•‘State transition’ cannot explain the behavior of PSII–LHCII phosphorylation.•PSI is sensitive to excess electrons from PSII.•LHCII phosphorylation prevents excess electrons from accumulating under ...low light.•PGR5-dependent regulation of linear electron transfer protects PSI under high light.
Highly flexible regulation of photosynthetic light reactions in plant chloroplasts is a prerequisite to provide sufficient energy flow to downstream metabolism and plant growth, to protect light reactions against photodamage, and to ensure controlled cellular signaling from the chloroplast to the nucleus. Such comprehensive regulation occurs via the control of excitation energy transfer to and between the two photosystems (PSII and PSI), of the electrochemical gradient across the thylakoid membrane (ΔpH), and of electron transfer from PSII to PSI electron acceptors. In this opinion article, we propose that these regulatory mechanisms, functioning at different levels of photosynthetic energy conversion, might be interconnected and describe how the concomitant and integrated function of these mechanisms might enable plants to acclimate to a full array of environmental changes.
Photodamage of Photosystem II (PSII) has been considered as an unavoidable and harmful reaction that decreases plant productivity. PSII, however, has an efficient and dynamically regulated repair ...machinery, and the PSII activity becomes inhibited only when the rate of damage exceeds the rate of repair. The speed of repair is strictly regulated according to the energetic state in the chloroplast. In contrast to PSII, Photosystem I (PSI) is very rarely damaged, but when occurring, the damage is practically irreversible. While PSII damage is linearly dependent on light intensity, PSI gets damaged only when electron flow from PSII exceeds the capacity of PSI electron acceptors to cope with the electrons. When electron flow to PSI is limited, for example in the presence of DCMU, PSI is extremely tolerant against light stress. Proton gradient (ΔpH)-dependent slow-down of electron transfer from PSII to PSI, involving the PGR5 protein and the Cyt b6f complex, protects PSI from excess electrons upon sudden increase in light intensity. Here we provide evidence that in addition to the ΔpH-dependent control of electron transfer, the controlled photoinhibition of PSII is also able to protect PSI from permanent photodamage. We propose that regulation of PSII photoinhibition is the ultimate regulator of the photosynthetic electron transfer chain and provides a photoprotection mechanism against formation of reactive oxygen species and photodamage in PSI.
•We show that PSII photoinhibition is not only a harmful reaction.•It is demonstrated that controlled PSII turnover protects PSI against photodamage.•We propose that the controlled PSII turnover is a photoprotection mechanism.
Photosystem I (PSI) has evolved in anaerobic atmospheric conditions and until today remains susceptible to oxygen. To minimize the probability of damaging side reactions, plants have evolved ...sophisticated mechanisms to control electron transfer, and PSI becomes inhibited only when malfunctions of these regulatory mechanisms occur. Because of the complicated induction of PSI photoinhibition, a detailed investigation into the process and following reactions are still largely missing. Here, we introduce the theoretical framework and a novel method for an easy and controlled induction of PSI photoinhibition in vivo. The method mimics the PSI damage mechanisms of fluctuating light‐sensitive mutant plants (stn7, pgr5) which cannot control electron donation to PSI. Because PSII and PSI have different light absorption properties, electrons accumulate in the intersystem electron transfer chain (ETC), if PSII is preferentially excited. A saturating light pulse given upon an over‐reduced ETC leads to the saturation of PSI electron acceptors, ultimately leading to the production of reactive oxygen species and photoinhibition of PSI. By adjusting the time of the light treatment, PSI can be gradually photoinhibited, providing a novel tool to holistically investigate the PSI photoinhibition phenomenon.
In higher plants, the photosystem (PS) II core and its several light harvesting antenna (LHCII) proteins undergo reversible phosphorylation cycles according to the light intensity. High light ...intensity induces strong phosphorylation of the PSII core proteins and suppresses the phosphorylation level of the LHCII proteins. Decrease in light intensity, in turn, suppresses the phosphorylation of PSII core, but strongly induces the phosphorylation of LHCII. Reversible and differential phosphorylation of the PSII-LHCII proteins is dependent on the interplay between the STN7 and STN8 kinases, and the respective phosphatases. The STN7 kinase phosphorylates the LHCII proteins and to a lesser extent also the PSII core proteins D1, D2 and CP43. The STN8 kinase, on the contrary, is rather specific for the PSII core proteins. Mechanistically, the PSII-LHCII protein phosphorylation is required for optimal mobility of the PSII-LHCII protein complexes along the thylakoid membrane. Physiologically, the phosphorylation of LHCII is a prerequisite for sufficient excitation of PSI, enabling the excitation and redox balance between PSII and PSI under low irradiance, when excitation energy transfer from the LHCII antenna to the two photosystems is efficient and thermal dissipation of excitation energy (NPQ) is minimised. The importance of PSII core protein phosphorylation is manifested under highlight when the photodamage of PSII is rapid and phosphorylation is required to facilitate the migration of damaged PSII from grana stacks to stroma lamellae for repair. The importance of thylakoid protein phosphorylation is highlighted under fluctuating intensity of light where the STN7 kinase dependent balancing of electron transfer is a prerequisite for optimal growth and development of the plant. This article is part of a Special Issue entitled: Photosystem II.
► LHCII protein phosphorylation allows the maintenance of redox balance upon regulation of NPQ. ► Balanced excitation of PSII and PSI is a prerequisite of plant growth under fluctuating intensity of light. ► PSII core protein phosphorylation allows efficient unpacking of PSII-LHCII complexes upon PSII turnover.
Oxygenic photosynthetic organisms experience strong fluctuations in light intensity in their natural terrestrial and aquatic growth environments. Recent studies with both plants and cyanobacteria ...have revealed that Photosystem (PS) I is the potential target of damage upon abrupt changes in light intensity. Photosynthetic organisms have, however, developed powerful mechanisms in order to protect their photosynthetic apparatus against such potentially hazardous light conditions. Although the electron transfer chain has remained relatively unchanged in both plant chloroplasts and their cyanobacterial ancestors, the photoprotective and regulatory mechanisms of photosynthetic light reactions have experienced conspicuous evolutionary changes. In cyanobacteria, the specific flavodiiron proteins (Flv1 and Flv3) are responsible for safeguarding PSI under rapidly fluctuating light intensities, whilst the thylakoid located terminal oxidases are involved in the protection of PSII during 12 h diurnal cycles involving abrupt, square-wave, changes from dark to high light. Higher plants such as Arabidopsis thaliana have evolved different protective mechanisms. In particular, the PGR5 protein controls electron flow during sudden changes in light intensity by allowing the regulation mostly via the Cytochrome b6f complex. Besides the function of PGR5, plants have also acquired other dynamic regulatory mechanisms, among them the STN7-related LHCII protein phosphorylation that is similarly responsible for protection against rapid changes in the light environment. The green alga Chlamydomonas reinhardtii, as an evolutionary intermediate between cyanobacteria and higher plants, probably possesses both protective mechanisms. In this review, evolutionarily different photoprotective mechanisms under fluctuating light conditions are described and their contributions to cyanobacterial and plant photosynthesis are discussed.
Summary
Conversion of solar energy into chemical energy in plant chloroplasts concomitantly modifies the thylakoid architecture and hierarchical interactions between pigment–protein complexes. Here, ...the thylakoids were isolated from light‐acclimated Arabidopsis leaves and investigated with respect to the composition of the thylakoid protein complexes and their association into higher molecular mass complexes, the largest one comprising both photosystems (PSII and PSI) and light‐harvesting chlorophyll a/b‐binding complexes (LHCII). Because the majority of plant light‐harvesting capacity is accommodated in LHCII complexes, their structural interaction with photosystem core complexes is extremely important for efficient light harvesting. Specific differences in the strength of LHCII binding to PSII core complexes and the formation of PSII supercomplexes are well characterized. Yet, the role of loosely bound L‐LHCII that disconnects to a large extent during the isolation of thylakoid protein complexes remains elusive. Because L‐LHCII apparently has a flexible role in light harvesting and energy dissipation, depending on environmental conditions, its close interaction with photosystems is a prerequisite for successful light harvesting in vivo. Here, to reveal the labile and fragile light‐dependent protein interactions in the thylakoid network, isolated membranes were subjected to sequential solubilization using detergents with differential solubilization capacity and applying strict quality control. Optimized 3D‐lpBN‐lpBN‐sodium dodecyl sulfate–polyacrylamide gel electrophoresis system demonstrated that PSII–LHCII supercomplexes, together with PSI complexes, hierarchically form larger megacomplexes via interactions with L‐LHCII trimers. The polypeptide composition of LHCII trimers and the phosphorylation of Lhcb1 and Lhcb2 were examined to determine the light‐dependent supramolecular organization of the photosystems into megacomplexes.
Significance Statement
L‐LHCII trimers are crucial for the formation of large thylakoid membrane protein megacomplexes, comprising both PSII and PSI. This megacomplex formation is based on specific distribution of different LHCII trimers and reversible phosphorylation of Lhcb1 and Lhcb2 proteins.
In plant chloroplasts, the two photosystems (PSII and PSI) are enriched in different thylakoid domains and, according to the established view, are regarded as energetically segregated from each ...other. A specific fraction of the light harvesting complex II (LHCII) has been postulated to get phosphorylated by the STN7 kinase and subsequently to migrate from PSII to PSI as part of a process called ‘state transition’. Nevertheless, the thylakoid membrane incorporates a large excess of LHCII not present in the isolatable PSII–LHCII and PSI–LHCII complexes. Moreover, LHCII phosphorylation is not limited to a specific LHCII pool and “state 2” condition, but is found in all thylakoid domains in any constant light condition. Here, using a targeted solubilization of pigment–protein complexes from different thylakoid domains, we demonstrate that even a minor detachment of LHCII leads to markedly increased fluorescence emission from LHCII and PSII both in grana core and non-appressed thylakoid membranes and the effect of the detergent to detach LHCII is enhanced in the absence of LHCII phosphorylation. These findings provide evidence that PSII and PSI are energy traps embedded in the same energetically connected LHCII lake. In the lake, PSI and LHCII are energetically connected even in the absence of LHCII phosphorylation, yet the phosphorylation enhances the interaction required for efficient energy transfer to PSI in the grana margin regions.
•We present a new model for the excitation energy distribution in plant thylakoids.•We assign a role to the fraction of LHCII denoted as ‘extra-LHCII’.•Extra LHCII ensures energetic connectivity between PSII and PSI.•The whole LHCII constitutes an antenna ‘lake’ in which PSII and PSI are embedded.•LHCII phosphorylation is a regulator, but not a necessity, for the connectivity.
For decades, the dynamic nature of chlorophyll a fluorescence (ChlaF) has provided insight into the biophysics and ecophysiology of the light reactions of photosynthesis from the subcellular to leaf ...scales. Recent advances in remote sensing methods enable detection of ChlaF induced by sunlight across a range of larger scales, from using instruments mounted on towers above plant canopies to Earth-orbiting satellites. This signal is referred to as solar-induced fluorescence (SIF) and its application promises to overcome spatial constraints on studies of photosynthesis, opening new research directions and opportunities in ecology, ecophysiology, biogeochemistry, agriculture and forestry. However, to unleash the full potential of SIF, intensive cross-disciplinary work is required to harmonize these new advances with the rich history of biophysical and ecophysiological studies of ChlaF, fostering the development of next-generation plant physiological and Earth-system models. Here, we introduce the scale-dependent link between SIF and photosynthesis, with an emphasis on seven remaining scientific challenges, and present a roadmap to facilitate future collaborative research towards new applications of SIF.
According to the "state transitions'' theory, the light-harvesting complex II (LHCII) phosphorylation in plant chloroplasts is essential to adjust the relative absorption cross section of photosystem ...II (PSII) and PSI upon changes in light quality. The role of LHCII phosphorylation upon changes in light intensity is less thoroughly investigated, particularly when changes in light intensity are too fast to allow the phosphorylation/dephosphorylation processes to occur. Here, we demonstrate that the Arabidopsis (Arabidopsis thaliana) stn7 (for state transition7) mutant, devoid of the STN7 kinase and LHCII phosphorylation, shows a growth penalty only under fluctuating white light due to a low amount of PSI. Under constant growth light conditions, stn7 acquires chloroplast redox homeostasis by increasing the relative amount of PSI centers. Thus, in plant chloroplasts, the steady-state LHCII phosphorylation plays a major role in preserving PSI upon rapid fluctuations in white light intensity. Such protection of PSI results from LHCII phosphorylation-dependent equal distribution of excitation energy to both PSII and PSI from the shared LHCII antenna and occurs in cooperation with nonphotochemical quenching and the proton gradient regulation5-dependent control of electron flow, which are likewise strictly regulated by white light intensity. LHCII phosphorylation is concluded to function both as a stabilizer (in time scales of seconds to minutes) and a dynamic regulator (in time scales from tens of minutes to hours and days) of redox homeostasis in chloroplasts, subject to modifications by both environmental and metabolic cues. Exceeding the capacity of LHCII phosphorylation/dephosphorylation to balance the distribution of excitation energy between PSII and PSI results in readjustment of photosystem stoichiometry.
In nature, plants are challenged by constantly changing light conditions. To reveal the molecular mechanisms behind acclimation to sometimes drastic and frequent changes in light intensity, we grew ...Arabidopsis thaliana under fluctuating light conditions, in which the low light periods were repeatedly interrupted with high light peaks. Such conditions had only marginal effect on photosystem II but induced damage to photosystem I (PSI), the damage being most severe during the early developmental stages. We showed that PROTON GRADIENT REGULATIONS (PGR5)—dependent regulation of electron transfer and proton motive force is crucial for protection of PSI against photodamage, which occurred particularly during the high light phases of fluctuating light cycles. Contrary to PGR5, the NAD(P)H dehydrogenase complex, which mediates cyclic electron flow around PSI, did not contribute to acclimation of the photosynthetic apparatus, particularly PSI, to rapidly changing light intensities. Likewise, the Arabidopsis pgr5 mutant exhibited a significantly higher mortality rate compared with the wild type under outdoor field conditions. This shows not only that regulation of PSI under natural growth conditions is crucial but also the importance of PGR5 in PSI protection.
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