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Despite our increasingly sophisticated understanding of mechanisms ensuring efficient photosynthesis under laboratory-controlled light conditions, less is known about the regulation of photosynthesis under fluctuating light. This is important because-in nature-photosynthetic organisms experience rapid and extreme changes in sunlight, potentially causing deleterious effects on photosynthetic efficiency and productivity. Here we report that the chloroplast thylakoid lumenal protein MAINTENANCE OF PHOTOSYSTEM II UNDER HIGH LIGHT 2 (MPH2; encoded by At4g02530 ) is required for growth acclimation of Arabidopsis thaliana plants under controlled photoinhibitory light and fluctuating light environments. Evidence is presented that mph2 mutant light stress susceptibility results from a defect in photosystem II (PSII) repair, and our results are consistent with the hypothesis that MPH2 is involved in disassembling monomeric complexes during regeneration of dimeric functional PSII supercomplexes. Moreover, mph2 -and previously characterized PSII repair-defective mutants-exhibited reduced growth under fluctuating light conditions, while PSII photoprotection-impaired mutants did not. These findings suggest that repair is not only required for PSII maintenance under static high-irradiance light conditions but is also a regulatory mechanism facilitating photosynthetic adaptation under fluctuating light environments. This work has implications for improvement of agricultural plant productivity through engineering PSII repair., Competing Interests: The authors declare no conflict of interest.

The flavodiiron proteins (FDPs) Flv1 and Flv3 in cyanobacteria function in photoreduction of O 2 to H 2 O, without concomitant formation of reactive oxygen species, known as the Mehler-like reaction. Both Flv1 and Flv3 are essential for growth under fluctuating light (FL) intensities, providing protection for PSI. Here we compared the global transcript profiles of the wild type (WT), Δflv1 and Δflv1/Δflv3 grown under constant light (GL) and FL. In the WT, FL induced the largest down-regulation in transcripts involved in carbon-concentrating mechanisms (CCMs), while those of the nitrogen assimilation pathways increased as compared with GL. Already under GL the Δflv1/Δflv3 double mutant demonstrated a partial down-regulation of transcripts for CCM and nitrogen metabolism, while in FL conditions the transcripts for nitrogen assimilation were strongly down-regulated. Many alterations were specific only for Δflv1/Δflv3, and not detected in Δflv1, suggesting that certain transcripts are affected primarily because of the lack of flv3 By constructing the strains overproducing solely either Flv1 or Flv3, we demonstrate that the homo-oligomers of these proteins also function in acclimation of cells to FL, by catalyzing reactions with as yet unidentified components, while the presence of both Flv1 and Flv3 is a prerequisite for the Mehler-like reaction and thus the electron transfer to O 2 Considering the low expression of flv1, it is unlikely that the Flv1 homo-oligomer is present in the WT., (© The Author 2016. Published by Oxford University Press on behalf of Japanese Society of Plant Physiologists.)

Plants have adopted a number of mechanisms to restore redox homeostasis in the chloroplast under fluctuating light conditions in nature. Chloroplast thioredoxin systems are crucial components of this redox network, mediating environmental signals to chloroplast proteins. In the reduced state, thioredoxins control the structure and function of proteins by reducing disulfide bridges in the redox active site of a protein. Subsequently, an oxidized thioredoxin is reduced by a thioredoxin reductase, the two enzymes together forming a thioredoxin system. Plant chloroplasts have versatile thioredoxin systems, including two reductases dependent on ferredoxin and NADPH as reducing power, respectively, several types of thioredoxins, and the system to deliver thiol redox signals to the thylakoid membrane and lumen. Light controls the activity of chloroplast thioredoxin systems in two ways. First, light reactions activate the thioredoxin systems via donation of electrons to oxidized ferredoxin and NADP(+), and second, light induces production of reactive oxygen species in chloroplasts which deactivate the components of the thiol redox network. The diversity and partial redundancy of chloroplast thioredoxin systems enable chloroplast metabolism to rapidly respond to ever-changing environmental conditions and to raise plant fitness in natural growth conditions.

Plants contain three NADPH‐thioredoxin reductases (NTR) located in the cytosol/mitochondria (NTRA/B) and the plastid (NTRC) with important metabolic functions. However, mutants deficient in all NTRs remained to be investigated. Here, we generated and characterised the triple Arabidopsis ntrabc mutant alongside with ntrc single and ntrab double mutants under different environmental conditions. Both ntrc and ntrabc mutants showed reduced growth and substantial metabolic alterations, especially in sink leaves and under high CO2 (HC), as compared to the wild type. However, ntrabc showed higher effective quantum yield of PSII under both constant and fluctuating light conditions, altered redox states of NADH/NAD+ and glutathione (GSH/GSSG) and lower potential quantum yield of PSII in sink leaves in ambient but not high CO2 concentrations, as compared to ntrc, suggesting a functional interaction between chloroplastic and extra‐chloroplastic NTRs in photosynthesis regulation depending on leaf development and environmental conditions. Our results unveil a previously unknown role of the NTR system in regulating sink leaf metabolism and plant acclimation to HC, while it is not affecting full plant development, indicating that the lack of the NTR system can be compensated, at least to some extent, by other redox mechanisms. Summary Statement: We unveil that NTRC is crucial for sink leaf metabolism and plant acclimation to high CO2. Although Arabidopsis plants lacking all NADPH‐thioredoxin reductases (NTRs) have severely reduced growth, they produced viable seeds, indicating that NTRs are not essential for plant development and compensated by other redox mechanisms. [ABSTRACT FROM AUTHOR]

Plants contain three NADPH‐thioredoxin reductases (NTR) located in the cytosol/mitochondria (NTRA/B) and the plastid (NTRC) with important metabolic functions. However, mutants deficient in all NTRs remained to be investigated. Here, we generated and characterised the triple Arabidopsis ntrabc mutant alongside with ntrc single and ntrab double mutants under different environmental conditions. Both ntrc and ntrabc mutants showed reduced growth and substantial metabolic alterations, especially in sink leaves and under high CO2 (HC), as compared to the wild type. However, ntrabc showed higher effective quantum yield of PSII under both constant and fluctuating light conditions, altered redox states of NADH/NAD+ and glutathione (GSH/GSSG) and lower potential quantum yield of PSII in sink leaves in ambient but not high CO2 concentrations, as compared to ntrc, suggesting a functional interaction between chloroplastic and extra‐chloroplastic NTRs in photosynthesis regulation depending on leaf development and environmental conditions. Our results unveil a previously unknown role of the NTR system in regulating sink leaf metabolism and plant acclimation to HC, while it is not affecting full plant development, indicating that the lack of the NTR system can be compensated, at least to some extent, by other redox mechanisms. Summary Statement: We unveil that NTRC is crucial for sink leaf metabolism and plant acclimation to high CO2. Although Arabidopsis plants lacking all NADPH‐thioredoxin reductases (NTRs) have severely reduced growth, they produced viable seeds, indicating that NTRs are not essential for plant development and compensated by other redox mechanisms. [ABSTRACT FROM AUTHOR]

Acclimation of photosynthesis to light intensity (photoacclimation) takes days to achieve and so naturally fluctuating light presents a potential challenge where leaves may be exposed to light conditions that are beyond their window of acclimation. Experiments generally have focused on unchanging light with a relatively fixed combination of photosynthetic attributes to confer higher efficiency in those conditions. Here a controlled LED experiment and mathematical modelling was used to assess the acclimation potential of contrasting Arabidopsis thaliana genotypes following transfer to a controlled fluctuating light environment, designed to present frequencies and amplitudes more relevant to natural conditions. We hypothesize that acclimation of light harvesting, photosynthetic capacity and dark respiration are controlled independently. Two different ecotypes were selected, Wassilewskija-4 (Ws), Landsberg erecta (Ler) and a GPT2 knock out mutant on the Ws background (gpt2-), based on their differing abilities to undergo dynamic acclimation i.e. at the sub-cellular or chloroplastic scale. Results from gas exchange and chlorophyll content indicate that plants can independently regulate different components that could optimize photosynthesis in both high and low light; targeting light harvesting in low light and photosynthetic capacity in high light. Empirical modelling indicates that the pattern of 'entrainment' of photosynthetic capacity by past light history is genotype-specific. These data show flexibility of photoacclimation and variation useful for plant improvement. [ABSTRACT FROM AUTHOR]

Photosynthesis involves a series of redox reactions and is the major source of reactive oxygen species in plant cells. Fluctuating light (FL) levels, which occur commonly in natural environments, affect photosynthesis; however, little is known about the specific effects of FL on the redox regulation of photosynthesis. Here, we performed global quantitative mapping of the Arabidopsis thaliana cysteine thiol redox proteome under constant light and FL conditions. We identified 8857 redox‐switched thiols in 4350 proteins, and 1501 proteins that are differentially modified depending on light conditions. Notably, proteins related to photosynthesis, especially photosystem I (PSI), are operational thiol‐switching hotspots. Exposure of wild‐type A. thaliana to FL resulted in decreased PSI abundance, stability, and activity. Interestingly, in response to PSI photodamage, more of the PSI assembly factor PSA3 dynamically switches to the reduced state. Furthermore, the Cys199 and Cys200 sites in PSA3 are necessary for its full function. Moreover, thioredoxin m (Trx m) proteins play roles in redox switching of PSA3, and are required for PSI activity and photosynthesis. This study thus reveals a mechanism for redox‐based regulation of PSI under FL, and provides insight into the dynamic acclimation of photosynthesis in a changing environment. [ABSTRACT FROM AUTHOR]

Satellite‐based remote sensing allows for global estimates of phytoplankton primary productivity by converting measurements of ocean color or photon absorption into units of carbon fixation. Models which perform this conversion often require an estimate of phytoplankton photoacclimation state such as the carbon to chlorophyll a ratio (C:Chl). Recently, our group developed a new photoacclimation model that can be applied to models of primary production. The model assumes that the phytoplankton photoacclimation state is not affected by periods of darkness during deep mixing beneath the photic zone, due to reduction in the plastoquinone pool in darkness and the subsequent deactivation of the signal for chlorophyll synthesis. In this study, we tested these assumptions by culturing the marine diatom Thalassiosira weissflogii under fluctuating light conditions simulating three different optical depths with progressively increasing deep mixing periods. The photoacclimation state, measured by the ratio of C:Chl, in T. weissflogii was not affected by changes in the length of simulated deep mixing periods. In addition, analysis of photosynthesis vs. irradiance (PE) curves showed that increases in optical depth caused decreases in both the maximum Chl‐normalized rate of photosynthesis (Pbmax) and in the slope of light‐limited photosynthesis (αb), but had no effect on the half‐saturation irradiance (Ek, another metric of photoacclimation). However, measurements of chlorophyll fluorescence during simulated deep mixing did not support the hypothesis that the PQ pool was reduced during dark periods. Thus, our findings support the use of the photoacclimation model for estimating primary production while suggesting the need for further research into the mechanisms controlling photoacclimation in the upper mixed layer environment of the ocean. [ABSTRACT FROM AUTHOR]

Satellite‐based remote sensing allows for global estimates of phytoplankton primary productivity by converting measurements of ocean color or photon absorption into units of carbon fixation. Models which perform this conversion often require an estimate of phytoplankton photoacclimation state such as the carbon to chlorophyll a ratio (C:Chl). Recently, our group developed a new photoacclimation model that can be applied to models of primary production. The model assumes that the phytoplankton photoacclimation state is not affected by periods of darkness during deep mixing beneath the photic zone, due to reduction in the plastoquinone pool in darkness and the subsequent deactivation of the signal for chlorophyll synthesis. In this study, we tested these assumptions by culturing the marine diatom Thalassiosira weissflogii under fluctuating light conditions simulating three different optical depths with progressively increasing deep mixing periods. The photoacclimation state, measured by the ratio of C:Chl, in T. weissflogii was not affected by changes in the length of simulated deep mixing periods. In addition, analysis of photosynthesis vs. irradiance (PE) curves showed that increases in optical depth caused decreases in both the maximum Chl‐normalized rate of photosynthesis (Pbmax) and in the slope of light‐limited photosynthesis (αb), but had no effect on the half‐saturation irradiance (Ek, another metric of photoacclimation). However, measurements of chlorophyll fluorescence during simulated deep mixing did not support the hypothesis that the PQ pool was reduced during dark periods. Thus, our findings support the use of the photoacclimation model for estimating primary production while suggesting the need for further research into the mechanisms controlling photoacclimation in the upper mixed layer environment of the ocean. [ABSTRACT FROM AUTHOR]

Plants in natural environments receive light through sunflecks, the duration and distribution of these being highly variable across the day. Consequently, plants need to adjust their photosynthetic processes to avoid photoinhibition and maximize yield. Changes in the composition of the photosynthetic apparatus in response to sustained changes in the environment are referred to as photosynthetic acclimation, a process that involves changes in protein content and composition. Considering this definition, acclimation differs from regulation, which involves processes that alter the activity of individual proteins over short-time periods, without changing the abundance of those proteins. The interconnection and overlapping of the short- and long-term photosynthetic responses, which can occur simultaneously or/and sequentially over time, make the study of long-term acclimation to fluctuating light in plants challenging. In this review we identify short-term responses of plants to fluctuating light that could act as sensors and signals for acclimation responses, with the aim of understanding how plants integrate environmental fluctuations over time and tailor their responses accordingly. Mathematical modeling has the potential to integrate physiological processes over different timescales and to help disentangle short-term regulatory responses from long-term acclimation responses. We review existing mathematical modeling techniques for studying photosynthetic responses to fluctuating light and propose new methods for addressing the topic from a holistic point of view. [ABSTRACT FROM AUTHOR]

Background: Diatoms contribute 20% of the global primary production and are adaptable in dynamic environments. Diatoms always bloom earlier in the annual phytoplankton succession instead of dinoflagellates. However, how diatoms acclimate to a dynamic environment, especially under changing light conditions, remains unclear. Results: We compared the growth and photosynthesis under fluctuating light conditions of red tide diatom Skeletonema costatum, red tide dinoflagellate Amphidinium carterae, Prorocentrum donghaiense, Karenia mikimotoi, model diatom Phaeodactylum tricornutum, Thalassiosira pseudonana and model dinoflagellate Dinophycae Symbiodinium. Diatoms grew faster and maintained a consistently higher level of photosynthesis. Diatoms were sensitive to the specific inhibitor of Proton Gradient Regulation 5 (PGR5) depending photosynthetic electron flow, which is a crucial mechanism to protect their photosynthetic apparatus under fluctuating light. In contrast, the dinoflagellates were not sensitive to this inhibitor. Therefore, we investigate how PGR5 functions under light fluctuations in the model diatom P. tricornutum by knocking down and overexpressing PGR5. Overexpression of PGR5 reduced the photosystem I acceptor side limitation (Y (NA)) and increased growth rate under severely fluctuating light in contrast to the knockdown of PGR5. Conclusion: Diatoms acclimatize to fluctuating light conditions better than dinoflagellates. PGR5 in diatoms can regulate their photosynthetic electron flow and accelerate their growth under severe light fluctuation, supporting fast biomass accumulation under dynamic environments in pioneer blooms. [ABSTRACT FROM AUTHOR]

In nature, soil salinity and fluctuating light (FL) often occur concomitantly. However, it is unknown whether salt stress interacts with FL on leaf photosynthesis, architecture, biochemistry, pigmentation, mineral concentrations, as well as whole-plant biomass. To elucidate this, tomato (Solanum lycopersicum) seedlings were grown under constant light (C, 200 μmol m−2 s−1) or FL (5-650 μmol m−2 s−1), in combination with no (0 mM NaCl) or moderate (80 mM NaCl) salinity, for 14 days, at identical photoperiods and daily light integrals. FL and salt stress had separate effects on leaf anatomy, biochemistry and photosynthetic capacity: FL reduced leaf thickness as well as nitrogen, chlorophyll and carotenoid contents per unit leaf area, but rarely affected steady-state and dynamic photosynthetic properties along with abundance of key proteins in the electron transport chain. Salt stress, meanwhile, mainly disorganized chloroplast grana stacking, reduced stomatal density, size and aperture as well as photosynthetic capacity. Plant biomass was affected interactively by light regime and salt stress: FL reduced biomass in salt stressed plants by 17%, but it did not affect biomass of non-stressed plants. Our results stress the importance of considering FL when inferring effects of salt-stress on photosynthesis and productivity under fluctuating light intensities. [ABSTRACT FROM AUTHOR]

Plants are subjected to strong fluctuations in light intensity in their natural growth environment, caused both by unpredictable changes due to weather conditions and movement of clouds and upper canopy leaves and predictable changes during day-night cycle. The mechanisms of long-term acclimation to fluctuating light (FL) are still not well understood. Here, we used quantitative mass spectrometry to investigate long-term acclimation of low light-grown Arabidopsis thaliana to a FL condition that induces mild photooxidative stress. On the third day of exposure to FL, young and mature leaves were harvested in the morning and at the end of day for proteome analysis using a stable isotope labeling approach. We identified 2,313 proteins, out of which 559 proteins exhibited significant changes in abundance in at least one of the four experimental groups (morning-young, morning-mature, end-of-day-young, end-of-day-mature). A core set of 49 proteins showed significant responses to FL in three or four experimental groups, which included enhanced accumulation of proteins involved in photoprotection, cyclic electron flow around photosystem I, photorespiration, and glycolysis, while specific glutathione transferases and proteins involved in translation and chlorophyll biosynthesis were reduced in abundance. In addition, we observed pathway- and protein-specific changes predominantly at the end of day, whereas few changes were observed exclusively in the morning. Comparison of the proteome data with the matching transcript data revealed gene- and protein-specific responses, with several chloroplast-localized proteins decreasing in abundance despite increased gene expression under FL. Together, our data shows moderate but widespread alterations of protein abundance during acclimation to FL and suggests an important role of post-transcriptional regulation of protein abundance. [ABSTRACT FROM AUTHOR]

Summary1. The effect of light fluctuations on the growth rates of four species of freshwater phytoplankton was investigated. Experimental light regimes included constant irradiance and fluctuations of a step function form, with equal proportion of high (maximum of 240 µmol photons m-2 s-1) and low light (minimum of 5 µmol photons m-2 s-1) (or dark) in a period. Fluctuations of 1, 8 and 24-h periods were imposed over several average irradiances (25, 50, 100 and 120 µmol photons m-2 s-1). 2. Growth rate responses to fluctuations were species-specific and depended on both the average irradiance and the period of fluctuations. Fluctuations at low average irradiances slightly increased growth rate of the diatom Nitzschia sp. and depressed growth of the cyanobacterium Phormidium luridum and the green alga Sphaerocystis schroeteri compared to a constant irradiance. 3. Fluctuations at higher average irradiance did not have a significant effect on the growth rates of Nitzschia sp. and Sphaerocystis schroeteri (fluctuations around saturating irradiances) and slightly increased the growth rates of the cyanobacteria Anabaena flos-aquae and Phormidium luridum (when irradiance fluctuated between limiting and inhibiting levels). 4. In general, the effect of fluctuations tended to be greater when irradiance fluctuated between limiting and saturating or inhibiting levels of a species growth-irradiance curve compared to fluctuations within a single region of the curve. 5. The growth rates of species under fluctuating light could not always be predicted from their growth-irradiance curves obtained under constant irradiance. When fluctuations occur between limiting and saturating or inhibiting irradiances for the alga and when the period of fluctuations is long (greater than 8 h), steady-state growth-irradiance curves may be insufficient to predict growth rates adequately. Consequently, additional data on physiological acclimation, such as changes in photosynthetic parameters, may be required for predictions under non-constant light supply in comparison to constant conditions. [ABSTRACT FROM AUTHOR]

• A disturbance in photosynthetic electron flow affects the chlorophyll-depleted wheat mutants. • Unexpectedly long-term acclimation to light fluctuations can be allowed in mutants. • Successful development of a fluctuating-light phenotype depends on the mutated locus. • Compensation of the mutation involves use of alternative electron sinks and thylakoid structural re-organization. The search for more productive crops is exploring accessions with reduced chlorophyll accumulation in leaves, which would promote plant growth mainly because of a higher light transmittance throughout the canopy. Under continuous light, chlorophyll-depleted chlorina mutants of wheat can reach yields similar to WT; however, their performance under fluctuating light could possibly be lowered by a disturbed photosynthetic electron transport. Six chlorina mutants of Triticum aestivum (ANBW4A, ANBW4B, ANK32A) or T. durum (ANDW7A, ANDW7B, ANDW8A) were compared to WT genotypes under continuous and fluctuating light regimes, the latter obtained through a randomized pattern of light intensity changes. After two weeks of plant acclimation under either regimes, light energy management was thoroughly analysed for four weeks. All chlorina mutants showed a defective ability to regulate the electron poise during a fast rise in irradiance. Different extent of deregulation depended on mutation and genomic background, durum wheat being more severely impaired than bread wheat. However, a great acclimative capacity to a fluctuating light regime unexpectedly still characterized the chlorina wheat plants, with the only exception of the mutants carrying the cn-B1b mutated locus (ANDW7B and ANBW4B). Under fluctuating light, all other chlorina mutants developed indeed an ability to improve their control of electron transport against the recurrent reducing bursts caused by lightflecks. Compensatory responses included the regulation of energy distribution between photosystems, the use of alternative electron sinks, and a structural reorganization of the thylakoid system. However, in no case a reduced chlorophyll content led to more productive plants. Among 23 measured photosynthetic parameters, especially the non-regulatory energy dissipation in photosystem II - Y(NO) –, when probed during a light rise, can be proposed in automated phenotyping experiments as a straightforward index to be used for chlorina wheat screening with respect to potential productivity. [ABSTRACT FROM AUTHOR]

In forests, understory plants are usually exposed to sunflecks on timescales of seconds or minutes. However, it is unclear how understory plants acclimate to fluctuating light. In this study, we compared chlorophyll fluorescence, PSI redox state and the electrochromic shift signal under fluctuating light between an understory plant Paris polyphylla (Liliaceae) and a light-demanding plant Bletilla striata (Orchidaceae). Within the first seconds after transition from low to high light, PSI was highly oxidized in P. polyphylla but was highly reduced in B. striata , although both species could not generate a sufficient trans-thylakoid proton gradient (ΔpH). Furthermore, the outflow of electrons from PSI to O 2 was not significant in P. polyphylla , as indicated by the P700 redox kinetics upon dark-to-light transition. Therefore, the different responses of PSI to fluctuating light between P. polyphylla and B. striata could not be explained by ΔpH formation or alternative electron transport. In contrast, upon a sudden transition from low to high light, electron flow from PSII was much lower in P. polyphylla than in B. striata , suggesting that the rapid oxidation of PSI in P. polyphylla was largely attributed to the lower PSII activity. We propose, for the first time, that down-regulation of PSII activity is an important strategy used by some understory angiosperms to cope with sunflecks. • PSI is highly oxidized in P. polyphylla upon a sudden transition from low to high light. • The rapid oxidation of PSI in P. polyphylla is not caused by an enough ΔpH. • Alternative electron flow from PSI to O 2 is not significant in P. polyphylla. • P. polyphylla shows low rate of electron flow from PSII under high light. • Down-regulation of PSII activity protects PSI under sunflecks in P. polyphylla. [ABSTRACT FROM AUTHOR]