Thermostability Of Photosystem II Research Articles

Enhanced thermotolerance of photosystem II by elevated pore-water salinity in the coastal marsh graminoid Sporobolus pumilus

In coastal marsh ecosystems, high salinities, anoxic waterlogged soils, and elevated summer temperatures often promote physiological strain that results in only a few tolerant halophytic species. Although not well understood, plant physiological responses to multiple stressors can be complex and may involve intensifying or offsetting reactions. In this study, we investigated physiological responses to combined salinity and high temperature in the coastal marsh graminoid Sporobolus pumilus (syn. Spartina patens). Specifically, we considered changes in plant-water relations and Photosystem II (PSII) behavior (involving chlorophyll [chl] a fluorescence) in heat-shocked plants that were acclimated to different salinities (0, 15, and 30 psu). Higher salinities fostered lower stomatal conductance (g), lower leaf-water potential (Ψleaf) and lower tissue-water content (θ), as well as decreased potential quantum yield (Fv/Fm) and decreased excitation energy capture efficiencies of open reaction centers (Fv’/Fm’). Heat-shocked plants acclimated to freshwater only had decreased Fv/Fm and PSII performance index (PIABS). Interestingly, there were no changes in chl a fluorescent outputs in heat-shocked plants acclimated to moderate salinities, and minimal changes in plants acclimated to high salinities. Approximately 25% of the heat-shocked S. pumilus in freshwater revealed a K-step in their polyphasic chl a fluorescent transients (OJIP procedure); K-steps were not observed in salt-treated plants. This suggests that, for plants residing in freshwater, heat-shock promoted disturbances in the PSII reaction centers and, in some cases, disrupted the oxygen-evolving complex. These PSII disruptions were either absent or less intense in salinity-treated plants, indicating that acclimation to environmental salts may provide PSII thermostability in S. pumilus.

Variation in the performance and thermostability of photosystem II in European beech (Fagus sylvatica L.) provenances is influenced more by acclimation than by adaptation

The assisted migration of resistant seeds and seedlings may be a key to mitigating the effects of climate change on the productivity and composition of forest ecosystems. These efforts require an understanding of the intraspecific variability in the response of trees to extreme weather events such as heat waves. In this study, we assessed the geographical patterns of photosystem II (PSII) performance and thermostability in European beech (Fagus sylvatica L.) and whether intraspecific differences are associated with climate of origin. Two provenance trials with starkly contrasting climates were used for this study. Leaves were sampled both before and after natural heat stress exposure. Rapid chlorophyll fluorescence kinetics was used to evaluate PSII performance and PSII thermostability after simulated heat stress. The performance of PSII at 30 °C, which is still considered a non-damaging temperature, was generally slightly better at the warmer location than at the colder location. The populations originating closer to the Slovenian refugium, as well as those growing closer to their site of origin, showed better performance of PSII but not greater thermostability. The effect of simulated heat stress was much stronger in the colder plots compared to the warmer plots, but only for previously stressed trees. Likewise, we found indicators of geographical patterns of thermotolerance as well as relationships between thermotolerance and climate of origin mostly for trees exposed to natural heat. While the origin of provenances partly explained the variation among provenances, acclimation driven by climate played a major role in the response to heat stress. In beech, PSII seems to have a potential for coping with high temperature.

Field-acclimated Gossypium hirsutum cultivars exhibit genotypic and seasonal differences in photosystem II thermostability

Previous investigations have demonstrated that photosystem II (PSII) thermostability acclimates to prior exposure to heat and drought, but contrasting results have been reported for cotton (Gossypium hirsutum). We hypothesized that PSII thermotolerance in G. hirsutum would acclimate to environmental conditions during the growing season and that there would be differences in PSII thermotolerance between commercially-available U.S. cultivars. To this end, three cotton cultivars were grown under dryland conditions in Tifton Georgia, and two under irrigated conditions in Marianna Arkansas. At Tifton, measurements included PSII thermotolerance (T15, the temperature causing a 15% decline in maximum quantum yield), leaf temperatures, air temperatures, midday (1200 to 1400h) leaf water potentials (ΨMD), leaf-air vapor pressure deficit (VPD), actual quantum yield (ΦPSII) and electron transport rate through PSII (ETR) on three sample dates. At Marianna, T15 was measured on two sample dates. Optimal air and leaf temperatures were observed on all sample dates in Tifton, but PSII thermotolerance increased with water deficit conditions (ΨMD=−3.1MPa), and ETR was either unaffected or increased under water-stress. Additionally, T15 for PHY 499 was ∼5°C higher than for the other cultivars examined (DP 0912 and DP 1050). The Marianna site experienced more extreme high temperature conditions (20–30 days Tmax≥35°C), and showed an increase in T15 with higher average Tmax. When average T15 values for each location and sample date were plotted versus average daily Tmax, strong, positive relationships (r2 from .954 to .714) were observed between Tmax and T15. For all locations T15 was substantially higher than actual field temperature conditions. We conclude that PSII thermostability in G. hirsutum acclimates to pre-existing environmental conditions; PSII is extremely tolerant to high temperature and water-deficit stress; and differences in PSII thermotolerance exist between commercially-available cultivars.

Exogenous glycine betaine and proline play a protective role in heat-stressed barley leaves (Hordeum vulgare L.): A chlorophyll a fluorescence study

Effects of drought and exogenous glycine betaine and proline on Photosystem II (PSII) photochemistry were studied in barley leaves under heat stress induced by exposing them to 45°C for 10 min. Polyphasic fluorescence transient (OJIP) was used to evaluate PSII photochemistry in leaves treated with either glycine betaine or proline, combined or not with heat treatment. A distinct K step in the fluorescence transient OJIP appeared in control leaves, indicating an inactivation of the oxygen evolving complex (OEC). Drought stress and exogenous glycine betaine and proline modified the shape of the OJIP curve of leaves heated at 45°C and the K step was not as pronounced. Increased thermostability of PSII may be associated with the resistance of OEC and increased energy connectivity between PSII units. The thermostability of PSII was also reflected by a lower decrease in maximum quantum yield of primary photochemistry (ϕPo = F V/F M) and performance index (PI). Exogenous application of glycine betaine or proline can play an important role in enhancing plant stress tolerance and may help reduce effects of environmental stresses.

Photosystem II thermostability in situ: Environmentally induced acclimation and genotype-specific reactions in Triticum aestivum L

Photosystem II (PSII) thermostability and acclimation effects on PSII photochemical efficiency were analyzed in thirty field grown winter wheat (Triticum aestivum L.) genotypes using prompt chlorophyll a fluorescence kinetics before and after dark heat treatment. A gradual increase in temperature caused the appearance of K-bands at 300 μs on the chlorophyll fluorescence induction curve, indicating the impairment of the PSII donor side (even by heat treatment at 38 °C). An increase in basal fluorescence, commonly used as a criterion of PSII thermostability, was observed beyond a temperature threshold of 44 °C. Moreover, an acclimation shift (increase of critical temperature) was observed at the 3.5 °C identified for K-band appearance, but only by 1.1 °C for a steep increase in F(0). The single temperature approach with regular weekly observations completed within two months using dark heat treatment at 40 °C demonstrated that the acclimation effect is not gradual, but occurs immediately and is associated with an increase of daily temperature maxima over 30 °C. The acclimated heat treated samples had less effect on the donor side of PSII, the higher fraction of active Q(A)(-) reducing reaction centers and causing a much lower decrease of connectivity among PSII units compared to non-acclimated samples. In the non-treated plants the reduction of antennae size, increase of PSII connectivity and changes in the acceptor side occurred as a result of heat acclimation. The enhancement of PSII thermostability persisted over several weeks regardless of weather conditions. The genotype comparison identified three groups that differed either in initial PSII thermostability or in acclimation capacity; these groupings were clearly associated with the origin of the genotypes.

Comparison of thermostability of PSII between the chromatic and green leaf cultivars of Amaranthus tricolor L.

In the present study, we investigated the antioxidative potential in leaves of the chromatic (CC) versus green (GC) Amaranthus tricolor L. under moderate high-temperature stress at 45°C. Before heat stress, CC had significantly higher levels of betacyanins [about 3.2 mg g−1(FM)] than the green [1.8 mg g−1(FM) (p<0.01), while similar chlorophyll (Chl) content [about 2 mg g−1(FM)] was observed between both cultivars. After exposure to high temperature (45°C) for 6 days, betacyanins in leaves of CC were remarkably increased (about 2 times of that in control samples grown at 30°C). In contrast, betacyanins in GC significantly decreased by 56% in comparison with that of the control. Chl level in CC was higher than that in GC after heat stress for 6 days. Flavonoids and total phenolics in both cultivars were increased, but much more in CC. Significantly less H2O2 accumulation was observed in the leaves and stems of CC than in those of GC under heat stress. Interestingly, much stronger circadian oscillation in fluorescence was observed in both cultivars after treatment at 45°C, which suggested that heat stress stimulates endogenous rhythms of photosystem II (PSII). Under moderate high-temperature stress, Chl fluorescence parameters Fv/Fm (maximum quantum yield of PSII), qP (coefficient of photochemical quenching), ΦPSII (effective PSII quantum yield), and ETR (electron transport rate) exhibited a gradual decrease, NPQ (nonphotochemical quenching) showed a slight increase followed by a gradual decline, whereas Fo (minimum fluorescence of a dark-adapted leaf) increased continuously. In contrast to GC, after 120 h of high-temperature treatment, CC exhibited significantly lower Fo level, and higher levels of Fv/Fm and NPQ. It is clear that PSII in CC was more stable than that in GC. The results indicate that betacyanins are an effective antioxidant, and probably contribute greatly to the higher thermal stability of PSII and higher tolerance to heat stress.

Effects of phospholipase and lipase treatments on photosystem II core dimer from a thermophilic cyanobacterium

Lipids are important components of transmembrane protein complexes. In order to study the roles of lipids in photosystem II (PSII), we treated the PSII core dimer complex from a thermophilic cyanobacterium Thermosynechococcus vulcanus with phospholipase A(2) (PLA(2)) and lipase, and examined their effects on PSII structure and function. PLA(2)-treatment decreased the content of phospholipid, phosphatidylglycerol (PG) by 59%, leading to a decrease of oxygen evolution by 40%. On the other hand, although treatment with lipase specifically decreased the content of monogalactosyldiacylglycerol (MGDG) by 52%, it decreased oxygen evolution only by 16%. This indicates that PG plays a more important role in PSII than MGDG. Both PLA(2)- and lipase-treatments induced neither the dissociation of PSII dimer, nor any loss of polypeptides. The degradation of PG resulted in a damage to the Q(B)-binding site as demonstrated from photoreduction activity of 2,6-dichlorophenolindophenol and chlorophyll fluorescence yields in the absence or presence of 3-(3,4-dichlorophenyl)-1,1-dimethylurea, and the dependencies of oxygen evolution on various electron acceptors before and after PLA(2)- or lipase-treatments. However, there were approximately three and five molecules of PG and MGDG per PSII reaction center left in the PSII dimeric complex after the PLA(2)- and lipase-treatments. These lipids are therefore bound to the interior of the protein matrix and resistant to the lipase treatments. The resistance of these lipids against PLA(2)- and lipase-treatments may be a specific feature of PSII from the thermophilic cyanobacterium, suggesting a possible correlation between binding of lipids and thermostability of PSII.

Changes in Thermostability of Photosystem II and Leaf Lipid Composition of Rice Mutant with Deficiency of Light‐harvesting Chlorophyll a/b Protein Complexes

AbstractWe studied the difference in thermostability of photosystem II (PSII) and leaf lipid composition between a T‐DNA insertion mutant rice (Oryza sativa L.) VG28 and its wild type Zhonghua 11. Native green gel and SDS‐PAGE electro‐phoreses revealed that the mutant VG28 lacked all light‐harvesting chlorophyll a/b protein complexes. Both the mutant and wild type were sensitive to high temperatures, and the maximal efficiency of PSII photochemistry (Fv/ Fm) and oxygen‐evolving activity of PSII in leaves significantly decreased with increasing temperature. However, the PSII activity of the mutant was markedly more sensitive to high temperatures than that of the wild type. Lipid composition analysis showed that the mutant had less phosphatidylglycerol and sulfoquinovosyl diacylglycerol compared with the wild type. Fatty acid analysis revealed that the mutant had an obvious decrease in the content of 16:1t and a marked increase in the content of 18:3 compared with the wild type. The effects of lipid composition and unsaturation of membrane lipids on the thermostability of PSII are discussed.

Increased photosynthetic activities and thermostability of photosystem II with leaf development of elm seedlings ( Ulmus pumila) probed by the fast fluorescence rise OJIP

Experiments were conducted to investigate the photosynthetic activity and thermostability of photosystem II (PSII) in elm seedling ( Ulmus pumila) leaves from initiation to full expansion. During leaf development, photosynthesis, measured as CO 2 fixation, increased gradually and reached a maximum value when leaves were fully developed. In parallel with the increase of carbon assimilation, chlorophyll content increased. The chlorophyll a fluorescence measurements showed that the maximum quantum yield of PSII primary photochemistry ( φ po), the efficiency with which the energy of trapped excitons is converted into the electron transport beyond Q A ( Ψ o) and the quantum yield of electron transport beyond Q A ( φ Eo) increased gradually. The low light experiments confirmed these results independently. When subjected to heat stress, young leaves exhibited progressively lower φ po and maximal fluorescence ( F m) values with considerably higher minimal fluorescence ( F o) than mature leaves, demonstrating that PSII in newly initiating leaves is more sensitive to heat stress. Further analysis revealed that PSII structure in newly initiating leaves showed a robust alteration under heat stress, which was reflected by the clear K phase in the OJIP curves. Therefore, we suggest that the enhanced thermostability of PSII in the case of leaf growth might be associated with an improvement of the stability of the oxygen-evolving complex (OEC) to heat stress during leaf development.

Chlorophyll fluorescence temperature curve on Klebsormidium flaccidum cultivated at different temperature regimes

Summary The alga Klebsormidium flaccidum from the Moroccan desert was studied using the measurement of the Fluorescence Temperature Curve - FTC (a dependence of chlorophyll fluorescence intensity on linearly increasing temperature) during the cell cycle. The green alga was cultivated at an alternating temperature regime (35 °C - light/5 °C - dark) simulating natural desert conditions, or at a constant temperature (20 °C). Pronounced reversible changes in FTC were detected during the diurnal cycle with alga cultivated at alternating temperatures. The critical temperature (TC) of the steep fluorescence rise up to the FTC maximum (the M1 maximum) and the temperature of the M1 FTC maximum (TP), which are usually used as the indicators of photosystem II (PSII) thermostability, gradually increased by about 2.5 °C during the light phase. The ratio of the height of M1 FTC maximum to the fluorescence intensity at 30 °C (M1/F(T30) ratio), usually reflecting PSII photochemistry, also significantly increased during the light phase of the diurnal cycle. However, the changes in the parameters corresponded with changes in the slope of the fluorescence rise to the M1 FTC maximum, and with changing temperature dependence of the maximal fluorescence - FM. Analysis of the data led to the conclusion that the change in the TC parameter and the M1/F(T30) ratio need not merely reflect the changes in the PSII thermostability and PSII photochemistry, respectively. The causes of these discrepancies are discussed.

Thermostability and Photostability of Photosystem II in Leaves of the Chlorina-f2 Barley Mutant Deficient in Light-Harvesting Chlorophyll a/b Protein Complexes.

The chlorophyll-b-less chlorina-f2 barley mutant is deficient in the major as well as some minor light-harvesting chlorophyll-protein complexes of photosystem II (LHCII). Although the LHCII deficiency had relatively minor repercussions on the leaf photosynthetic performances, the responses of photosystem II (PSII) to elevated temperatures and to bright light were markedly modified. The chlorina-f2 mutation noticeably reduced the thermostability of PSII, with thermal denaturation of PSII starting at about 35[deg]C and 38.5[deg]C in chlorina-f2 and in the wild type, respectively. The increased susceptibility of PSII to heat stress in chlorina-f2 leaves was due to the weakness of its electron donor side, with moderate heat stress causing detachment of the 33-kD extrinsic PSII protein from the oxygen-evolving complex. Prolonged dark adaptation of chlorina-f2 leaves was also observed to inhibit the PSII donor side. However, weak illumination slowly reversed the dark-induced inhibition of PSII in chlorina-f2 and cancelled the difference in PSII thermostability observed between chlorina-f2 and wild-type leaves. The mutant was more sensitive to photoinhibition than the wild type, with strong light stress impairing the PSII donor side in chlorina-f2 but not in the wild type. This difference was not observed in anaerobiosis or in the presence of 3-(3,4-dichlorophenyl)- 1,1-dimethylurea, diuron. The acceptor side of PSII was only slightly affected by the mutation and/or the aforementioned stress conditions. Taken together, our results indicate that LHCII stabilize the PSII complexes and maintain the water-oxidizing system in a functional state under varying environmental conditions.

Photosynthesis, chlorophyll fluorescence, light-harvesting system and photoinhibition resistance of a zeaxanthindashaccumulating mutant of Arabidopsis thaliana

The abscisic-acid-deficient aba-1 mutant of Arabidopsis thaliana is unable to epoxidize zeaxanthin. As a consequence, it contains large amounts of this carotenoid and lacks epoxy-xanthophylls. HPLC analysis of pigment contents in leaves, isolated thylakoids and preparations of the major light-harvesting complex of photosystem II (PSII) (LHC-II) indicated that zeaxanthin replaced neoxanthin, violaxanthin and antheraxanthin in the light-harvesting system of PSII in aba-1. Nondashdenaturing electrophoretic fractionation of solubilized thylakoids showed that the xanthophyll imbalance in aba-1 was associated with a pronounced decrease in trimeric LHC-II in favour of monomeric complexes, with a substantial increase in free pigments (mainly zeaxanthin and chlorophyll b), suggesting a decreased stability of LHC-II. The reduced thermostability of PSII in aba-1 was also deduced from in vivo chlorophyll fluorescence measurements. Wild-type and aba-1 leaves could not be distinguished on the basis of their photosynthetic performance: no significant difference was observed between the two types of leaves for light-limited and light-saturated photosynthetic oxygen evolution, PSII photochemistry and PSII to PSI electron flow. When dark-adapted leaves (grown in white light of 80 μmol m −2 s −1) were suddenly exposed to red light of 150 μmol m −2 s −1, there was a strong nondashphotochemical quenching of chlorophyll fluorescence, the amplitude of which was virtually identical (at steady state) in aba-1 and wild-type leaves, despite the fact that the xanthophyll cycle pigment pool was completely in the form of zeaxanthin in aba-1 and almost exclusively in the form of violaxanthin in the wild type. A high concentration of zeaxanthin in aba-1 thylakoids did not, in itself, provide any particular protection against the photoinhibition of PSII. Taken together, the presented results indicate the following: (1) zeaxanthin can replace epoxy-xanthophylls in LHC-II without significantly affecting the photochemical efficiency of PSII; (2) zeaxanthin dose not play any specific role in direct (thermal) energy dissipation in PSII; (3) the photoprotective action of the xanthophyll cycle (rapid photoconversion of violaxanthin to zeaxanthin) is not based on the mere substitution of violaxanthin by zeaxantin in the chlorophyll antennae.

Temperature Sensitivity of the Photochemical Function of Photosynthesis in Potato ( Solanum tuberosum) and a Cultivated Andean Hybrid ( Solanum X juzepczukii)

The responses of the photochemical apparatus of photosynthesis to low and high temperatures were compared in leaves of the frost-sensitive Solanum tuberosum (cv. Haig) and of a frost-tolerant Andean potato, Solanum x juzepczukii (cv. Lucki). The main observations and conclusions of this study are that: (i) Photosystem II (PSII) is noticeably more heat-resistant in S. x juzepczukii than in S. tuberosum, indicating an enhanced generalized stress tolerance of the former genotype to extremes of temperature. (ii) The higher thermostability of PSII in S. x juzepczukii leaves is not associated with any enhancement of the sensitivity of PSII photochemistry to chilling temperature. In both species, the chilling-induced inhibition of electron transport through PSII is closely correlated with the inhibition of the PSII-to-PSI electron flow, the rate of which is determined by the reoxidation of reduced plastoquinone. A slowdown of the latter reaction at low temperature can be attributed to the accumulation of protons in the thylakoid lumen associated with the inhibition of the Calvin cycle activity in chilled leaves, as suggested by the strong non-photochemical quenching of chlorophyll fluorescence. (iii) The photochemical activities of both species are similarly impaired by chilling treatments in the light, indicating that frost resistance does not preclude susceptibility to photoinhibition damage at chilling temperature. (iv) A striking difference between S. tuberosum and S. x juzepczukii is the high plasticity of the PSII thermotolerance in the latter species, with low (8 °C) and high (35 °C) temperature treatments respectively decreasing and increasing the heat-tolerance of PSII. These changes are not observed or are very limited in the Haig variety of S. tuberosum. (v) In contrast to the constitutive thermotolerance of PSII (measured in 23 °C-grown plants), 35 °C-induced thermotolerance has a dramatic effect on the photochemical activity at chilling temperature. When placed at 5 °C, the intersystem electron flow of 35 °C-treated leaves is dramatically inhibited as compared with non-treated leaves whereas ΔpH-related quenching of chlorophyll fluorescence is unchanged. These findings indicate independent control of non-acclimated heat-tolerance and thermally induced heat-tolerance of the photosynthetic membranes. Taken together, the presented data show that the photosynthetic apparatus of the cultivated Andean hybrid, S. x juzepczukii, though sensitive to chilling injury in the light, is adapted to the changing temperature conditions prevailing in the natural habitat of its wild progenitor where night frosts are associated with warm and sunny days.