Photodamaged Photosystem II Research Articles

Thylakoid-Bound FtsH Proteins Facilitate Proper Biosynthesis of Photosystem I.

Thylakoid membrane-bound FtsH proteases have a well-characterized role in degradation of the photosystem II (PSII) reaction center protein D1 upon repair of photodamaged PSII. Here, we show that the Arabidopsis (Arabidopsis thaliana) var1 and var2 mutants, devoid of the FtsH5 and FtsH2 proteins, respectively, are capable of normal D1 protein turnover under moderate growth light intensity. Instead, they both demonstrate a significant scarcity of PSI complexes. It is further shown that the reduced level of PSI does not result from accelerated photodamage of the PSI centers in var1 or var2 under moderate growth light intensity. On the contrary, radiolabeling experiments revealed impaired synthesis of the PsaA/B reaction center proteins of PSI, which was accompanied by the accumulation of PSI-specific assembly factors. psaA/B transcript accumulation and translation initiation, however, occurred in var1 and var2 mutants as in wild-type Arabidopsis, suggesting problems in later stages of PsaA/B protein expression in the two var mutants. Presumably, the thylakoid membrane-bound FtsH5 and FtsH2 have dual functions in the maintenance of photosynthetic complexes. In addition to their function as a protease in the degradation of the photodamaged D1 protein, they also are required, either directly or indirectly, for early assembly of the PSI complexes.

Glutathione reductase 2 maintains the function of photosystem II in Arabidopsis under excess light

Glutathione reductase plays a crucial role in the elimination of H2O2 molecules via the ascorbate–glutathione cycle. In this study, we used transgenic Arabidopsis plants with decreased glutathione reductase 2 (GR2) levels to investigate whether this GR2 activity protects the photosynthetic machinery under excess light. The transgenic plants were highly sensitive to excess light and accumulated high levels of H2O2. Photosystem II (PSII) activity was significantly decreased in transgenic plants. Flash-induced fluorescence relaxation and thermoluminescence measurements demonstrated inhibition of electron transfer between QA and QB and decreased redox potential of QB in transgenic plants. Immunoblot and blue native gel analysis showed that the levels of PSII proteins and PSII complexes were decreased in transgenic plants. Analyses of the repair of photodamaged PSII and in vivo pulse labeling of thylakoid proteins showed that the repair of photodamaged PSII is inhibited due to the inhibition of the synthesis of the D1 protein de novo in transgenic plants. Taken together, our results suggest that under excess light conditions, GR2 plays an important role in maintaining both the function of the acceptor side of PSII and the repair of photodamaged PSII by preventing the accumulation of H2O2. In addition, our results provide details of the role of H2O2 in vivo accumulation in photoinhibition in plants.

Identification and Roles of Photosystem II Assembly, Stability, and Repair Factors in Arabidopsis.

Photosystem II (PSII) is a multi-component pigment-protein complex that is responsible for water splitting, oxygen evolution, and plastoquinone reduction. Components of PSII can be classified into core proteins, low-molecular-mass proteins, extrinsic oxygen-evolving complex (OEC) proteins, and light-harvesting complex II proteins. In addition to these PSII subunits, more than 60 auxiliary proteins, enzymes, or components of thylakoid protein trafficking/targeting systems have been discovered to be directly or indirectly involved in de novo assembly and/or the repair and reassembly cycle of PSII. For example, components of thylakoid-protein-targeting complexes and the chloroplast-vesicle-transport system were found to deliver PSII subunits to thylakoid membranes. Various auxiliary proteins, such as PsbP-like (Psb stands for PSII) and light-harvesting complex-like proteins, atypical short-chain dehydrogenase/reductase family proteins, and tetratricopeptide repeat proteins, were discovered to assist the de novo assembly and stability of PSII and the repair and reassembly cycle of PSII. Furthermore, a series of enzymes were discovered to catalyze important enzymatic steps, such as C-terminal processing of the D1 protein, thiol/disulfide-modulation, peptidylprolyl isomerization, phosphorylation and dephosphorylation of PSII core and antenna proteins, and degradation of photodamaged PSII proteins. This review focuses on the current knowledge of the identities and molecular functions of different types of proteins that influence the assembly, stability, and repair of PSII in the higher plant Arabidopsis thaliana.

Conversion of photosystem II dimer to monomers during photoinhibition is tightly coupled with decrease in oxygen-evolving activity in the diatom Chaetoceros gracilis.

The rapid turnover of photosystem II (PSII) in diatoms is thought to be at an exceptionally high rate compared with other oxyphototrophs; however, its molecular mechanisms are largely unknown. In this study, we examined the photodamage and repair processes of PSII in the marine centric diatom Chaetoceros gracilis incubated at 30 or 300μmol photons m-2s-1 in the presence of a de novo protein-synthesis inhibitor. When de novo protein synthesis was blocked by chloramphenicol (Cm), oxygen-evolving activity gradually decreased even at 30μmol photons m-2s-1 and could not be detected at 12h. PSII inactivation was enhanced by higher illumination. Using Cm-treated cells, the conversion of PSII dimer to monomers was observed by blue native PAGE. The rate of PSII monomerization was very similar to that of the decrease in oxygen-evolving activity under both light conditions. Immunological detection of D1 protein in the Cm-treated cells showed that the rate of D1 degradation was slower than that of the former two events, although it was more rapid than that observed in other oxyphototrophs. Thus, the three accelerated events, especially PSII monomerization, appear to cause the unusually high rate of PSII turnover in diatoms.

Differences in the Responses of Photosystems I and II in Cymbidium sinense and C. tracyanum to Long-Term Chilling Stress.

The susceptibility of photosystem I (PSI) and photosystem II (PSII) to chilling stress depends on plant species, and cyclic electron flow (CEF) plays an important role in photoprotection for some species under short stress periods. However, little is known about the responses of PSI and PSII to long-term chilling stress. We studied two orchid species—Cymbidium sinense and C. tracyanum— that differ in their capacity to adapt to low temperature, and exposed plants for 19 d to stress conditions that included 4°C and a light intensity of 250 to 350 μmol photons m-2 s-1. Meanwhile, we investigated their dynamic variations in Chl fluorescence and P700 parameters. After exposure to 4°C and 250 μmol photons m-2 s-1 for 6 h, PSI activity was maintained stable in both species, but stronger PSII photoinhibition was observed in C. sinense. During the long-term treatment, the maximum quantum yield of PSII was significantly reduced, with that decrease being greater in C. sinense. After 19 d of chilling treatment, the maximum photo-oxidizable P700 declined only slightly in C. tracyanum but dropped significantly in C. sinense. Linear electron flow was largely depressed during the long-term chilling treatment, especially in C. sinense. Meanwhile, C. tracyanum showed higher CEF activity than C. sinense. These results indicate that PSII is more sensitive to chilling-light stress than PSI in both species. The rate of PSII photodamage at chilling-light stress is higher in C. sinense than C. tracyanum, and CEF contributes to photoprotection for PSI and PSII under long-term chilling stress in C. tracyanum.

D1 fragmentation in photosystem II repair caused by photo-damage of a two-step model.

Light energy drives photosynthesis, but it simultaneously inactivates photosynthetic mechanisms. A major target site of photo-damage is photosystem II (PSII). It further targets one reaction center protein, D1, which is maintained efficiently by the PSII repair cycle. Two proteases, FtsH and Deg, are known to contribute to this process, respectively, by efficient degradation of photo-damaged D1 protein processively and endoproteolytically. This study tested whether the D1 cleavage accomplished by these proteases is affected by different monochromic lights such as blue and red light-emitting-diode light sources, remaining mindful that the use of these lights distinguishes the current models for photoinhibition: the excess-energy model and the two-step model. It is noteworthy that in the two-step model, primary damage results from the absorption of light energy in the Mn-cluster, which can be enhanced by a blue rather than a red light source. Results showed that blue and red lights affect D1 degradation differently. One prominent finding was that D1 fragmentation that is specifically generated by luminal Deg proteases was enhanced by blue light but not by red light in the mutant lacking FtsH2. Although circumstantial, this evidence supports a two-step model of PSII photo-damage. We infer that enhanced D1 fragmentation by luminal Deg proteases is a response to primary damage at the Mn-cluster.

Slr0151 in Synechocystis sp. PCC 6803 is required for efficient repair of photosystem II under high-light condition.

Cyanobacteria are ancient photosynthetic prokaryotes that have adapted successfully to adverse environments including high-light irradiation. Although it is known that the repair of photodamaged photosystem II (PSII) in the organisms is a highly regulated process, our knowledge of the molecular components that regulate each step of the process is limited. We have previously identified a hypothetical protein Slr0151 in the membrane fractions of cyanobacterium Synechocystis sp. PCC 6803. Here, we report that Slr0151 is involved in PSII repair of the organism. We generated a mutant strain (Δslr0151) lacking the protein Slr0151 and analyzed its characteristics under normal and high-light conditions. Targeted deletion of slr0151 resulted in decreased PSII activity in Synechocystis. Moreover, the mutant exhibited increased photoinhibition due to impairment of PSII repair under high-light condition. Further analysis using in vivo radioactive labeling and 2-D blue native/sodium dodecylsulfate polyacrylamide gel electrophoresis indicated that the PSII repair cycle was hindered at the levels of D1 synthesis and disassembly and/or assembly of PSII in the mutant. Protein interaction assays demonstrated that Slr0151 interacts with D1 and CP43 proteins. Taken together, these results indicate that Slr0151 plays an important role in regulating PSII repair in the organism under high-light stress condition.

Photosystem II recovery in the presence and absence of chloroplast protein repair in the symbionts of corals exposed to bleaching conditions

Increased seawater temperature causes photoinhibition due to accumulation of photodamaged photosystem II (PSII) in symbiotic algae (genus Symbiodinium) within corals, and it is assumed to be associated with coral bleaching. To avoid photoinhibition, photosynthetic organisms repair the photodamaged PSII through replacing the PSII proteins, primarily the D1 protein, with newly synthesised proteins. However, in experiments using cultured Symbiodinium strains, the PSII repair of Symbiodinium has been suggested not to be related to the synthesis of the D1 protein. In this study, we examined the relationship between the recovery of PSII photochemical efficiency (F V/F M) and the content of D1 protein after high-light and high-temperature treatments using the bleaching-sensitive coral species, Pocillopora damicornis and Acropora millepora, and the bleaching-tolerant coral species, Montipora digitata and Pavona decussata. When corals were exposed to strong light (600 µmol photons m−2 s−1) at elevated temperature (32 °C) for 8 h, significant bleaching occurred in bleaching-sensitive coral species although an almost similar extent of reduced PSII function was found across all coral species tested. During a subsequent 15-h recovery under low light (10 µmol photons m−2 s−1) at optimal temperature (22 °C), the reduced F V/F M recovered close to initial levels in all coral species, but the reduced D1 content recovered only in one coral species (Pavona decussata). D1 content was therefore not strongly linked to chloroplast protein synthesis-dependent PSII repair. These results demonstrate that the recovery of photodamaged PSII does not always correspond with the recovery of D1 protein content in Symbiodinium within corals, suggesting that photodamaged PSII can be repaired by a unique mechanism in Symbiodinium within corals.

Evidence for the regulation of leaf movement by photosystem II activity

Some light-demanding plants fold leaves under high light and open leaves under low light. Since paraheliotropism leaf movement under high light could be induced by environmental stresses that aggravate photoinhibition of photosystem II (PSII), we hypothesize that the leaf movement is regulated by PSII activity. To test this hypothesis, we examined photosynthetic gas exchange and chlorophyll fluorescence, diurnal changes in leaf angle, and maximum quantum yield of PSII (Fv/Fm) in a leaf-foldable canopy liana, Bauhinia tenuiflora, grown in an open field. The rate of CO2 assimilation, electron transport rate, and non-photochemical quenching was saturated under light of 1000μmolphotonsm−2s−1. After exposure to high light of 1000μmolphotonsm−2s−1 and 2000μmolphotonsm−2s−1 for 8h, Fv/Fm decreased to 54% and 19%, respectively. The repair of photodamaged PSII was strongly suppressed when illuminated at high light. After high light treatment, the recovery of PSII activity under low light functions efficiently. During the daytime, the minimum values of Fv/Fm and leaf angle were 0.75° and 9°, respectively. In the early morning, high Fv/Fm was accompanied by large leaf angle. At noon, when Fv/Fm was lower than 0.8, B. tenuiflora strongly folded its leaves. In the afternoon, when Fv/Fm was higher than 0.8, leaf angle gradually increased. After treatment with 3-(3,4-dichlorophenyl)-1,1-dimethylurea (DCMU, an inhibitor of PSII), Fv/Fm and leaf angle decreased significantly. Based on these results, the leaf movement in B. tenuiflora can be regulated by PSII photoinhibition, suggesting that PSII photoinhibition plays a potential role in the regulation of leaf movement under environmental stresses.

Regulation and Dynamics of the Light-Harvesting System

Photosynthetic organisms are continuously subjected to changes in light quantity and quality, and must adjust their photosynthetic machinery so that it maintains optimal performance under limiting light and minimizes photodamage under excess light. To achieve this goal, these organisms use two main strategies in which light-harvesting complex II (LHCII), the light-harvesting system of photosystem II (PSII), plays a key role both for the collection of light energy and for photoprotection. The first is energy-dependent nonphotochemical quenching, whereby the high-light-induced proton gradient across the thylakoid membrane triggers a process in which excess excitation energy is harmlessly dissipated as heat. The second involves a redistribution of the mobile LHCII between the two photosystems in response to changes in the redox poise of the electron transport chain sensed through a signaling chain. These two processes strongly diminish the production of damaging reactive oxygen species, but photodamage of PSII is unavoidable, and it is repaired efficiently.

Regulation of Reversible Dissociation of LHCII from PSII by Phosphorylation in Plants

LHCII is a crucial light-harvesting pigment/protein complex in photosystem II (PSII) supercomplex. It also participates in the light energy redistribution between photosystems and in the photoprotection via its reversible dissociation with PSII and PSI (photosystem I). This reversible detachment of LHCII is regulated by phosphorylation of its own and PSII core protein. Under low light conditions, LHCII is phosphorylated and dissociated with PSII core protein complex and combined with PSI, which balances the excitation energy between PSII and PSI; Under high light environment, the phosphorylation of PSII core proteins makes LHCII detach from PSII. The dissociated LHCII presents in a free state, which involves in the thermal dissipation of excess excitation energy. During photodamage, dual phosphorylations of both PSII core proteins and LHCII complexes occur. The phosphorylation of D1 is conductive to the disintegration of photodamaged PSII and the cycle of repair. In this circumstance, the phosphorylation of LHCII is induced by reactive oxygen species (ROS) and then the phosphorylated LHCII migrates to PSI, into the repair cycle of damaged PSII. The ferredoxin (Fdr) and thioredoxin (Tdr) system may play a possible central role in the phosphorylation regulation on LHCII dissociation.

Ammonium tolerance in the cyanobacterium Synechocystis sp. strain PCC 6803 and the role of the psbA multigene family

Ammonium is one of the major nutrients for plants, and a ubiquitous intermediate in plant metabolism, but it is also known to be toxic to many organisms, in particular to plants and oxygenic photosynthetic microorganisms. Although previous studies revealed a link between ammonium toxicity and photodamage in cyanobacteria under in vivo conditions, ammonium-induced photodamage of photosystem II (PSII) has not yet been investigated with isolated thylakoid membranes. We show here that ammonium directly accelerated photodamage of PSII in Synechocystis sp. strain PCC6803, rather than affecting the repair of photodamaged PSII. Using isolated thylakoid membranes, it could be demonstrated that ammonium-induced photodamage of PSII primarily occurred at the oxygen evolution complex, which has a known binding site for ammonium. Wild-type Synechocystis PCC6803 cells can tolerate relatively high concentrations of ammonium because of efficient PSII repair. Ammonium tolerance requires all three psbA genes since mutants of any of the three single psbA genes are more sensitive to ammonium than wild-type cells. Even the poorly expressed psbA1 gene, whose expression was studied in some detail, plays a detectable role in ammonium tolerance.

Improvement of Cerium on Photosynthesis of Maize Seedlings Under a Combination of Potassium Deficiency and Salt Stress

Added Ce(3+) can partly substitute for Ca(2+) or Mg(2+) and improve photosynthesis under the deficiency of these elements, but very few studies focused on photosynthetic improvement in maize seedlings caused by K(+) deficiency, salt stress, especially a combination of K(+) deficiency and salt stress. In the present study, the effects of Ce(3+) on the photosynthesis of maize seedlings under the three different stresses were investigated. The results showed that added Ce(3+) under various stresses increased the ratios of free water/bound water and of K(+)/Na(+), the pigment contents, the values of Fv/Fm, Y(II), ETR(II), Y(NPQ), Qp, qL, NPQ, and qN of photosystem II (PSII), the values of Y(I) and ETR(I) of photosystem I (PSI) and the expression levels of LhcII cab1 and rbcL, and decreased the values of Y(NO) and Y(NA). This implied that added Ce(3+) depressed ion toxicity, photodamage of PSII, and acceptor side constraints of PSI, and enhanced adjustable energy dissipation, the responses of photochemistry, and carbon assimilation caused by K(+) deficiency, salt stress, and the combination of K(+) deficiency and salt stress. However, Ce(3+) mitigation of photosynthetic inhibition in maize seedlings caused by the combined stresses was greater than that of salt stress, and Ce(3+) mitigation under salt stress was greater than that under K(+) deficiency. In addition, the results also showed that Ce(3+) cannot improve photosynthesis and growth of maize seedlings under K(+) deficiency by substituting for K(+).

Molecular Cloning and Characterization of the PsbP Domain Protein 1 Gene (GhPPD1) in Cotton (Gossypium hirsutum L.)

As a member of the PsbP superfamily in plants, the PsbP protein is essential for the water splitting reaction in photosynthesis. PsbP-like proteins (PPLs) are required for the repair of photodamaged photosystem II (PSII) under high-intensity light and the accumulation of chloroplast NADPH dehydrogenase (NDH). However, to date, studies on PsbP domain proteins (PPDs) are rather limited with literature reported on only PPD5 and PPD6. Other PPDs have not been studied yet. In this study, a cotton PsbP domain protein 1 gene (GhPPD1, GenBank accession no. HQ404251) encoding the PPD1 protein was cloned by rapid amplification of complementary DNA (cDNA) ends-polymerase chain reaction. The full-length cDNA is 951 bp and encodes an open reading frame of 257 amino acids with deduced molecular weight of 29 kDa. The GhPPD1 protein shared 77–86 % identity at the amino acid level with PPD1 isolated from Populus trichocarpa, Ricinus communis, Vitis vinifera, Glycine max, and Arabidopsis thaliana. The corresponding genomic DNA containing three exons and two introns was isolated and analyzed. The 5′ flanking region was also analyzed to identify a group of putative cis-acting elements. DNA gel blot analysis revealed that the GhPPD1 gene has two to five copies in the cotton genome. Additionally, real-time PCR analysis revealed that GhPPD1 was expressed in cotton leaves, anthers, and stems, and its expression level in leaves was much higher than those in anthers and stems. It was minimally expressed in other tissues. On the basis of these results, we propose that GhPPD1 is not only associated with photosynthesis but also related to pollen activity and male fertility.

Expression, purification, crystallization and preliminary X-ray diffraction analysis ofArabidopsis thalianaDeg8

Arabidopsis thaliana Deg8, an ATP-independent serine endopeptidase, is involved in the repair of photosystem II (PSII), specifically the degradation of the photo-damaged PSII reaction centre D1 protein. To understand the molecular mechanism underlying the participation of Deg8 in the degradation of the photo-damaged D1 protein, the structure of Deg8 is needed. Until recently, however, no structure of Deg8 had been solved. In this study, Deg8 from A.thaliana was cloned, overexpressed and purified in Escherichia coli. Crystallization was performed at 277 K using tribasic sodium citrate as the precipitant and the crystals diffracted to 2.0 Å resolution, belonging to space group C2 with unit-cell parameters a = 129.5, b = 124.2, c = 93.3 Å, α = γ = 90, β=132.4°. Assuming one trimer in the asymmetric unit, the Matthews coefficient and the solvent content were calculated to be 2.35 Å(3) Da(-1) and 47.6%, respectively.

Cost and benefit of the repair of photodamaged photosystem II in spinach leaves: roles of acclimation to growth light

When visible light is excess, the photosynthetic machinery is photoinhibited. The extent of net photoinhibition of photosystem II (PSII) is determined by a balance between the rate of photodamage to D1 and some other PSII proteins and the rate of the turnover cycle of these proteins. It is widely believed that the protein turnover requires much energy cost. The aims of this study are to (1) evaluate the energy cost of PSII repair, (2) measure the benefit in terms of photosynthetic gain realized by the repairing of the photodamaged PSII, and (3) know whether acclimation of photosynthesis to growth light affects the rates of the photodamage and repair. We grew spinach in high-light (HL) and low-light (LL) and measured the rates of D1 photodamage and repair in these leaves. We determined the rate constants of photodamage (k (pi)) and repair (k (rec)) by the PAM fluorometry in the presence or in the absence of lincomycin, an inhibitor of 70S protein synthesis. HL leaves showed smaller k (pi) and greater k (rec) than LL leaves. The energy cost of the repairing of the photodamaged D1 protein was <0.5% of ATP produced by photophosphorylation at PPFDs ranging from 400 to 1600μmolm(-2)s(-1) and was greater in HL leaves than in LL leaves. The benefits brought about by the repair were more than from 35 to 270 times the cost at PPFDs ranging from 400 to 1600μmolm(-2)s(-1). The benefits of HL leaves were greater than those of LL leaves because of the higher photosynthesis rates in HL leaves. Running a simple simulation of daily photosynthesis using the parameters obtained in this study, we discuss why the plants need to pay the cost of D1 protein turnover to repair the photodamaged PSII.

Mitochondrial alternative oxidase pathway protects plants against photoinhibition by alleviating inhibition of the repair of photodamaged PSII through preventing formation of reactive oxygen species in Rumex K‐1 leaves

The purpose of this study was to explore how the mitochondrial AOX (alternative oxidase) pathway alleviates photoinhibition in Rumex K-1 leaves. Inhibition of the AOX pathway decreased the initial activity of NADP-malate dehydrogenase (EC 1.1.1.82, NADP-MDH) and the pool size of photosynthetic end electron acceptors, resulting in an over-reduction of the photosystem I (PSI) acceptor side. The over-reduction of the PSI acceptor side further inhibited electron transport from the photosystem II (PSII) reaction centers to the PSII acceptor side as indicated by an increase in V(J) (the relative variable fluorescence at J-step), causing an imbalance between photosynthetic light absorption and energy utilization per active reaction center (RC) under high light, which led to the over-excitation of the PSII reaction centers. The over-reduction of the PSI acceptor side and the over-excitation of the PSII reaction centers enhanced the accumulation of reactive oxygen species (ROS), which inhibited the repair of the photodamaged PSII. However, the inhibition of the AOX pathway did not change the level of photoinhibition under high light in the presence of the chloroplast D1 protein synthesis inhibitor chloramphenicol, indicating that the inhibition of the AOX pathway did not accelerate the photodamage to PSII directly. All these results suggest that the AOX pathway plays an important role in the protection of plants against photoinhibition by minimizing the inhibition of the repair of the photodamaged PSII through preventing the over-production of ROS.

Phosphorylation and nitration levels of photosynthetic proteins are conversely regulated by light stress

Using a label-free mass spectrometric approach, we investigated light-induced changes in the distribution of phosphorylated and nitrated proteins within subpopulations of native photosynthetic complexes in the thylakoid membrane of Arabidopsis thaliana leaves adapted to growth light (GL) and subsequently exposed to high light (HL). Eight protein phosphorylation sites were identified in photosystem II (PSII) and the phosphorylation level of seven was regulated by HL as determined based on peak areas from ion chromatograms of phosphorylated and non-phosphorylated peptides. Although the phosphorylation of PSII proteins was reported in the past, we demonstrated for the first time that two minor antenna LHCB4 isoforms are alternately phosphorylated under GL and HL conditions in PSII monomers, dimers and supercomplexes. A role of LHCB4 phosphorylation in state transition and monomerization of PSII under HL conditions is proposed. We determined changes in the nitration level of 23 tyrosine residues in five photosystem I (PSI) and nine PSII proteins and demonstrated for the majority of them a lower nitration level in PSI and PSII complexes and supercomplexes under HL conditions, as compared to GL. In contrast, the nitration level significantly increased in assembled/disassembled PSI and PSII subcomplexes under HL conditions. A possible role of nitration in (1) monomerization of LHCB1-3 trimers under HL conditions (2) binding properties of ferredoxin-NADP+ oxidoreductase to photosystem I, and (3) PSII photodamage and repair cycle, is discussed. Based on these data, we propose that the conversely regulated phosphorylation and nitration levels regulate the stability and turnover of photosynthetic complexes under HL conditions.

A Small Zinc Finger Thylakoid Protein Plays a Role in Maintenance of Photosystem II in Arabidopsis thaliana

This work identifies LOW QUANTUM YIELD OF PHOTOSYSTEM II1 (LQY1), a Zn finger protein that shows disulfide isomerase activity, interacts with the photosystem II (PSII) core complex, and may act in repair of photodamaged PSII complexes. Two mutants of an unannotated small Zn finger containing a thylakoid membrane protein of Arabidopsis thaliana (At1g75690; LQY1) were found to have a lower quantum yield of PSII photochemistry and reduced PSII electron transport rate following high-light treatment. The mutants dissipate more excess excitation energy via nonphotochemical pathways than wild type, and they also display elevated accumulation of reactive oxygen species under high light. After high-light treatment, the mutants have less PSII-light-harvesting complex II supercomplex than wild-type plants. Analysis of thylakoid membrane protein complexes showed that wild-type LQY1 protein comigrates with the PSII core monomer and the CP43-less PSII monomer (a marker for ongoing PSII repair and reassembly). PSII repair and reassembly involve the breakage and formation of disulfide bonds among PSII proteins. Interestingly, the recombinant LQY1 protein demonstrates a protein disulfide isomerase activity. LQY1 is more abundant in stroma-exposed thylakoids, where key steps of PSII repair and reassembly take place. The absence of the LQY1 protein accelerates turnover and synthesis of PSII reaction center protein D1. These results suggest that the LQY1 protein may be involved in maintaining PSII activity under high light by regulating repair and reassembly of PSII complexes.

Protein synthesis is the primary target of reactive oxygen species in the photoinhibition of photosystem II

Photoinhibition of photosystem II (PSII) occurs when the rate of photodamage to PSII exceeds the rate of the repair of photodamaged PSII. Recent examination of photoinhibition by separate determinations of photodamage and repair has revealed that the rate of photodamage to PSII is directly proportional to the intensity of incident light and that the repair of PSII is particularly sensitive to the inactivation by reactive oxygen species (ROS). The ROS-induced inactivation of repair is attributable to the suppression of the synthesis de novo of proteins, such as the D1 protein, that are required for the repair of PSII at the level of translational elongation. Furthermore, molecular analysis has revealed that the ROS-induced suppression of protein synthesis is associated with the specific inactivation of elongation factor G via the formation of an intramolecular disulfide bond. Impairment of various mechanisms that protect PSII against photoinhibition, including photorespiration, thermal dissipation of excitation energy, and the cyclic transport of electrons, decreases the rate of repair of PSII via the suppression of protein synthesis. In this review, we present a newly established model of the mechanism and the physiological significance of repair in the regulation of the photoinhibition of PSII.