Metabolic flux from the chloroplast provides signals controlling photosynthetic acclimation to cold in Arabidopsis thaliana

Photosynthesis is especially sensitive to environmental conditions, and the composition of the photosynthetic apparatus can be modulated in response to environmental change, a process termed photosynthetic acclimation. Previously, we identified a role for a cytosolic fumarase, FUM2 in acclimation to low temperature in Arabidopsis thaliana. Mutant lines lacking FUM2 were unable to acclimate their photosynthetic apparatus to cold. Here, using gas exchange measurements and metabolite assays of acclimating and non‐acclimating plants, we show that acclimation to low temperature results in a change in the distribution of photosynthetically fixed carbon to different storage pools during the day. Proteomic analysis of wild‐type Col‐0 Arabidopsis and of a fum2 mutant, which was unable to acclimate to cold, indicates that extensive changes occurring in response to cold are affected in the mutant. Metabolic and proteomic data were used to parameterize metabolic models. Using an approach called flux sampling, we show how the relative export of triose phosphate and 3‐phosphoglycerate provides a signal of the chloroplast redox state that could underlie photosynthetic acclimation to cold.     

Interaction of Temperature and Light in the Development of Freezing Tolerance in Plants

Freezing tolerance is the result of a wide range of physical and biochemical processes, such as the induction of antifreeze proteins, changes in membrane composition, the accumulation of osmoprotectants, and changes in the redox status, which allow plants to function at low temperatures. Even in frost-tolerant species, a certain period of growth at low but nonfreezing temperatures, known as frost or cold hardening, is required for the development of a high level of frost hardiness. It has long been known that frost hardening at low temperature under low light intensity is much less effective than under normal light conditions; it has also been shown that elevated light intensity at normal temperatures may partly replace the cold-hardening period. Earlier results indicated that cold acclimation reflects a response to a chloroplastic redox signal while the effects of excitation pressure extend beyond photosynthetic acclimation, influencing plant morphology and the expression of certain nuclear genes involved in cold acclimation. Recent results have shown that not only are parameters closely linked to the photosynthetic electron transport processes affected by light during hardening at low temperature, but light may also have an influence on the expression level of several other cold-related genes; several cold-acclimation processes can function efficiently only in the presence of light. The present review provides an overview of mechanisms that may explain how light improves the freezing tolerance of plants during the cold-hardening period.     

The hidden function of photosynthesis: a sensing system for environmental conditions that regulates plant acclimation responses

Plants convert light energy from the sun into chemical energy by photosynthesis. Since they are sessile, they have to deal with a wide range of conditions in their immediate environment. Many abiotic and biotic parameters exhibit considerable fluctuations which can have detrimental effects especially on the efficiency of photosynthetic light harvesting. During evolution, plants, therefore, evolved a number of acclimation processes which help them to adapt photosynthesis to such environmental changes. This includes protective mechanisms such as excess energy dissipation and processes supporting energy redistribution, e.g. state transitions or photosystem stoichiometry adjustment. Intriguingly, all these responses are triggered by photosynthesis itself via the interplay of its light reaction and the Calvin–Benson cycle with the residing environmental condition. Thus, besides its primary function in harnessing and converting light energy, photosynthesis acts as a sensing system for environmental changes that controls molecular acclimation responses which adapt the photosynthetic function to the environmental change. Important signalling parameters directly or indirectly affected by the environment are the pH gradient across the thylakoid membrane and the redox states of components of the photosynthetic electron transport chain and/or electron end acceptors coupled to it. Recent advances demonstrate that these signals control post-translational modifications of the photosynthetic protein complexes and also affect plastid and nuclear gene expression machineries as well as metabolic pathways providing a regulatory framework for an integrated response of the plant to the environment at all cellular levels.     

The hidden function of photosynthesis: a sensing system for environmental conditions that regulates plant acclimation responses

Plants convert light energy from the sun into chemical energy by photosynthesis. Since they are sessile, they have to deal with a wide range of conditions in their immediate environment. Many abiotic and biotic parameters exhibit considerable fluctuations which can have detrimental effects especially on the efficiency of photosynthetic light harvesting. During evolution, plants, therefore, evolved a number of acclimation processes which help them to adapt photosynthesis to such environmental changes. This includes protective mechanisms such as excess energy dissipation and processes supporting energy redistribution, e.g. state transitions or photosystem stoichiometry adjustment. Intriguingly, all these responses are triggered by photosynthesis itself via the interplay of its light reaction and the Calvin-Benson cycle with the residing environmental condition. Thus, besides its primary function in harnessing and converting light energy, photosynthesis acts as a sensing system for environmental changes that controls molecular acclimation responses which adapt the photosynthetic function to the environmental change. Important signalling parameters directly or indirectly affected by the environment are the pH gradient across the thylakoid membrane and the redox states of components of the photosynthetic electron transport chain and/or electron end acceptors coupled to it. Recent advances demonstrate that these signals control post-translational modifications of the photosynthetic protein complexes and also affect plastid and nuclear gene expression machineries as well as metabolic pathways providing a regulatory framework for an integrated response of the plant to the environment at all cellular levels.     

植物对大气CO2浓度升高的光合适应机理

光合作用对大气中CO2浓度升高适应的可能原因主要表现在以下几个方面:由于CO2浓度升高,碳水化合物过量积累,光合电子传递链中质体醌与过氧化氢(H2O2)的氧化还原信号对光合作用发生反馈抑制;核酮糖1,5-二磷酸羧化/加氧酶(Rubisco)的含量及其活性下降;气孔状态发生变化.此外,植物体内C/N平衡、生长调节物质和己糖激酶对光合基因表达水平的调控等多个方面会对光合适应产生影响.     

植物对大气CO2 浓度升高的光合适应机理

光合作用对大气中CO2浓度升高适应的可能原因主要表现在以下几个方面: 由于CO2浓度升高,碳水化合物过量积累, 光合电子传递链中质体醌与过氧化氢(H2O2)的氧化还原信号对光合作用发生反馈抑制; 核酮糖1,5-二磷酸羧化/加氧酶(Rubisco)的含量及其活性下降; 气孔状态发生变化。此外, 植物体内C/N平衡、生长调节物质和己糖激酶对光合基因表达水平的调控等多个方面会对光合适应产生影响。     

Effects of MPK3 and MPK6 kinases on the chloroplast architecture and function induced by cold acclimation in Arabidopsis

Photosynthesis Research - Exposure to low, non-freezing temperatures develops freezing tolerance in many plant species. Such process is called cold acclimation. Molecular changes undergone during...     

Hypothesis: A binary redox control mode as universal regulator of photosynthetic light acclimation

In nature, plants experience considerable changes in the prevailing illumination, which can drastically reduce photosynthetic efficiency and yield. Such adverse effects are counterbalanced by acclimation responses which ensure high photosynthetic productivity by structural reconfiguration of the photosynthetic apparatus. Those acclimation responses are controlled by reduction-oxidation (redox) signals from two pools of redox compounds, the plastoquinone and the thioredoxin pools. The relative impact of these two redox signaling systems on this process, however, remains controversial. Recently, we showed that photosynthesis controls nuclear gene expression and cellular metabolite states in an integrated manner, thus, stabilizing the varying energetic demands of the plant. Here, we propose a novel model based on a binary redox control mode to explain adaptation of plant primary productivity to the light environment. Plastoquinone and thioredoxin pools are proposed to define specific environmental situations cooperatively and to initiate appropriate acclimation responses controlled by four binary combinations of their redox states. Our model indicates a hierarchical redox regulation network that controls plant primary productivity and supports the notion that photosynthesis is an environmental sensor affecting plant growth and development.Key words: photosynthetic light acclimation, redox control, sensor function, arabidopsis, plant fitness     

Chloroplast redox signals: how photosynthesis controls its own genes

The photosynthetic apparatus of higher plants and algae is composed of plastid- and nuclear-encoded components, therefore the expression of photosynthesis genes needs to be highly coordinated. Expression is regulated by various factors, one of the most important of which is light. Photosynthesis functions as a sensor for such light signals, and the redox state of photosynthetic electron transport components and redox-active soluble molecules act as regulating parameters. This provides a feedback response loop in which the expression of photosynthesis genes is coupled to the function of the photosynthetic process, and highlights the dual role of photosynthesis in energy fixation and the reception of environmental information.     

A plant for all seasons: alterations in photosynthetic carbon metabolism during cold acclimation in Arabidopsis

Low temperatures lead to the inhibition of sucrose synthesis and photosynthesis. The biochemical and physiological adaptations of plants to low temperatures include the post-translational activation and increased expression of enzymes of the sucrose synthesis pathway, the changed expression of Calvin cycle enzymes, and changes in the leaf protein content. Recent progress has been made in understanding both the signals that trigger these processes and how the regulation of photosynthetic carbon metabolism interacts with other processes during cold acclimation.     

Effect of light on photosynthetic capacity during cold acclimation in a cold-sensitive and a cold-tolerant potato species

The effect of low temperature acclimation at various light levels on the photosynthetic capacity of Solanum species was examined. Two species, Solanum tuberosum L. cv. Red Pontiac and Solanum acaule Bitt., which differ significantly in degree of frost-tolerance and in their ability to acclimate to low temperature stress, were compared. Acclimation conditions included 5/2°C (day/night) temperatures, and either moderate (400 · mol · m⁻²· s⁻¹) or low (40 · mol · m⁻²· s⁻¹) photosynthetic photon flux densities. Several parameters of photosynthesis were measured in tissue pieces during acclimation treatments including chlorophyll content, chlorophyll a/b ratios and carbon dioxide-saturated photosynthetic oxygen evolution during light-limited and light-saturated assays.
Most measured photosynthetic parameters of low temperature-grown plants of both species showed greater declines under the moderate light than the low light conditions. Chlorophyll a/b ratios were unchanged after low temperature exposures in both light level treatments. At low temperatures, the cold-sensitive S. tuberosum demonstrated a greater inhibition of photosynthetic capacity in light- and carbon dioxide-saturated assays than S. acaule at all light levels. In addition to a pronounced inhibition at the higher light level, S. tuberosum demonstrated a very strong inhibition of photosynthetic capacity at very low light levels. Our results suggest a correlation between ability to maintain essential metabolic processes during low temperature stress in the presence of moderate light levels and the ability to increase cold tolerance.     

Thermal acclimation of photosynthesis: on the importance of adjusting our definitions and accounting for thermal acclimation of respiration

While interest in photosynthetic thermal acclimation has been stimulated by climate warming, comparing results across studies requires consistent terminology. We identify five types of photosynthetic adjustments in warming experiments: photosynthesis as measured at the high growth temperature, the growth temperature, and the thermal optimum; the photosynthetic thermal optimum; and leaf-level photosynthetic capacity. Adjustments of any one of these variables need not mean a concurrent adjustment in others, which may resolve apparently contradictory results in papers using different indicators of photosynthetic acclimation. We argue that photosynthetic thermal acclimation (i.e., that benefits a plant in its new growth environment) should include adjustments of both the photosynthetic thermal optimum (T _opt) and photosynthetic rates at the growth temperature (A _growth), a combination termed constructive adjustment. However, many species show reduced photosynthesis when grown at elevated temperatures, despite adjustment of some photosynthetic variables, a phenomenon we term detractive adjustment. An analysis of 70 studies on 103 species shows that adjustment of T _opt and A _growth are more common than adjustment of other photosynthetic variables, but only half of the data demonstrate constructive adjustment. No systematic differences in these patterns were found between different plant functional groups. We also discuss the importance of thermal acclimation of respiration for net photosynthesis measurements, as respiratory temperature acclimation can generate apparent acclimation of photosynthetic processes, even if photosynthesis is unaltered. We show that while dark respiration is often used to estimate light respiration, the ratio of light to dark respiration shifts in a non-predictable manner with a change in leaf temperature.     

Controlled levels of salicylic acid are required for optimal photosynthesis and redox homeostasis

Sudden exposure of plants to high light (HL) leads to metabolic and physiological disruption of the photosynthetic cells. Changes in ROS content, adjustment of photosynthetic processes and the antioxidant pools and, ultimately, gene induction are essential components for a successful acclimation to the new light conditions. The influence of salicylic acid (SA) on plant growth, short-term acclimation to HL, and on the redox homeostasis of Arabidopsis thaliana leaves was assessed here. The dwarf phenotype displayed by mutants with high SA content (cpr1-1, cpr5-1, cpr6-1, and dnd1-1) was less pronounced when these plants were grown in HL, suggesting that the inhibitory effect of SA on growth was partly overcome at higher light intensities. Moreover, higher SA content affected energy conversion processes in low light, but did not impair short-term acclimation to HL. On the other hand, mutants with low foliar SA content (NahG and sid2-2) were impaired in acclimation to transient exposure to HL and thus predisposed to oxidative stress. Low and high SA levels were strictly correlated to a lower and higher foliar H(2)O(2) content, respectively. Furthermore high SA was also associated with higher GSH contents, suggesting a tight correlation between SA, H(2)O(2) and GSH contents in plants. These observations implied an essential role of SA in the acclimation processes and in regulating the redox homeostasis of the cell. Implications for the role of SA in pathogen defence signalling are also discussed.     

Subcellular reprogramming of metabolism during cold acclimation in Arabidopsis thaliana

Metabolite changes in plant leaves during exposure to low temperatures involve re‐allocation of a large number of metabolites between sub‐cellular compartments. Therefore, metabolite determination at the whole cell level may be insufficient for interpretation of the functional significance of cellular compounds. To investigate the cold‐induced metabolite dynamics at the level of individual sub‐cellular compartments, an integrative platform was developed that combines quantitative metabolite profiling by gas chromatography coupled to mass spectrometry (GC‐MS) with the non‐aqueous fractionation technique allowing separation of cytosol, vacuole and the plastidial compartment. Two mutants of Arabidopsis thaliana representing antipodes in the diversion of carbohydrate metabolism between sucrose and starch were compared to Col‐0 wildtype before and after cold acclimation to investigate interactions of cold acclimation with subcellular re‐programming of metabolism. A multivariate analysis of the data set revealed dominant effects of compartmentation on metabolite concentrations that were modulated by environmental condition and genetic determinants. While for both, the starchless mutant of plastidial phospho‐gluco mutase (pgm) and a mutant defective in sucrose‐phosphate synthase A1, metabolic constraints, especially at low temperature, could be uncovered based on subcellularly resolved metabolite profiles, only pgm had lowered freezing tolerance. Metabolic profiles of pgm point to redox imbalance as a possible reason for reduced cold acclimation capacity.     

Cold acclimation of Arabidopsis thaliana results in incomplete recovery of photosynthetic capacity, associated with an increased reduction of the chloroplast stroma

The effects of short-term cold stress and long-term cold acclimation on the light reactions of photosynthesis were examined in vivo to assess their contributions to photosynthetic acclimation to low temperature in Arabidopsis thaliana (L.) Heynh.. All photosynthetic measurements were made at the temperature of exposure: 23 degrees C for non-acclimated plants and 5 degrees C for cold-stressed and cold-acclimated plants. Three-day cold-stress treatments at 5 degrees C inhibited light-saturated rates of CO2 assimilation and O2 evolution by approximately 75%. The 3-day exposure to 5 degrees C also increased the proportion of reduced QA by 50%, decreased the yield of PSII electron transport by 65% and decreased PSI activity by 31%. In contrast, long-term cold acclimation resulted in a strong but incomplete recovery of light-saturated photosynthesis at 5 degrees C. The rates of light-saturated CO2 and O2 gas exchange and the in vivo yield of PSII activity under light-saturating conditions were only 35-40% lower, and the relative redox state of QA only 20% lower, at 5 degrees C after cold acclimation than in controls at 23 degrees C. PSI activity showed full recovery during long-term cold acclimation. Neither short-term cold stress nor long-term cold acclimation of Arabidopsis was associated with a limitation in ATP, and both treatments resulted in an increase in the ATP/NADPH ratio. This increase in ATP/NADPH was associated with an inhibition of PSI cyclic electron transport but there was no apparent change in the Mehler reaction activity in either cold-stressed or cold-acclimated leaves. Cold acclimation also resulted in an increase in the reduction state of the stroma, as indicated by an increased total activity and activation state of NADP-dependent malate dehydrogenase, and increased light-dependent activities of the major regulatory enzymes of the oxidative pentose-phosphate pathway. We suggest that the photosynthetic capacity during cold stress as well as cold acclimation is altered by limitations at the level of consumption of reducing power in carbon metabolism.