Higher Cyclic Electron Flow Research Articles

Induction of photosynthesis under anoxic condition in Thalassiosira pseudonana and Euglena gracilis: interactions between fermentation and photosynthesis.

In their natural environment, microalgae can be transiently exposed to hypoxic or anoxic environments. Whereas fermentative pathways and their interactions with photosynthesis are relatively well characterized in the green alga model Chlamydomonas reinhardtii, little information is available in other groups of photosynthetic micro-eukaryotes. In C. reinhardtii cyclic electron flow (CEF) around photosystem (PS) I, and light-dependent oxygen-sensitive hydrogenase activity both contribute to restoring photosynthetic linear electron flow (LEF) in anoxic conditions. Here we analyzed photosynthetic electron transfer after incubation in dark anoxic conditions (up to 24h) in two secondary microalgae: the marine diatom Thalassiosira pseudonana and the excavate Euglena gracilis. Both species showed sustained abilities to prevent over-reduction of photosynthetic electron carriers and to restore LEF. A high and transient CEF around PSI was also observed specifically in anoxic conditions at light onset in both species. In contrast, at variance with C. reinhardtii, no sustained hydrogenase activity was detected in anoxic conditions in both species. Altogether our results suggest that another fermentative pathway might contribute, along with CEF around PSI, to restore photosynthetic activity in anoxic conditions in E. gracilis and T. pseudonana. We discuss the possible implication of the dissimilatory nitrate reduction to ammonium (DNRA) in T. pseudonana and the wax ester fermentation in E. gracilis.

High salt-induced PSI-supercomplex is associated with high CEF and attenuation of state transitions

While PSI-driven cyclic electron flow (CEF) and assembly of thylakoid supercomplexes have been described in model organisms like Chlamydomonas reinhardtii, open questions remain regarding their contributions to survival under long-term stress. The Antarctic halophyte, C. priscuii UWO241 (UWO241), possesses constitutive high CEF rates and a stable PSI-supercomplex as a consequence of adaptation to permanent low temperatures and high salinity. To understand whether CEF represents a broader acclimation strategy to short- and long-term stress, we compared high salt acclimation between the halotolerant UWO241, the salt-sensitive model, C. reinhardtii, and a moderately halotolerant Antarctic green alga, C. sp. ICE-MDV (ICE-MDV). CEF was activated under high salt and associated with increased non-photochemical quenching in all three Chlamydomonas species. Furthermore, high salt-acclimated cells of either strain formed a PSI-supercomplex, while state transition capacity was attenuated. How the CEF-associated PSI-supercomplex interferes with state transition response is not yet known. We present a model for interaction between PSI-supercomplex formation, state transitions, and the important role of CEF for survival during long-term exposure to high salt.

Moderate photoinhibition of PSII and oxidation of P700 contribute to chilling tolerance of tropical tree species in subtropics of China

In the subtropics, a few tropical tree species are distributed and planted for ornamental and horticultural purposes; however, the photosynthesis of these species can be impaired by chilling. This study aimed to understand how these species respond to chilling. Light-dependent and CO₂ assimilation reactions of six tropical tree species from geographically diverse areas, but grown at a lower subtropical site in China, were monitored during a chilling (≤ 10°C). Chilling induced stomatal and nonstomatal effects and moderate photoinhibition of PSII, with severe effect in <i>Ixora chinensis</i>. <i>Woodfordia fruticosa</i> was little affected by chilling, with negligible reduction of photosynthesis and PSII activity, higher cyclic electron flow (CEF), and oxidation state of P700 (P700⁺). Photoinhibition of PSII thus reduced electron flow to P700, while active CEF reduced oxidative damage of PSI and maintained photosynthesis during chilling. Studied parameters revealed that coupling between light-dependent and CO₂ assimilation reactions was enhanced under chilling.

Responses of Linear and Cyclic Electron Flow to Nitrogen Stress in an N-Sensitive Species Panax notoginseng.

Nitrogen (N) is a primary factor limiting leaf photosynthesis. However, the mechanism of N-stress-driven photoinhibition of the photosystem I (PSI) and photosystem II (PSII) is still unclear in the N-sensitive species such as Panax notoginseng, and thus the role of electron transport in PSII and PSI photoinhibition needs to be further understood. We comparatively analyzed photosystem activity, photosynthetic rate, excitation energy distribution, electron transport, OJIP kinetic curve, P700 dark reduction, and antioxidant enzyme activities in low N (LN), moderate N (MN), and high N (HN) leaves treated with linear electron flow (LEF) inhibitor [3-(3,4-dichlorophenyl)-1,1-dimethyl urea (DCMU)] and cyclic electron flow (CEF) inhibitor (methyl viologen, MV). The results showed that the increased application of N fertilizer significantly enhance leaf N contents and specific leaf N (SLN). Net photosynthetic rate (Pn) was lower in HN and LN plants than in MN ones. Maximum photochemistry efficiency of PSII (Fv/Fm), maximum photo-oxidation P700+ (Pm), electron transport rate of PSI (ETRI), electron transport rate of PSII (ETRII), and plastoquinone (PQ) pool size were lower in the LN plants. More importantly, K phase and CEF were higher in the LN plants. Additionally, there was not a significant difference in the activity of antioxidant enzyme between the MV- and H2O-treated plants. The results obtained suggest that the lower LEF leads to the hindrance of the formation of ΔpH and ATP in LN plants, thereby damaging the donor side of the PSII oxygen-evolving complex (OEC). The over-reduction of PSI acceptor side is the main cause of PSI photoinhibition under LN condition. Higher CEF and antioxidant enzyme activity not only protected PSI from photodamage but also slowed down the damage rate of PSII in P. notoginseng grown under LN.

Responses of Photosynthetic Electron Transport to Drought and Re-watering in Two Maize Genotypes

Effects of drought stress on photosynthesis have been well-documented. However, photosynthetic electron transport process in response to combined drought stress and recovery in maize is relatively scant. In this study, the photosynthetic electron flow, the energy quenching in PSII and PSI, and cyclic electron flow (CEF) activity in two maize (Zea mays L.) genotypes were measured. In both genotypes, chlorophyll a fluorescence transient (OJIP) showed progressive drought caused increases of J and I step, the positive of K-band and L-band; and decreases in TR0/ABS, ET0/TR0, ET0/ABS, RE0/ET0 and PIABS. Analysis of the modulated 820 nm reflection (MR) showed progressive drought decreased the values of VPSI and VPSII-PSI. Decreases in quantum yields of Y(I) and Y(II) were accompanied by increase of Y(NPQ) and CEF. Compare to Shaanke9 (SK9), the drought-induced changes in Dafeng30 (DF30) were stronger, and SK9 kept higher CEF under drought stress. After re-watering, SK9 recovered more completely in all parameters than DF30, suggesting that the reversible down-regulation of PSII and PSI in SK9 maintained the functional integrity of photosystems. The photosynthetic apparatus of SK9 cultivar is more resistant to drought than that of DF30. These results indicate that more efficient regulation of photosynthetic electron transport between two photosystems and higher CEF in the SK9 jointly play crucial role in recovery from drought damages, which could contribute to a better adaptation under varying drought environment.

Chlamydomonas sp. UWO 241 Exhibits High Cyclic Electron Flow and Rewired Metabolism under High Salinity.

The Antarctic green alga Chlamydomonas sp. UWO 241 (UWO 241) is adapted to permanent low temperatures, hypersalinity, and extreme shade. One of the most striking phenotypes of UWO 241 is an altered PSI organization and constitutive PSI cyclic electron flow (CEF). To date, little attention has been paid to CEF during long-term stress acclimation, and the consequences of sustained CEF in UWO 241 are not known. In this study, we combined photobiology, proteomics, and metabolomics to understand the underlying role of sustained CEF in high-salinity stress acclimation. High salt-grown UWO 241 exhibited increased thylakoid proton motive flux and an increased capacity for nonphotochemical quenching. Under high salt, a significant proportion of the up-regulated enzymes were associated with the Calvin-Benson-Bassham cycle, carbon storage metabolism, and protein translation. Two key enzymes of the shikimate pathway, 3-deoxy-d-arabinoheptulosonate 7-phosphate synthase and chorismate synthase, were also up-regulated, as well as indole-3-glycerol phosphate synthase, an enzyme involved in the biosynthesis of l-Trp and indole acetic acid. In addition, several compatible solutes (glycerol, Pro, and Suc) accumulated to high levels in high salt-grown UWO 241 cultures. We suggest that UWO 241 maintains constitutively high CEF through the associated PSI-cytochrome b 6 f supercomplex to support robust growth and strong photosynthetic capacity under a constant growth regime of low temperatures and high salinity.

Effects of extreme temperatures on the growth and photosynthesis of invasive Bidens alba and its native congener B. biternata

Temperatures are expected to fluctuate widely under climate change but little is known about how extreme temperatures might affect the physiology and performance of invasive compared to native plant species. In this study, we evaluated the effects of high (40/35°C) and low (10/5°C) temperature regimes on the growth and photosynthesis of the invasive Asteraceae species Bidens alba and its native congener B. biternata using a growth chamber experiment. Results showed that invasive B. alba had significantly greater total biomass and relative growth rate, accompanied by higher net photosynthetic rate (Pn), than native B. biternata at both low and high temperature extremes. The reduction in Pn for B. alba was mainly caused by stomatal limitations, but for B. biternata it was caused by non‐stomatal factors, indicating that greater damage to physiological processes may occur in native B. biternata under both low and high temperature stress. Higher cyclic electron flow around photosystem I in invasive B. alba than in native B. biternata under extreme temperatures might alleviate the negative effect of temperature extremes to photosynthetic and thus promote its photosynthetic efficiency. To conclude, the invasive B. alba has both greater cold and heat tolerance than its native congener B. biternata, suggesting that the invader may outperform native species under future extreme temperature conditions.

Cyclic electron flow may provide some protection against PSII photoinhibition in rice (Oryza sativa L.) leaves under heat stress

Previously we have shown that a quick down-regulation in PSI activity compares to that of PSII following short-term heat stress for two rice groups including C4023 and Q4149, studied herein. These accessions were identified to have different natural capacities in driving cyclic electron flow (CEF) around PSI; i.e., low CEF (lcef) and high CEF (hcef) for C4023 and Q4149, respectively. The aim of this study was to investigate whether these two lines have different mechanisms of protecting photosystem II from photodamage under heat stress. We observed a stepwise alteration in the shape of Chl a fluorescence induction (OJIP) with increasing temperature treatment. The effect of 44°C treatment on the damping in Chl a fluorescence was more pronounced in C4023 than in Q4149. Likewise, we noted a disruption in the I-step, a decline in the Fv due to a strong damping in the Fm, and a slight increase in the F0. Normalized data demonstrated that the I-step seems more susceptible to 44°C in C4023 than in Q4149. We also measured the redox states of plastocyanin (PC) and P700 by monitoring the transmission changes at 820nm (I820), and observed a disturbance in the oxidation/reduction kinetics of PC and P700. The decline in the amplitude of their oxidation was shown to be about 29% and 13% for C4023 and Q4149, respectively. The electropotential component (Δφ) of ms-DLE appeared more sensitive to temperature stress than the chemical component (ΔpH), and the impact of heat was more evident and drastic in C4023 than in Q4149. Under heat stress, we noticed a concomitant decline in the primary photochemistry of PSII as well as in both the membrane energization process and the lumen protonation for both accessions, and it is evident that heat affects these parameters more in C4023 than in Q4149. All these data suggest that higher CET can confer higher photoprotection to PSII in rice lines, which can be a desirable trait during rice breeding, especially in the context of a “warming” world.

Defects in the Expression of Chloroplast Proteins Leads to H2O2 Accumulation and Activation of Cyclic Electron Flow around Photosystem I.

We describe a new member of the class of mutants in Arabidopsis exhibiting high rates of cyclic electron flow around photosystem I (CEF), a light-driven process that produces ATP but not NADPH. High cyclic electron flow 2 (hcef2) shows strongly increased CEF activity through the NADPH dehydrogenase complex (NDH), accompanied by increases in thylakoid proton motive force (pmf), activation of the photoprotective qE response, and the accumulation of H2O2. Surprisingly, hcef2 was mapped to a non-sense mutation in the TADA1 (tRNA adenosine deaminase arginine) locus, coding for a plastid targeted tRNA editing enzyme required for efficient codon recognition. Comparison of protein content from representative thylakoid complexes, the cytochrome bf complex, and the ATP synthase, suggests that inefficient translation of hcef2 leads to compromised complex assembly or stability leading to alterations in stoichiometries of major thylakoid complexes as well as their constituent subunits. Altered subunit stoichiometries for photosystem I, ratios and properties of cytochrome bf hemes, and the decay kinetics of the flash-induced thylakoid electric field suggest that these defect lead to accumulation of H2O2 in hcef2, which we have previously shown leads to activation of NDH-related CEF. We observed similar increases in CEF, as well as increases in H2O2 accumulation, in other translation defective mutants. This suggests that loss of coordination in plastid protein levels lead to imbalances in photosynthetic energy balance that leads to an increase in CEF. These results taken together with a large body of previous observations, support a general model in which processes that lead to imbalances in chloroplast energetics result in the production of H2O2, which in turn activates CEF. This activation could be from either H2O2 acting as a redox signal, or by a secondary effect from H2O2 inducing a deficit in ATP.

Cyanobacterial Alkanes Modulate Photosynthetic Cyclic Electron Flow to Assist Growth under Cold Stress.

All cyanobacterial membranes contain diesel-range C15-C19 hydrocarbons at concentrations similar to chlorophyll. Recently, two universal but mutually exclusive hydrocarbon production pathways in cyanobacteria were discovered. We engineered a mutant of Synechocystis sp. PCC 6803 that produces no alkanes, which grew poorly at low temperatures. We analyzed this defect by assessing the redox kinetics of PSI. The mutant exhibited enhanced cyclic electron flow (CEF), especially at low temperature. CEF raises the ATP:NADPH ratio from photosynthesis and balances reductant requirements of biosynthesis with maintaining the redox poise of the electron transport chain. We conducted in silico flux balance analysis and showed that growth rate reaches a distinct maximum for an intermediate value of CEF equivalent to recycling 1 electron in 4 from PSI to the plastoquinone pool. Based on this analysis, we conclude that the lack of membrane alkanes causes higher CEF, perhaps for maintenance of redox poise. In turn, increased CEF reduces growth by forcing the cell to use less energy-efficient pathways, lowering the quantum efficiency of photosynthesis. This study highlights the unique and universal role of medium-chain hydrocarbons in cyanobacterial thylakoid membranes: they regulate redox balance and reductant partitioning in these oxygenic photosynthetic cells under stress.

Insusceptibility of oxygen-evolving complex to high light in Betula platyphylla.

High mountain plants growing at high altitude have to regularly cope with high light and high UV radiation that can lead to photodamage of oxygen-evolving complex (OEC). However, the underlying mechanism of photoprotection for OEC in high mountain plants is unclear. Sun leaves of Betula platyphylla were used to examine whether cyclic electron flow (CEF) around photosystem I (PSI) plays an important role in photoprotection for OEC. Our results indicated that the value of ETRI/ETRII ratio significantly increased under high light. With increasing light intensity, non-photochemical quenching (NPQ) gradually increased, and the fraction of P700 that is oxidized in a given state gradually increased. These results indicated that CEF was significantly activated under high light. After treatment with a high light of 1600 μmol photons m(-2) s(-1) for 8 h, the OEC activity did not decline, but the maximum quantum yield of PSII (F v /F m ) ratio significantly decreased. These results suggested that CEF-dependent generation of proton gradient across thylakoid membrane protected OEC activity against high light. Furthermore, the stability of PSI activity during exposure to high light suggested that the high CEF activity in B. platyphylla played an important role in photoprotection for PSI activity.

Wheat-Aegilops biuncialis amphiploids have efficient photosynthesis and biomass production during osmotic stress

Osmotic stress responses of water content, photosynthetic parameters and biomass production were investigated in wheat-Aegilops biuncialis amphiploids and in wheat genotypes to clarify whether they can use to improve the drought tolerance of bread wheat. A decrease in the osmotic pressure of the medium resulted in considerable water loss, stomatal closure and a decreased CO2 assimilation rate for the wheat genotypes, while the changes in these parameters were moderate for the amphiploids. Maximal assimilation rate was maintained at high level even under severe osmotic stress in the amphiploids, while it decreased substantially in the wheat genotypes. Nevertheless, the effective quantum yield of PS II was higher and the quantum yield of non-photochemical quenching of PS II and PS I was lower for the amphiploids than for the wheat cultivars. Parallel with this, higher cyclic electron flow was detected in wheat than in the amphiploids. The elevated photosynthetic activity of amphiploids under osmotic stress conditions was manifested in higher biomass production by roots and shoots as compared to wheat genotypes. These results indicate that the drought-tolerant traits of Ae. biuncialis can be manifested in the wheat genetic background and these amphiploids are suitable genetic materials for improving drought tolerance of wheat.

Reflectance and Cyclic Electron Flow as an Indicator of Drought Stress in Cotton (Gossypium hirsutum)

The response and the functioning of the photosynthetic machinery of cotton, Gossypium hirsutum during water stress was studied by leaf optical properties, linear (ETRII) and cyclic electron flow (CEF) and chlorophyll a fluorescence. We observed that in G. hirsutum, during water limitation, Chlorophyll b showed the best correlation with reflectance at 731nm and is a better indicator of drought. Fv /Fm was observed to be very insensitive to mild water stress. However, during severe water stress the leaves exhibit considerable inhibition in Fv /Fm and an increase in anthocyanin levels by about 20-fold. CEF was very responsive to mild water stress. The mild drought stress caused large decrease in the ability of the leaves to utilize the light energy. Photosystem I and photosystem II is protected from photoinhibition by high CEF and nonphotochemical quenching under mild water stress. While during severe drought stress, linear electron flow showed a sharp decrease in comparison to CEF. CEF play a major role in G. hirsutum leaves during mild as well as under severe water stress condition and is thus a good indicator of water stress.

Dissipation of excess photosynthetic energy contributes to salinity tolerance: A comparative study of salt-tolerant Ricinus communis and salt-sensitive Jatropha curcas

The relationships between salt tolerance and photosynthetic mechanisms of excess energy dissipation were assessed using two species that exhibit contrasting responses to salinity, Ricinus communis (tolerant) and Jatropha curcas (sensitive). The salt tolerance of R. communis was indicated by unchanged electrolyte leakage (cellular integrity) and dry weight in leaves, whereas these parameters were greatly affected in J. curcas. The leaf Na+ content was similar in both species. Photosynthesis was intensely decreased in both species, but the reduction was more pronounced in J. curcas. In this species biochemical limitations in photosynthesis were more prominent, as indicated by increased Ci values and decreased Rubisco activity. Salinity decreased both the Vcmax (in vivo Rubisco activity) and Jmax (maximum electron transport rate) more significantly in J. curcas. The higher tolerance in R. communis was positively associated with higher photorespiratory activity, nitrate assimilation and higher cyclic electron flow. The high activity of these alternative electron sinks in R. communis was closely associated with a more efficient photoprotection mechanism. In conclusion, salt tolerance in R. communis, compared with J. curcas, is related to higher electron partitioning from the photosynthetic electron transport chain to alternative sinks.

Two distinct strategies of cotton and soybean differing in leaf movement to perform photosynthesis under drought in the field.

This paper reports an experimental test of the hypothesis that cotton and soybean differing in leaf movement have distinct strategies to perform photosynthesis under drought. Cotton and soybean were exposed to two water regimes: drought stressed and well watered. Drought-stressed cotton and soybean had lower maximum CO2 assimilation rates than well-watered (control) plants. Drought reduced the light saturation point and photorespiration of both species - especially in soybean. Area-based leaf nitrogen decreased in drought-stressed soybean but increased in drought-stressed cotton. Drought decreased PSII quantum yield (ΦPSII) in soybean leaves, but increased ΦPSII in cotton leaves. Drought induced an increase in light absorbed by the PSII antennae that is dissipated thermally via ΔpH- and xanthophylls-regulated processes in soybean leaves, but a decrease in cotton leaves. Soybean leaves appeared to have greater cyclic electron flow (CEF) around PSI than cotton leaves and drought further increased CEF in soybean leaves. In contrast, CEF slightly decreased in cotton under drought. These results suggest that the difference in leaf movement between cotton and soybean leaves gives rise to different strategies to perform photosynthesis and to contrasting photoprotective mechanisms for utilisation or dissipation of excess light energy. We suggest that soybean preferentially uses light-regulated non-photochemical energy dissipation, which may have been enhanced by the higher CEF in drought-stressed leaves. In contrast, cotton appears to rely on enhanced electron transport flux for light energy utilisation under drought, for example, in enhanced nitrogen assimilation.

Sinks for photosynthetic electron flow in green petioles and pedicels of Zantedeschia aethiopica: evidence for innately high photorespiration and cyclic electron flow rates

A combination of gas exchange and various chlorophyll fluorescence measurements under varying O(2) and CO(2) partial pressures were used to characterize photosynthesis in green, stomata-bearing petioles of Zantedeschia aethiopica (calla lily) while corresponding leaves served as controls. Compared to leaves, petioles displayed considerably lower CO(2) assimilation rates, limited by both stomatal and mesophyll components. Further analysis of mesophyll limitations indicated lower carboxylating efficiencies and insufficient RuBP regeneration but almost similar rates of linear electron transport. Accordingly, higher oxygenation/carboxylation ratios were assumed for petioles and confirmed by experiments under non-photorespiratory conditions. Higher photorespiration rates in petioles were accompanied by higher cyclic electron flow around PSI, the latter being possibly linked to limitations in electron transport from intermediate electron carriers to end acceptors and low contents of PSI. Based on chlorophyll fluorescence methods, similar conclusions can be drawn for green pedicels, although gas exchange in these organs could not be applied due to their bulky size. Since our test plants were not subjected to stress we argue that higher photorespiration and cyclic electron flow rates are innate attributes of photosynthesis in stalks of calla lily. Active nitrogen metabolism may be inferred, while increased cyclic electron flow may provide the additional ATP required for the enhanced photorespiratory activity in petiole and pedicel chloroplasts and/or the decarboxylation of malate ascending from roots.

An Arabidopsis mutant with high cyclic electron flow around photosystem I (hcef) involving the NADPH dehydrogenase complex.

Cyclic electron flow (CEFI) has been proposed to balance the chloroplast energy budget, but the pathway, mechanism, and physiological role remain unclear. We isolated a new class of mutant in Arabidopsis thaliana, hcef for high CEF1, which shows constitutively elevated CEF1. The first of these, hcef1, was mapped to chloroplast fructose-1,6-bisphosphatase. Crossing hcef1 with pgr5, which is deficient in the antimycin A-sensitive pathway for plastoquinone reduction, resulted in a double mutant that maintained the high CEF1 phenotype, implying that the PGR5-dependent pathway is not involved. By contrast, crossing hcef1 with crr2-2, deficient in thylakoid NADPH dehydrogenase (NDH) complex, results in a double mutant that is highly light sensitive and lacks elevated CEF1, suggesting that NDH plays a direct role in catalyzing or regulating CEF1. Additionally, the NdhI component of the NDH complex was highly expressed in hcef1, whereas other photosynthetic complexes, as well as PGR5, decreased. We propose that (1) NDH is specifically upregulated in hcef1, allowing for increased CEF1; (2) the hcef1 mutation imposes an elevated ATP demand that may trigger CEF1; and (3) alternative mechanisms for augmenting ATP cannot compensate for the loss of CEF1 through NDH.