Acclimation of photosynthesis to lightflecks in tomato leaves: interaction with progressive shading in a growing canopy

Plants in natural environments are often exposed to fluctuations in light intensity, and leaf‐level acclimation to light may be affected by those fluctuations. Concurrently, leaves acclimated to a given light climate can become progressively shaded as new leaves emerge and grow above them. Acclimation to shade alters characteristics such as photosynthetic capacity. To investigate the interaction of fluctuating light and progressive shading, we exposed three‐week old tomato (Solanum lycopersicum ) plants to either lightflecks or constant light intensities. Lightflecks of 20 s length and 1000 μmol m^?2 s^?1 peak intensity were applied every 5 min for 16 h per day, for 3 weeks. Lightfleck and constant light treatments received identical daily light sums (15.2 mol m^?2 day^?1). Photosynthesis was monitored in leaves 2 and 4 (counting from the bottom) during canopy development throughout the experiment. Several dynamic and steady‐state characteristics of photosynthesis became enhanced by fluctuating light when leaves were partially shaded by the upper canopy, but much less so when they were fully exposed to lightflecks. This was the case for CO₂‐saturated photosynthesis rates in leaves 2 and 4 growing under lightflecks 14 days into the treatment period. Also, leaf 2 of plants in the lightfleck treatment showed significantly faster rates of photosynthetic induction when exposed to a stepwise change in light intensity on day 15. As the plants grew larger and these leaves became increasingly shaded, acclimation of leaf‐level photosynthesis to lightflecks disappeared. These results highlight continuous acclimation of leaf photosynthesis to changing light conditions inside developing canopies.     

Effect of light fluctuations on photosynthesis and metabolic flux in Synechocystis sp. PCC 6803

In nature, photosynthetic organisms are exposed to fluctuating light, and their physiological systems must adapt to this fluctuation. To maintain homeostasis, these organisms have a light fluctuation photoprotective mechanism, which functions in both photosystems and metabolism. Although the photoprotective mechanisms functioning in the photosystem have been studied, it is unclear how metabolism responds to light fluctuations within a few seconds. In the present study, we investigated the metabolic response of Synechocystis sp. PCC 6803 to light fluctuations using ¹³C-metabolic flux analysis. The light intensity and duty ratio were adjusted such that the total number of photons or the light intensity during the low-light phase was equal. Light fluctuations affected cell growth and photosynthetic activity under the experimental conditions. However, metabolic flux distributions and cofactor production rates were not affected by the light fluctuations. Furthermore, the estimated ATP and NADPH production rates in the photosystems suggest that NADPH-consuming electron dissipation occurs under fluctuating light conditions. Although we focused on the water–water cycle as the electron dissipation path, no growth effect was observed in an flv3-disrupted strain under fluctuating light, suggesting that another path contributes to electron dissipation under these conditions.     

PHOTOSYNTHETIC RESPONSE OF STREAM PERIPHYTON TO FLUCTUATING LIGHT REGIMES

  An experiment was conducted on intact algal assemblages of stream periphyton to test their response to fluctuating and constant light regimes having the same mean intensity. The light regimes (in μmol·m⁻²·s⁻¹) were constant light at 100, light fluctuating between 50 and 150 with a period of 5 min, and light fluctuating between 10 and 460 with periods of either 4:1 or 8:2 min. Compared to the rates measured under 100 in μmol·m⁻²·s⁻¹ constant light conditions, fluctuations ranging between 50 and 150 in μmol·m⁻²·s⁻¹ with a 5-min period produced a 23% greater rate of photosynthesis. Conversely, fluctuations between 10 and 460 in μmol·m⁻²·s⁻¹ led to a 59%–74% decrease in photosynthetic activity. Detailed examination of periphytic algal responses to fluctuating light revealed that higher light intensities produced steeper photosynthesis/time slopes, but it was the combined interaction with lower light intensity that ultimately determined overall photosynthetic rate for a given light regime. This study offers compelling evidence that variable light regimes have important consequences for algal photosynthesis in natural streams.     

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.     

In memory of Thomas Turpin Bannister (1930–2018)

Plants grown in the field experience sharp changes in irradiation due to shading effects caused by clouds, other leaves, etc. The excess of absorbed light energy is dissipated by a number of mechanisms including cyclic electron transport, photorespiration, and Mehler-type reactions. This protection is essential for survival but decreases photosynthetic efficiency. All phototrophs except angiosperms harbor flavodiiron proteins (Flvs) which relieve the excess of excitation energy on the photosynthetic electron transport chain by reducing oxygen directly to water. Introduction of cyanobacterial Flv1/Flv3 in tobacco chloroplasts resulted in transgenic plants that showed similar photosynthetic performance under steady-state illumination, but displayed faster recovery of various photosynthetic parameters, including electron transport and non-photochemical quenching during dark–light transitions. They also kept the electron transport chain in a more oxidized state and enhanced the proton motive force of dark-adapted leaves. The results indicate that, by acting as electron sinks during light transitions, Flvs contribute to increase photosynthesis protection and efficiency under changing environmental conditions as those found by plants in the field.     

Increased stomatal conductance induces rapid changes to photosynthetic rate in response to naturally fluctuating light conditions in rice

A close correlation between stomatal conductance and the steady-state photosynthetic rate has been observed for diverse plant species under various environmental conditions. However, it remains unclear whether stomatal conductance is a major limiting factor for the photosynthetic rate under naturally fluctuating light conditions. We analysed a SLAC1 knockout rice line to examine the role of stomatal conductance in photosynthetic responses to fluctuating light. SLAC1 encodes a stomatal anion channel that regulates stomatal closure. Long exposures to weak light before treatments with strong light increased the photosynthetic induction time required for plants to reach a steady-state photosynthetic rate and also induced stomatal limitation of photosynthesis by restricting the diffusion of CO₂ into leaves. The slac1 mutant exhibited a significantly higher rate of stomatal opening after an increase in irradiance than wild-type plants, leading to a higher rate of photosynthetic induction. Under natural conditions, in which irradiance levels are highly variable, the stomata of the slac1 mutant remained open to ensure efficient photosynthetic reaction. These observations reveal that stomatal conductance is important for regulating photosynthesis in rice plants in the natural environment with fluctuating light.     

E-photosynthesis: a comprehensive modeling approach to understand chlorophyll fluorescence transients and other complex dynamic features of photosynthesis in fluctuating light

Plants are exposed to a temporally and spatially heterogeneous environment, and photosynthesis is well adapted to these fluctuations. Understanding of the complex, non-linear dynamics of photosynthesis in fluctuating light requires novel-modeling approaches that involve not only the primary light and dark biochemical reactions, but also networks of regulatory interactions. This requirement exceeds the capacity of the existing molecular models that are typically reduced to describe a partial process, dynamics of a specific complex or its particular dynamic feature. We propose a concept of comprehensive model that would represent an internally consistent, integral framework combining information on the reduced models that led to its construction. This review explores approaches and tools that exist in engineering, mathematics, and in other domains of biology that can be used to develop a comprehensive model of photosynthesis. Equally important, we investigated techniques by which one can rigorously reduce such a comprehensive model to models of low dimensionality, which preserve dynamic features of interest and, thus, contribute to a better understanding of photosynthesis under natural and thus fluctuating conditions. The web-based platform www.e-photosynthesis.org is introduced as an arena where these concepts and tools are being introduced and tested.     

Drought stress memory in the photosynthetic mechanisms of an invasive CAM species, <Emphasis Type="Italic">Aptenia cordifolia</Emphasis>

Plants are known for their high capacity to acclimatise to fluctuating environmental conditions. A wide range of environmental conditions can lead to suboptimal physiological efficiency. However, recent studies have shown that plants can withstand repeated periods of stress. To find out how they do it, we studied photosynthetic adjustments to repeated water stress in Aptenia cordifolia: a facultative, invasive CAM species. Plants were subjected to three cycles of water deficit, and photosynthetic parameters and chloroplast antioxidants were quantified to gain an understanding of the mechanisms by which they cope with repeated stress periods. Significant modification of the photosystems’ antenna and reaction centres was observed in plants subjected to previous water stress cycles, and this led to higher PSII efficiency than in plants challenged with drought for the first time. These findings underline the biological significance of stress memory and show how plants can adjust their photosynthetic apparatus to fluctuating environmental conditions and thus optimise photosynthesis and photoprotection under drought conditions.     

Novel insights into plant light-harvesting complex II phosphorylation and 'state transitions'

Plants need a highly responsive regulatory system to keep photosynthetic light reactions in balance with the needs and restrictions of the downstream metabolism. This mechanism optimises plant growth under naturally fluctuating light conditions. In this opinion article, we present a model addressing the biological role of the light intensity-controlled phosphorylation of light-harvesting complex II (LHCII) proteins and its relation with the non-photochemical quenching of excitation energy (NPQ). We overturn a long held view of the possible role of 'state transitions'. Instead, we discuss the interplay between LHCII protein phosphorylation and NPQ, a mechanism that is crucial for regulating excitation energy distribution to the two photosystems (PSII and PSI) and balancing the intersystem electron flow despite constant fluctuations in light intensity.     

Hunting the main player enabling Chlamydomonas reinhardtii growth under fluctuating light

Photosynthetic organisms have evolved numerous photoprotective mechanisms and alternative electron sinks/pathways to fine‐tune the photosynthetic apparatus under dynamic environmental conditions, such as varying carbon supply or fluctuations in light intensity. In cyanobacteria flavodiiron proteins (FDPs) protect the photosynthetic apparatus from photodamage under fluctuating light (FL). In Arabidopsis thaliana, which does not possess FDPs, the PGR5‐related pathway enables FL photoprotection. The direct comparison of the pgr5, pgrl1 and flv knockout mutants of Chlamydomonas reinhardtii grown under ambient air demonstrates that all three proteins contribute to the survival of cells under FL, but to varying extents. The FDPs are crucial in providing a rapid electron sink, with flv mutant lines unable to survive even mild FL conditions. In contrast, the PGRL1 and PGR5‐related pathways operate over relatively slower and longer time‐scales. Whilst deletion of PGR5 inhibits growth under mild FL, the pgrl1 mutant line is only impacted under severe FL conditions. This suggests distinct roles, yet a close relationship, between the function of PGR5, PGRL1 and FDP proteins in photoprotection.     

Simulation of photosynthetic plasticity in response to highly fluctuating light: an empirical model integrating dynamic photosynthetic induction and capacity

An empirical model was developed to simulate photosynthetic responses of leaves to highly fluctuating light, with a special focus on the functional role of photosynthetic induction and capacity. Based on diurnal courses of light as input data, which were recorded at natural plant sites, we applied this model to simulate the corresponding course of net photosynthesis (output data) for leaves of two neotropical tree species. All six model input parameters (leaf-specific) were obtained via measurements of leaf gas exchange. The model was tested for leaves in their natural environments, characterized by frequent light-flecks. We compared measured carbon gains with computed ones, using a standard steady-state and our induction model. Simulation runs with the steady-state model can result in an immense overestimation of the true situation, by 13.4% at open sites [pioneer species Heliocarpus appendiculatus (Turczaninow)] and by 86.5% at low light environments of the understorey [mid to late successional species Billia colombiana (Planchon and Lindley)]. These significant overestimations, particularly in the understorey, are mainly the consequence of neglecting a dynamic photosynthetic induction under fluctuating light conditions. The model presented here resulted in clearly improved predictions; in open and understorey sites the true carbon gain of leaves was computed with a mean error of less than 7%. As most leaves at natural plant sites are exposed to light environments allowing for dynamic rather than steady-state CO₂ assimilation, the significance of such induction models is evident and is discussed in relation to scaling-up from leaf to canopy and to the whole plant indicating a large potential for errors. Received: 3 May 1999 / Accepted: 9 July 1999     

Photosynthetic apparatus of pea thylakoid membranes : response to growth light intensity

We investigated the effect of growth light intensity on the photosynthetic apparatus of pea (Pisum sativum) thylakoid membranes. Plants were grown either in a growth chamber at light intensities that ranged from 8 to 1050 microeinsteins per square meter per second, or outside under natural sunlight. In thylakoid membranes we determined: the amounts of active and inactive photosystem II, photosystem I, cytochrome b/f, and high potential cytochrome b₅₅₉, the rate of uncoupled electron transport, and the ratio of chlorophyll a to b. In leaves we determined: the amounts of the photosynthetic components per leaf area, the fresh weight per leaf area, the rate of electron transport, and the light compensation point. To minimize factors other than growth light intensity that may alter the photosynthetic apparatus, we focused on peas grown above the light compensation point (20-40 microeinsteins per square meter per second), and harvested only the unshaded leaves at the top of the plant. The maximum difference in the concentrations of the photosynthetic components was about 30% in thylakoids isolated from plants grown over a 10-fold range in light intensity, 100 to 1050 microeinsteins per square meter per second. Plants grown under natural sunlight were virtually indistinguishable from plants grown in growth chambers at the higher light intensities. On a leaf area basis, over the same growth light regime, the maximum difference in the concentration of the photosynthetic components was also about 30%. For peas grown at 1050 microeinsteins per square meter per second we found the concentrations of active photosystem II, photosystem I, and cytochrome b/f were about 2.1 millimoles per mol chlorophyll. There were an additional 20 to 33% of photosystem II complexes that were inactive. Over 90% of the heme-containing cytochrome f detected in the thylakoid membranes was active in linear electron transport. Based on these data, we do not find convincing evidence that the stoichiometries of the electron transport components in the thylakoid membrane, the size of the light-harvesting system serving the reaction centers, or the concentration of the photosynthetic components per leaf area, are regulated in response to different growth light intensities. The concept that emerges from this work is of a relatively fixed photosynthetic apparatus in thylakoid membranes of peas grown above the light compensation point.     

Dynamic Acclimation of Photosynthesis Increases Plant Fitness in Changing Environments

Plants growing in different environments develop with different photosynthetic capacities—developmental acclimation of photosynthesis. It is also possible for fully developed leaves to change their photosynthetic capacity—dynamic acclimation. The importance of acclimation has not previously been demonstrated. Here, we show that developmental and dynamic acclimation are distinct processes. Furthermore, we demonstrate that dynamic acclimation plays an important role in increasing the fitness of plants in natural environments. Plants of Arabidopsis (Arabidopsis thaliana) were grown at low light and then transferred to high light for up to 9 d. This resulted in an increase in photosynthetic capacity of approximately 40%. A microarray analysis showed that transfer to high light resulted in a substantial but transient increase in expression of a gene, At1g61800, encoding a glucose-6-phosphate/phosphate translocator GPT2. Plants where this gene was disrupted were unable to undergo dynamic acclimation. They were, however, still able to acclimate developmentally. When grown under controlled conditions, fitness, measured as seed output and germination, was identical, regardless of GPT2 expression. Under naturally variable conditions, however, fitness was substantially reduced in plants lacking the ability to acclimate. Seed production was halved in gpt2− plants, relative to wild type, and germination of the seed produced substantially less. Dynamic acclimation of photosynthesis is thus shown to play a crucial and previously unrecognized role in determining the fitness of plants growing in changing environments.It has long been recognized that when plants are grown under a particular set of conditions they adjust their photosynthetic capacity to match those conditions (for review, see Walters, 2005). For example, early work from Bjorkman and Holmgren (1963) showed that plants of Solidago virgaurea had different photosynthetic capacities when grown either in sun or shade. In spite of its long history, however, neither the mechanism nor the significance of this response is understood (Walters, 2005). Work from Murchie and Horton (1997) showed that there is substantial variation between species in their ability to acclimate, with plants from semishaded habitats having the greatest variation in photosynthetic capacity, suggesting that there is both a benefit and cost of acclimation. Neither benefit nor cost has been demonstrated.Photosynthetic acclimation can be observed at levels ranging from whole-plant morphology to the detailed stoichiometry of the photosynthetic apparatus (Boardman, 1977; Walters, 2005). Plants grown at low light tend to invest more in leaves than in roots and to have thinner leaves. They have more chlorophyll-containing light-harvesting proteins relative to light-using enzymes involved in electron transport and metabolism, meaning that photosynthesis saturates with light at a lower irradiance. Plants can also adjust the relative proportions of the different photosystems to suit the light quality they experience (Chow et al., 1990; Walters and Horton, 1995a, 1995b).Most studies that have examined the acclimation of plants have done so by making measurements on material that has experienced only one set of conditions—e.g. either high or low light. Differences between plants therefore reflect the conditions experienced as the leaves develop, with leaf morphology and composition being optimized for the conditions seen. Plants do not, however, exist in static environments. Even for a plant growing in an unshaded location, the light incident on a leaf can vary by an order of magnitude from second to second, day to day, and week to week depending on the weather conditions. This variation will typically be accompanied by variation in the temperature, which will also impact on metabolic capacity.When plants are exposed to light at irradiances that are above saturating for photosynthesis, which may result from increases in light or from environmental conditions (e.g. cold, drought) restricting metabolism, they are liable to suffer from stress (Demmig-Adams and Adams, 1992). Specifically, excess light can give rise to reactive oxygen species (Asada, 2006). The damaging effects of this can be limited by investing in antioxidant systems; however, these are metabolically expensive with, for example, substantial amounts of individual antioxidants such as ascorbic acid, being found in the chloroplast (Asada, 2006). It seems likely therefore that the ability of a plant to minimize stress, by adjusting photosynthetic capacity to suit as well as possible the prevailing conditions, will benefit the plant and increase overall fitness.In this study, we have investigated photosynthetic acclimation of the model plant Arabidopsis (Arabidopsis thaliana). Starting with a microarray analysis, we have identified a gene that is essential for acclimation to increases in irradiance. We further show that the ability to acclimate to changes in light has a major role in determining fitness under naturally variable light conditions.     

光环境对胡桃楸幼苗生长与光合作用的影响

为了解胡桃楸幼苗对光的需求及适应规律,采用Li-6400便携式光合测定系统研究了不同光环境处理（100%、60%、30％和15%自然光）条件下3年生胡桃楸幼苗（适应1年后）叶片光合能力的季节变化及其对光强的响应.结果表明：在春季,胡桃楸幼苗对光反应不敏感,夏季和秋季随着光强的增加,叶片的最大光合速率、最大羧化速率和最大电子传递速率均显著增加（P<0.05）.光饱和点随光强的下降而降低（P<0.05）,表观量子效率、暗呼吸速率和光补偿点在不同光环境下未发现显著差异.100%和60%自然光处理的幼苗相对生长率差异不显著,但是随着光强下降,相对生长率显著下降（P<0.05）,为60%>30％>15%自然光处理.胡桃楸幼苗对不同的光环境表现出较强的适应性和可塑性;同时,通过降低光饱和点和减少碳积累,也能适应15%～30％自然光环境.     

Acclimation of the diatom Stephanodiscus neoastraea and the cyanobacterium Planktothrix agardhii to simulated natural light fluctuations

Functional and structural characteristics of the photosynthetic apparatus were studied in the diatom Stephanodiscus neoastraea and the cyanobacterium Planktothrix agardhii which were grown semi-continuously under constant irradiance or under simulated natural light fluctuations. The light fluctuations consisted of 24 oscillations of exponentially increasing and decreasing irradiance over a 12-h light period. Maximum irradiance was 1100 μmol photons m⁻² s⁻¹ with the ratio of maximum to minimum intensities being 100, simulating Langmuir circulations with a ratio of euphotic to mixing depth of 1. S. neoastraea acclimated to the light fluctuations by doubling the number and halving the size of photosynthetic units (PS II) while the amount of chlorophylls and carotenoids remained unchanged. The chlorophyll-specific maximum photosynthetic rate was enhanced while the slope of the photosynthesis versus irradiance curves was not influenced by the light fluctuations. Acclimation of P. agardhii was mainly characterized by an increase in chlorophyll content. Both photosystems showed only little changes in number and size. Maximum photosynthetic rate, saturating irradiance and initial slope of the photosynthesis versus irradiance curves did not vary. Although both high and low light were contained in the fluctuating light, an analogy to low or high light acclimation was not found for the diatom nor for the cyanobacterium acclimated to light fluctuations. We suggest that the acclimation to fluctuating light is a response type outside the known scheme of low and high light acclimation. This revised version was published online in June 2006 with corrections to the Cover Date.     

Improving yield by exploiting mechanisms underlying natural variation of photosynthesis

Increasing photosynthesis in C3 species has been identified as an approach to increase the yield of crop plants. Most of our knowledge of photosynthetic performance has come from studies in which plants were grown in controlled growth conditions but plants in natural environments have to cope with unpredictable and rapidly changing conditions. Plants adapt to the light environment in which they grow and this is demonstrated by the differences in anatomy and morphology of leaves in sun and shade leaves. Superimposed on this are the dynamic responses of plants to rapid changes in the light environment that occur throughout the day. Application of next generation sequencing (NGS), QTL analysis and innovative phenomic screening can provide information to underpin approaches for breeding of higher yielding crop plants.     

A bestrophin‐like protein modulates the proton motive force across the thylakoid membrane in Arabidopsis

During photosynthesis, photosynthetic electron transport generates a proton motive force(pmf) across the thylakoid membrane, which is used for ATP biosynthesis via ATP synthase in the chloroplast. The pmf is composed of an electric potential(△Ψ) and an osmotic component(△pH).Partitioning between these components in chloroplasts is strictly regulated in response to fluctuating environments.However, our knowledge of the molecular mechanisms that regulate pmf partitioning is limited. Here, we report a bestrophin-like protein(At Best), which is critical for pmf partitioning. While the Dp H component was slightly reduced in atbest, the △Ψ component was much greater in this mutant than in the wild type, resulting in less efficient activation of nonphotochemical quenching(NPQ) upon both illumination and a shift from low light to high light. Although no visible phenotype was observed in the atbest mutant in the greenhouse, this mutant exhibited stronger photoinhibition than the wild type when grown in the field. At Best belongs to the bestrophin family proteins, which are believed to function as chloride(Cl~-) channels. Thus, our findings reveal an Researimportant Cl~- channel required for ion transport and homeostasis across the thylakoid membrane in higher plants. These processes are essential for fine-tuning photosynthesis under fluctuating environmental conditions.