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.     

Rising CO2 levels and their potential significance for carbon flow in photosynthetic cells

Abstract. In the first part of this review, I discuss how we can predict the direct short-term effect of enhanced CO₂ on photosynthetic rate in C₃ terrestrial plants. To do this, I consider: (1) to what extent enhanced CO₂ will stimulate or relieve demand on partial processes like carboxylation, light harvesting and electron transport, the Calvin cycle, and end-product synthesis; and (2) the extent to which these various processes actually control the rate of photosynthesis. I conclude that control is usually shared between Rubisco (which responds sensitively to CO₂) and other components (which respond less sensitively), and that photosynthesis will be stimulated by 25–75% when the CO₂ concentration is doubled from 35 to 70 Pa. This is in good agreement with the published responses. In the next part of the review, I discuss the evidence that most plants undergo a gradual inhibition of photosynthesis during acclimation to enhanced CO₂. I argue that this is related to an inadequate demand for carbohydrate in the remainder of the plant. Differences in the long-term response to CO₂ may be explained by differences in the sink-source status of plants, depending upon the species, the developmental stage, and the developmental conditions. In the third part of the review, I consider the biochemical mechanisms which are involved in ‘sink’ regulation of photosynthesis. Accumulating carbohydrate could lead to a direct inhibition of photosynthesis, involving mechanical damage by large starch grains or Pi-limitation due to inhibition of sucrose synthesis. I argue that Pi is important in the short-term regulation of partitioning to sucrose and starch, but that its contribution to ‘sink’ regulation has not yet been conclusively demonstrated. Indirect or ‘adaptive’ regulation of photosynthesis is probably more important, involving decreases in amounts of key photosynthetic enzymes, including Rubisco. This decreases the rate of photosynthesis, and potentially would allow resources (e.g. amino acids) to be remobilized from the leaves and reinvested in sink growth to readjust the sink-source balance. In the final part of the review, I argue that similar changes of Rubisco and, possibly, other proteins are probably also involved during acclimation to high CO₂.     

Light acclimation,retrograde signalling,cell death and immune defences in plants

This review confronts the classical view of plant immune defence and light acclimation with recently published data. Earlier findings have linked plant immune defences to nucleotide‐binding site leucine‐rich repeat (NBS‐LRR)‐dependent recognition of pathogen effectors and to the role of plasma membrane‐localized NADPH‐dependent oxidoreductase (AtRbohD), reactive oxygen species (ROS) and salicylic acid (SA). However, recent results suggest that plant immune defence also depends on the absorption of excessive light energy and photorespiration. Rapid changes in light intensity and quality often cause the absorption of energy, which is in excess of that required for photosynthesis. Such excessive light energy is considered to be a factor triggering photoinhibition and disturbance in ROS/hormonal homeostasis, which leads to cell death in foliar tissues. We highlight here the tight crosstalk between ROS‐ and SA‐dependent pathways leading to light acclimation, and defence responses leading to pathogen resistance. We also show that LESION SIMULATING DISEASE 1 (LSD1) regulates and integrates these processes. Moreover, we discuss the role of plastid–nucleus signal transduction, photorespiration, photoelectrochemical signalling and ‘light memory’ in the regulation of acclimation and immune defence responses. All of these results suggest that plants have evolved a genetic system that simultaneously regulates systemic acquired resistance (SAR), cell death and systemic acquired acclimation (SAA).     

Photostasis and cold acclimation: sensing low temperature through photosynthesis

Photosynthesis is a highly integrated and regulated process which is highly sensitive to any change in environmental conditions, because it needs to balance the light energy absorbed by the photosystems with the energy consumed by metabolic sinks of the plant. Low temperatures exacerbate an imbalance between the source of energy and the metabolic sink, thus requiring adjustments of photosynthesis to maintain the balance of energy flow. Photosynthesis itself functions as a sensor of this imbalance through the redox state of photosynthetic electron-transport components and regulates photophysical, photochemical and metabolic processes in the chloroplast. Recent progress has been made in understanding how plants sense the low temperature signal. It is clear that photosynthesis interacts with other processes during cold acclimation involving crosstalk between photosynthetic redox, cold acclimation and sugar-signalling pathways to regulate plant acclimation to low temperatures.     

Photosynthetic acclimation: state transitions and adjustment of photosystem stoichiometry--functional relationships between short-term and long-term light quality acclimation in plants

In dense plant populations, individuals shade each other resulting in a low-light habitat that is enriched in far-red light. This light quality gradient decreases the efficiency of the photosynthetic light reaction as a result of imbalanced excitation of the two photosystems. Plants counteract such conditions by performing acclimation reactions. Two major mechanisms are known to assure efficient photosynthesis: state transitions, which act on a short-term timescale; and a long-term response, which enables the plant to re-adjust photosystem stoichiometry in favour of the rate-limiting photosystem. Both processes start with the perception of the imbalanced photosystem excitation via reduction/oxidation (redox) signals from the photosynthetic electron transport chain. Recent data in Arabidopsis indicate that initialization of the molecular processes in both cases involve the activity of the thylakoid membrane-associated kinase, STN7. Thus, redox-controlled phosphorylation events may not only adjust photosystem antenna structure but may also affect plastid, as well as nuclear, gene expression. Both state transitions and the long-term response have been described mainly in molecular terms, while the physiological relevance concerning plant survival and reproduction has been poorly investigated. Recent studies have shed more light on this topic. Here, we give an overview on the long-term response, its physiological effects, possible mechanisms and its relationship to state transitions as well as to nonphotochemical quenching, another important short-term mechanism that mediates high-light acclimation. Special emphasis is given to the functional roles and potential interactions between the different light acclimation strategies. A working model displays the various responses as an integrated molecular system that helps plants to acclimate to the changing light environment.     

MITOGEN-ACTIVATED PROTEIN KINASE 4 impacts leaf development,temperature, and stomatal movement in hybrid aspen

Stomatal movement and density influence plant water use efficiency and thus biomass production. Studies in model plants within controlled environments suggest MITOGEN-ACTIVATED PROTEIN KINASE 4 (MPK4) may be crucial for stomatal regulation. We present functional analysis of MPK4 for hybrid aspen (Populus tremula × tremuloides) grown under natural field conditions for several seasons. We provide evidence of the role of MPK4 in the genetic and environmental regulation of stomatal formation, differentiation, signaling, and function; control of the photosynthetic and thermal status of leaves; and growth and acclimation responses. The long-term acclimation manifested as variations in stomatal density and distribution. Short-term acclimation responses were derived from changes in the stomatal aperture. MPK4 localized in the cytoplasm of guard cells (GCs) was a positive regulator of abscisic acid (ABA)-dependent stomatal closure and nitric oxide metabolism in the ABA-dependent pathways, while to a lesser extent, it was involved in ABA-induced hydrogen peroxide accumulation. MPK4 also affected the stomatal aperture through deregulation of microtubule patterns and cell wall structure and composition, including via pectin methyl-esterification, and extensin levels in the GC wall. Deregulation of leaf anatomy (cell compaction) and stomatal movement, together with increased light energy absorption, resulted in altered leaf temperature, photosynthesis, cell death, and biomass accumulation in mpk4 transgenic plants. Divergence between absorbed energy and assimilated energy is a bottleneck, and MPK4 can participate in the control of energy dissipation (thermal effects). Furthermore, MPK4 can participate in balancing the photosynthetic energy distribution via its effective use in growth or redirection to acclimation/defense responses.

MITOGEN-ACTIVATED PROTEIN KINASE 4 plays a multilevel role in stomatal formation, function, and signaling in the photosynthetic and thermal status of leaves and in growth and acclimation responses.     

State-transitions facilitate robust quantum yields and cause an over-estimation of electron transport in Dunaliella tertiolecta cells held at the CO2 compensation point and re-supplied with DIC

Photosynthetic energy consumption and non-photosynthetic energy quenching processes are inherently linked. Both processes must be controlled by the cell to allow cell maintenance and growth, but also to avoid photodamage. We used the chlorophyte algae Dunaliella tertiolecta to investigate how the interactive regulation of photosynthetic and non-photosynthetic pathways varies along dissolved inorganic carbon (DIC) and photon flux gradients. Specifically, cells were transferred to DIC-deplete media to reach a CO₂ compensation before being re-supplied with DIC at various concentrations and different photon flux levels. Throughout these experiments we monitored and characterized the photophysiological responses using pulse amplitude modulated fluorescence, oxygen evolution, 77 K fluorescence emission spectra, and fast-repetition rate fluorometry. O₂ uptake was not significantly stimulated at DIC depletion, which suggests that O₂ production rates correspond to assimilatory photosynthesis. Fluorescence-based measures of relative electron transport rates (rETRs) over-estimated oxygen-based photosynthetic measures due to a strong state-transitional response that facilitated high effective quantum yields. Adoption of an alternative fluorescence-based rETR calculation that accounts for state-transitions resulted in improved linear oxygen versus rETR correlation. This study shows the extraordinary capacity of D. tertiolecta to maintain stable effective quantum yields by flexible regulation of state-transitions. Uncertainties about the control mechanisms of state-transitions are presented.     

Ion regulation in fish gills: recent progress in the cellular and molecular mechanisms

Fish encounter harsh ionic/osmotic gradients on their aquatic environments, and the mechanisms through which they maintain internal homeostasis are more challenging compared with those of terrestrial vertebrates. Gills are one of the major organs conducting the internal ionic and acid-base regulation, with specialized ionocytes as the major cells carrying out active transport of ions. Exploring the iono/osmoregulatory mechanisms in fish gills, extensive literature proposed several models, with many conflicting or unsolved issues. Recent studies emerged, shedding light on these issues with new opened windows on other aspects, on account of available advanced molecular/cellular physiological approaches and animal models. Respective types of ionocytes and ion transporters, and the relevant regulators for the mechanisms of NaCl secretion, Na(+) uptake/acid secretion/NH(4)(+) excretion, Ca(2+) uptake, and Cl(-) uptake/base secretion, were identified and functionally characterized. These new ideas broadened our understanding of the molecular/cellular mechanisms behind the functional modification/regulation of fish gill ion transport during acute and long-term acclimation to environmental challenges. Moreover, a model for the systematic and local carbohydrate energy supply to gill ionocytes during these acclimation processes was also proposed. These provide powerful platforms to precisely study transport pathways and functional regulation of specific ions, transporters, and ionocytes; however, very few model species were established so far, whereas more efforts are needed in other species.     

Photosynthesis, photorespiration, and light signalling in defence responses

Visible light is the basic energetic driver of plant biomass production through photosynthesis. The constantly fluctuating availability of light and other environmental factors means that the photosynthetic apparatus must be able to operate in a dynamic fashion appropriate to the prevailing conditions. Dynamic regulation is achieved through an array of homeostatic control mechanisms that both respond to and influence cellular energy and reductant status. In addition, light availability and quality are continuously monitored by plants through photoreceptors. Outside the laboratory growth room, it is within the context of complex changes in energy and signalling status that plants must regulate pathways to deal with biotic challenges, and this can be influenced by changes in the highly energetic photosynthetic pathways and in the turnover of the photosynthetic machinery. Because of this, defence responses are neither simple nor easily predictable, but rather conditioned by the nutritional and signalling status of the plant cell. This review discusses recent data and emerging concepts of how recognized defence pathways interact with and are influenced by light-dependent processes. Particular emphasis is placed on the potential roles of the chloroplast, photorespiration, and photoreceptor-associated pathways in regulating the outcome of interactions between plants and pathogenic organisms.     

Short-term acclimation of the photosynthetic electron transfer chain to changing light: a mathematical model

Photosynthetic eukaryotes house two photosystems with distinct light absorption spectra. Natural fluctuations in light quality and quantity can lead to unbalanced or excess excitation, compromising photosynthetic efficiency and causing photodamage. Consequently, these organisms have acquired several distinct adaptive mechanisms, collectively referred to as non-photochemical quenching (NPQ) of chlorophyll fluorescence, which modulates the organization and function of the photosynthetic apparatus. The ability to monitor NPQ processes fluorometrically has led to substantial progress in elucidating the underlying molecular mechanisms. However, the relative contribution of distinct NPQ mechanisms to variable light conditions in different photosynthetic eukaryotes remains unclear. Here, we present a mathematical model of the dynamic regulation of eukaryotic photosynthesis using ordinary differential equations. We demonstrate that, for Chlamydomonas, our model recapitulates the basic fluorescence features of short-term light acclimation known as state transitions and discuss how the model can be iteratively refined by comparison with physiological experiments to further our understanding of light acclimation in different species.     

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.     

Some insights into energy metabolism for osmoregulation in fish

A sufficient and timely energy supply is a prerequisite for the operation of iono- and osmoregulatory mechanisms in fish. Measurements of whole-fish or isolated-gill (or other organs) oxygen consumption have demonstrated regulation of the energy supply during acclimation to different osmotic environments, and such regulation is dependent on species, the situation of acclimation or acclimatization, and life habits. Carbohydrate metabolism appears to play a major role in the energy supply for iono- and osmoregulation, and the liver is the major source supplying carbohydrate metabolites to osmoregulatory organs. Compared with carbohydrates, the roles of lipids and proteins remain largely unclear. Energy metabolite translocation was recently found to occur between fish gill ionocytes and neighboring glycogen-rich (GR) cells, indicating the physiological significance of a local energy supply for gill ion regulatory mechanisms. Spatial and temporal relationships between the liver and other osmoregulatory and non-osmoregulatory organs in partitioning the energy supply for ion regulatory mechanisms during salinity challenges were also proposed. A novel glucose transporter was found to specifically be expressed and function in gill ionocytes, providing the first cue for investigating energy translocation among gill cells. Advanced molecular physiological approaches can be used to examine energy metabolism relevant to a particular cell type (e.g., gill ionocytes), and functional genomics may also provide another powerful approach to explore new metabolic pathways related to fish ion regulation.