been demonstrated that acclimation of higher plants, green algae and cyanobacteria to low temperature or high light conditions which potentially induce an imbalance between energy supply and energy utilization is accompanied by the development of higher reduction state of Q_A and higher resistance to photoinhibition (Huner et al., 1998). Although this is a fundamental feature of all photoautotrophs, and the acquisition of increased tolerance to photoinhibition has been ascribed to growth and development under high PSII excitation pressure, the precise mechanism controlling the redox state of Q_A and its physiological significance in developing higher resistance to photoinhibition has not been fully elucidated. In this review we summarize recent data indicating that the increased resistance to high light in a broad spectrum of photosynthetic organisms acclimated to high excitation pressure conditions is associated with an increase probability for alternative non-radiative P680⁺Q_A ^- radical pair recombination pathway for energy dissipation within the reaction centre of PSII. The various molecular mechanisms that could account for non-photochemical quenching through PSII reaction centre are also discussed.     

Increased photoinhibition in dehydrated leaves of hot pepper (Capsicum annuum L.) is not accompanied by an incremental loss of functional PSII

We examined the photosynthetic responses to photoinhibition in dehydrated leaves of hot pepper (Capsicum annuum L.). Stress was induced by immersing the roots of whole plants in Hoaglands solution containing polyethylene glycol (PEG) under high light (900 μmol photons m^-2 · s^-1). This PEG-treatment lowered the leaf water potential and the maximal rate of photosynthetic O₂ evolution (Pmax) linearly, in a time-dependent manner, to about 50% inhibition after 6 h. Pmax also decreased linearly as the period of high-light treatment lengthened. That inhibitory response was not as extreme, showing about 30% inhibition after 6 h. However, when the treatments of dehydration and high light were simultaneously administered, Pmax decreased more rapidly, in a synergistic fashion, showing about 90% inhibition within 2 h. Dehydration, in contrast to the light treatment, did not lower the maximal photochemical efficiency (Fv/Fm). Furthermore, this decline in Fv/Fm for light-treated, dehydrated leaves was almost identical to the response of photoinhibited leaves that were not dehydrated. Similar changes were observed in the number of functional PSII complexes. The decrease in Pmax and the amount of functional PSII was linearly correlated in photoinhibited leaves, but not in dehydrated leaves, regardless of light treatment. Therefore, we have demonstrated that exacerbated photoinhibition in dehydrated leaves occurs without an incremental loss of functional PSII.     

Activation of photosynthesis and resistance to photoinhibition in cyanobacteria within biological desert crust

Filamentous cyanobacteria are the main primary producers in biological desert sand crusts. The cells are exposed to extreme environmental conditions including temperature, light, and diurnal desiccation/rehydration cycles. We have studied the kinetics of activation of photosynthesis during rehydration of the cyanobacteria, primarily Microcoleus sp., within crust samples collected in the Negev desert, Israel. We also investigated their susceptibility to photoinhibition. Activation of the photosynthetic apparatus, measured by fluorescence kinetics, thermoluminescence, and low temperature fluorescence emission spectra, did not require de novo protein synthesis. Over 50% of the photosystem II (PSII) activity, assembled phycobilisomes, and photosystem I (PSI) antennae were detected within less than 5 min of rehydration. Energy transfer to PSII and PSI by the respective antennae was fully established within 10 to 20 min of rehydration. The activation of a fraction of PSII population (about 20%-30%) was light and temperature-dependent but did not require electron flow to plastoquinone [was not inhibited by 3-(3,4-dichlorophenyl)-1,1-dimethylurea]. The cyanobacteria within the crusts are remarkably resistant to photoinhibition even in the absence of protein synthesis. The rate of PSII repair increased with light intensity and with time of exposure. Consequently, the extent of photoinhibition in high-light-exposed crusts reached a constant, relatively low, level. This is in contrast to model organisms such as Synechocystis sp. strain PCC 6803 where PSII activity declined continuously over the entire exposure to high illumination. Ability of the crust's organisms to rapidly activate photosynthesis upon rehydration and withstand photoinhibition under high light intensity may partly explain their ability to survive in this ecosystem.     

Effects of hypo- and hypersalinity on photosynthetic performance of Sargassum fusiforme (Fucales,Heterokontophyta)

Photoprotection mechanisms protect photosynthetic organisms, especially under stress conditions, against photodamage that may inhibit photosynthesis. We investigated the effects of short-term immersion in hypo- and hypersalinity sea water on the photosynthesis and xanthophyll cycle in Sargassum fusiforme (Harvey) Setchell. The results indicated that under moderate light [110 μmol(photon) m^?2 s^?1], the effective quantum yield of PSII was not reduced in S. fusiforme fronds after 1 h in hyposalinity conditions, even in fresh water, but it was significantly affected by extreme hypersalinity treatment (90‰ sea water). Under high light [HL, 800 μmol(photon) m^?2 s^?1], photoprotective mechanisms operated efficiently in fronds immersed in fresh water as indicated by high reversible nonphotochemical quenching of chlorophyll fluorescence (NPQ) and de-epoxidation state; the quantum yield of PSII recovered during the subsequent relaxation period. In contrast, fronds immersed in 90‰ sea water did not withstand HL, barely developed reversible NPQ, and accumulated little antheraxanthin and zeaxanthin during HL, while recovery of the quantum yield of PSII was severely inhibited during the subsequent relaxation period. The data provided concrete evidence supporting the short-term tolerance of S. fusiforme to immersion in fresh water compared to hypersalinity conditions. The potential practical implications of these results were also discussed.     

Revised scheme for the mechanism of photoinhibition and its application to enhance the abiotic stress tolerance of the photosynthetic machinery

When photosynthetic organisms are exposed to abiotic stress, their photosynthetic activity is significantly depressed. In particular, photosystem II (PSII) in the photosynthetic machinery is readily inactivated under strong light and this phenomenon is referred to as photoinhibition of PSII. Other types of abiotic stress act synergistically with light stress to accelerate photoinhibition. Recent studies of photoinhibition have revealed that light stress damages PSII directly, whereas other abiotic stresses act exclusively to inhibit the repair of PSII after light-induced damage (photodamage). Such inhibition of repair is associated with suppression, by reactive oxygen species (ROS), of the synthesis of proteins de novo and, in particular, of the D1 protein, and also with the reduced efficiency of repair under stress conditions. Gene-technological improvements in the tolerance of photosynthetic organisms to various abiotic stresses have been achieved via protection of the repair system from ROS and, also, by enhancing the efficiency of repair via facilitation of the turnover of the D1 protein in PSII. In this review, we summarize the current status of research on photoinhibition as it relates to the effects of abiotic stress and we discuss successful strategies that enhance the activity of the repair machinery. In addition, we propose several potential methods for activating the repair system by gene-technological methods.     

The Susceptibility of Photosynthesis to Photoinhibition and the Capacity of Recovery in High and Low Light Grown Cyanobacteria, Anacystis nidulans

The susceptibility of photosynthesis to photoinhibition and the rate of its recovery were studied in the cyanobacterium Anacystis nidulans grown at a low (10 micromoles per square meter per second) and a high (120 micromoles per square meter per second) photosynthetically active radiation. The rate of light limited photosynthetic O₂ evolution was measured to determine levels of photoinhibition and rates of recovery. Studies of photoinhibition and recovery with and without the translation inhibitor streptomycin demonstrated the importance of a recovery process for the susceptibility of photosynthesis to photoinhibition. We concluded that the approximately 3 times lower susceptibility to photoinhibition of high light than of low light grown cells, significantly depended on high light grown cells having an approximately 3 times higher recovery capacity than low light grown cells. It is suggested that these differences in susceptibility to photoinhibition and recovery depends on high light grown cells having a higher turnover rate of photosystem II protein(s) that is(are) the primary site(s) of photodamage, than have low light grown cells. Furthermore, we demonstrated that photoinhibition of A. nidulans may occur under physiological light conditions without visible harm to the growth of the cell culture. The results give support for the hypotheses that the net photoinhibitory damage of photosystem II results from the balance between the photoinhibitory process and the operation of a recovery process; the capacity of the latter determining significant differences in the susceptibility of photosynthesis to photoinhibition of high and low light grown A. nidulans.