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Molecular Plant Dec 2023State transition is a fundamental light acclimation mechanism of photosynthetic organisms in response to the environmental light conditions. This process rebalances the...
State transition is a fundamental light acclimation mechanism of photosynthetic organisms in response to the environmental light conditions. This process rebalances the excitation energy between photosystem I (PSI) and photosystem II through regulated reversible binding of the light-harvesting complex II (LHCII) to PSI. However, the structural reorganization of PSI-LHCI, the dynamic binding of LHCII, and the regulatory mechanisms underlying state transitions are less understood in higher plants. In this study, using cryoelectron microscopy we resolved the structures of PSI-LHCI in both state 1 (PSI-LHCI-ST1) and state 2 (PSI-LHCI-LHCII-ST2) from Arabidopsis thaliana. Combined genetic and functional analyses revealed novel contacts between Lhcb1 and PsaK that further enhanced the binding of the LHCII trimer to the PSI core with the known interactions between phosphorylated Lhcb2 and the PsaL/PsaH/PsaO subunits. Specifically, PsaO was absent in the PSI-LHCI-ST1 supercomplex but present in the PSI-LHCI-LHCII-ST2 supercomplex, in which the PsaL/PsaK/PsaA subunits undergo several conformational changes to strengthen the binding of PsaO in ST2. Furthermore, the PSI-LHCI module adopts a more compact configuration with shorter Mg-to-Mg distances between the chlorophylls, which may enhance the energy transfer efficiency from the peripheral antenna to the PSI core in ST2. Collectively, our work provides novel structural and functional insights into the mechanisms of light acclimation during state transitions in higher plants.
Topics: Photosystem I Protein Complex; Cryoelectron Microscopy; Interleukin-1 Receptor-Like 1 Protein; Light-Harvesting Protein Complexes; Chlorophyll; Arabidopsis
PubMed: 37936349
DOI: 10.1016/j.molp.2023.11.002 -
Nature Communications Jun 2024Cryptophytes are ancestral photosynthetic organisms evolved from red algae through secondary endosymbiosis. They have developed alloxanthin-chlorophyll a/c2-binding...
Cryptophytes are ancestral photosynthetic organisms evolved from red algae through secondary endosymbiosis. They have developed alloxanthin-chlorophyll a/c2-binding proteins (ACPs) as light-harvesting complexes (LHCs). The distinctive properties of cryptophytes contribute to efficient oxygenic photosynthesis and underscore the evolutionary relationships of red-lineage plastids. Here we present the cryo-electron microscopy structure of the Photosystem II (PSII)-ACPII supercomplex from the cryptophyte Chroomonas placoidea. The structure includes a PSII dimer and twelve ACPII monomers forming four linear trimers. These trimers structurally resemble red algae LHCs and cryptophyte ACPI trimers that associate with Photosystem I (PSI), suggesting their close evolutionary links. We also determine a Chl a-binding subunit, Psb-γ, essential for stabilizing PSII-ACPII association. Furthermore, computational calculation provides insights into the excitation energy transfer pathways. Our study lays a solid structural foundation for understanding the light-energy capture and transfer in cryptophyte PSII-ACPII, evolutionary variations in PSII-LHCII, and the origin of red-lineage LHCIIs.
Topics: Photosystem II Protein Complex; Light-Harvesting Protein Complexes; Cryptophyta; Cryoelectron Microscopy; Photosynthesis; Models, Molecular; Energy Transfer; Photosystem I Protein Complex; Chlorophyll A
PubMed: 38866834
DOI: 10.1038/s41467-024-49453-0 -
Plant Signaling & Behavior Dec 2023The chloroplasts in terrestrial plants play a functional role as a major sensor for perceiving physiological changes under normal and stressful conditions. Despite the...
The chloroplasts in terrestrial plants play a functional role as a major sensor for perceiving physiological changes under normal and stressful conditions. Despite the fact that the plant chloroplast genome encodes around 120 genes, which are mainly essential for photosynthesis and chloroplast biogenesis, the functional roles of the genes remain to be determined in plant's response to environmental stresses. Photosynthetic electron transfer D (PETD) is a key component of the chloroplast cytochrome bf complex. Chloroplast ndhA (NADH dehydrogenase A) and ndhB (NADH dehydrogenase B) interact with photosystem I (PSI), forming NDH-PSI supercomplex. Notably, artificial targeting of chloroplasts-encoded proteins, PETD, NDHA, or NDHB, was successfully relocated from cytosols into chloroplasts. The result suggests that artificial targeting of proteins to chloroplasts is potentially open to the possibility of chloroplast biotechnology in engineering of plant tolerance against biotic and abiotic stresses.
Topics: Cytosol; Chloroplast Proteins; Cytochrome b6f Complex; NADH Dehydrogenase; Chloroplasts
PubMed: 37707988
DOI: 10.1080/15592324.2023.2258321 -
The Plant Cell Apr 2024Cyanobacteria, red algae, and cryptophytes produce two classes of proteins for light-harvesting: water-soluble phycobiliproteins and membrane-intrinsic proteins that...
Cyanobacteria, red algae, and cryptophytes produce two classes of proteins for light-harvesting: water-soluble phycobiliproteins and membrane-intrinsic proteins that bind chlorophylls and carotenoids. In cyanobacteria, red algae, and glaucophytes, phycobilisomes (PBS) are complexes of brightly colored phycobiliproteins and linker (assembly) proteins. To date, six structural classes of phycobilisomes have been described: hemiellipsoidal, block-shaped, hemidiscoidal, bundle-shaped, paddle-shaped, and far-red-light bicylindrical. Two additional antenna complexes containing single types of phycobiliproteins have also been described. Since 2017, structures have been reported for examples of all of these complexes except bundle-shaped phycobilisomes by cryogenic electron microscopy. Phycobilisomes range in size from about 4.6 to 18 MDa and can include ∼900 polypeptides and bind >2000 chromophores. Cyanobacteria additionally produce membrane-associated proteins of the PsbC/CP43 superfamily of Chl a/b/d-binding proteins, including the iron-stress protein IsiA and other paralogous chlorophyll-binding proteins that can form antenna complexes with Photosystem I and/or Photosystem II. Red and cryptophyte algae also produce chlorophyll-binding proteins associated with Photosystem I but which belong to the chlorophyll a/b-binding (CAB) protein superfamily and which are unrelated to the chlorophyll-binding proteins (CBP) of cyanobacteria. This review describes recent progress in structure determination for phycobilisomes and the chlorophyll proteins of cyanobacteria, red algae, and cryptophytan algae.
PubMed: 38652697
DOI: 10.1093/plcell/koae126 -
The Plant Cell Apr 2024Cyanobacteria and chloroplasts of algae and plants harbor specialized thylakoid membranes that convert sunlight into chemical energy. These membranes house photosystems...
Cyanobacteria and chloroplasts of algae and plants harbor specialized thylakoid membranes that convert sunlight into chemical energy. These membranes house photosystems II and I, the vital protein-pigment complexes that drive oxygenic photosynthesis. In the course of their evolution, thylakoid membranes have diversified in structure. However, the core machinery for photosynthetic electron transport remained largely unchanged, with adaptations occurring primarily in the light-harvesting antenna systems. Whereas thylakoid membranes in cyanobacteria are relatively simple they become more complex in algae and plants. The chloroplasts of vascular plants contain intricate networks of stacked grana and unstacked stroma thylakoids. This review provides an in-depth view of thylakoid membrane architectures in phototrophs, and the determinants that shape their forms, as well as presenting recent insights into the spatial organization of their biogenesis and maintenance. Its overall goal is to define the underlying principles that have guided the evolution of these bioenergetic membranes.
PubMed: 38567528
DOI: 10.1093/plcell/koae102 -
Accounts of Chemical Research Nov 2023Oxygenic photosynthesis is the fundamental energy-converting process that utilizes sunlight to generate molecular oxygen and the organic compounds that sustain life....
Oxygenic photosynthesis is the fundamental energy-converting process that utilizes sunlight to generate molecular oxygen and the organic compounds that sustain life. Protein-pigment complexes harvest light and transfer excitation energy to specialized pigment assemblies, reaction centers (RC), where electron transfer cascades are initiated. A molecular-level understanding of the primary events is indispensable for elucidating the principles of natural photosynthesis and enabling development of bioinspired technologies. The primary enzyme in oxygenic photosynthesis is Photosystem II (PSII), a membrane-embedded multisubunit complex, that catalyzes the light-driven oxidation of water. The RC of PSII consists of four chlorophyll and two pheophytin pigments symmetrically arranged along two core polypeptides; only one branch participates in electron transfer. Despite decades of research, fundamental questions remain, including the origin of this functional asymmetry, the nature of primary charge-transfer states and the identity of the initial electron donor, the origin of the capability of PSII to enact charge separation with far-red photons, i.e., beyond the "red limit" where individual chlorophylls absorb, and the role of protein conformational dynamics in modulating charge-separation pathways.In this Account, we highlight developments in quantum-chemistry based excited-state computations for multipigment assemblies and the refinement of protocols for computing protein-induced electrochromic shifts and charge-transfer excitations calibrated with modern local correlation coupled cluster methods. We emphasize the importance of multiscale atomistic quantum-mechanics/molecular-mechanics and large-scale molecular dynamics simulations, which enabled direct and accurate modeling of primary processes in RC excitation at the quantum mechanical level.Our findings show how differential protein electrostatics enable spectral tuning of RC pigments and generate functional asymmetry in PSII. A chlorophyll pigment on the active branch (Chl) has the lowest site energy in PSII and is the primary electron donor. The complete absence of low-lying charge-transfer states within the central pair of chlorophylls excludes a long-held assumption about the initial charge separation. Instead, we identify two primary charge separation pathways, both with the same pheophytin acceptor (Pheo): a fast pathway with Chl as the primary electron donor (short-range charge-separation) and a slow pathway with PP as the initial donor (long-range charge separation). The low-energy spectrum is dominated by two states with significant charge-transfer character, ChlPheo and PPheo. The conformational dynamics of PSII allows these charge-transfer states to span wide energy ranges, pushing oxygenic photosynthesis beyond the "red limit". These results provide a quantum mechanical picture of the primary events in the RC of oxygenic photosynthesis, forming a solid basis for interpreting experimental observations and for extending photosynthesis research in new directions.
Topics: Photosystem II Protein Complex; Chlorophyll A; Photosynthesis; Electron Transport; Chlorophyll
PubMed: 37844298
DOI: 10.1021/acs.accounts.3c00392 -
Environmental Geochemistry and Health Nov 2023Indian camphorweed (Pluchea indica (L.) Less.) is used as herbal tea due to the presence of volatile aromatic oils and several phytochemical compounds. The aim of this...
Indian camphorweed (Pluchea indica (L.) Less.) is used as herbal tea due to the presence of volatile aromatic oils and several phytochemical compounds. The aim of this study was to assess the impact of copper (Cu) contamination on the physiology and morphology of P. indica, and the health risks associated with its consumption as tea. The cuttings of P. indica were subjected to 0 mM (control), 5 mM (low Cu), and 20 mM (excess Cu) of CuSO treatments for 1, 2, and 4 weeks. Thereafter, Cu contamination as well as physiological and morphological parameters were assessed. Cu accumulation was higher in the root tissues of plants (25.8 folds higher as compared to the leaves) grown under 20 mM CuSO for 4 weeks. This increased Cu accumulation resulted in the inhibition of root length, root fresh weight, and root dry weight. Cu concentration was found maximum (1.36 μg g DW) in the leaf tissues under 20 mM Cu exposure for 4 weeks, with the highest target hazard quotient (THQ = 1.85), whereas Cu was not detected in control. Under exposure to 20 mM Cu treatment for 4 weeks, leaf greenness, maximum quantum yield of photosystem II, and photon yield of photosystem II diminished by 21.4%, 16.1%, and 22.4%, respectively, as compared to the control. Leaf temperature was increased by 2.5 °C, and the crop stress index (CSI) exceeded 0.6 when exposed to 20 mM Cu treatment for 2 and 4 weeks; however, the control had a CSI below 0.5. This led to a reduced transpiration rate and stomatal conductance. In addition, the net photosynthetic rate was also found sensitive to Cu treatment, which resulted in decreased shoot and root growth. Based on the key results, it can be suggested that P. indica herbal tea derived from the foliage of plants grown under a 5 mM Cu level (0.75 μg g DW) with a target hazard quotient below one aligns with the recommended dietary intake of Cu in leafy vegetables. The study recommends choosing cuttings from plants with a small canopy as plant material in the greenhouse microclimates to validate the growth performance in the Cu-contaminated soil and simulate the natural shrub architecture and life cycle.
Topics: Copper; Photosystem II Protein Complex; Teas, Herbal; Photosynthesis; Antioxidants; Plant Leaves
PubMed: 37402936
DOI: 10.1007/s10653-023-01679-5 -
International Journal of Molecular... Mar 2024Photosystem I (PSI) is one of the two main pigment-protein complexes where the primary steps of oxygenic photosynthesis take place. This review describes low-temperature... (Review)
Review
Photosystem I (PSI) is one of the two main pigment-protein complexes where the primary steps of oxygenic photosynthesis take place. This review describes low-temperature frequency-domain experiments (absorption, emission, circular dichroism, resonant and non-resonant hole-burned spectra) and modeling efforts reported for PSI in recent years. In particular, we focus on the spectral hole-burning studies, which are not as common in photosynthesis research as the time-domain spectroscopies. Experimental and modeling data obtained for trimeric cyanobacterial Photosystem I (PSI), PSI mutants, and PSI-IsiA supercomplexes are analyzed to provide a more comprehensive understanding of their excitonic structure and excitation energy transfer (EET) processes. Detailed information on the excitonic structure of photosynthetic complexes is essential to determine the structure-function relationship. We will focus on the so-called "red antenna states" of cyanobacterial PSI, as these states play an important role in photochemical processes and EET pathways. The high-resolution data and modeling studies presented here provide additional information on the energetics of the lowest energy states and their chlorophyll (Chl) compositions, as well as the EET pathways and how they are altered by mutations. We present evidence that the low-energy traps observed in PSI are excitonically coupled states with significant charge-transfer (CT) character. The analysis presented for various optical spectra of PSI and PSI-IsiA supercomplexes allowed us to make inferences about EET from the IsiA ring to the PSI core and demonstrate that the number of entry points varies between sample preparations studied by different groups. In our most recent samples, there most likely are three entry points for EET from the IsiA ring per the PSI core monomer, with two of these entry points likely being located next to each other. Therefore, there are nine entry points from the IsiA ring to the PSI trimer. We anticipate that the data discussed below will stimulate further research in this area, providing even more insight into the structure-based models of these important cyanobacterial photosystems.
Topics: Photosystem I Protein Complex; Circular Dichroism; Energy Transfer; Chlorophyll; Cold Temperature
PubMed: 38612659
DOI: 10.3390/ijms25073850 -
Plant Physiology and Biochemistry : PPB Feb 2024Because of a high sensitivity to high temperature, both the yield and quality of tomato (Solanum lycopersicum L.) are severely restricted by heat stress. The...
Because of a high sensitivity to high temperature, both the yield and quality of tomato (Solanum lycopersicum L.) are severely restricted by heat stress. The Bcl-2-associated athanogene (BAG) proteins, a family of multi-functional co-chaperones, are involved in plant growth, development, and stress tolerance. We have previously demonstrated that BAG9 positively regulates thermotolerance in tomato. However, the BAG9-mediated mechanism of thermotolerance in tomato has remained elusive. In the present study, we report that BAG9 interacts with heat shock protein 70 (HSP70) in vitro and in vivo. Silencing HSP70 decreased thermotolerance of tomato plants, as reflected by the phenotype, relative electrolyte leakage and malondialdehyde. Furthermore, the photosystem activities, activities of antioxidant enzymes and expression of key genes encoding antioxidant enzymes were reduced in HSP70-silenced plants under heat stress. Additionally, silencing HSP70 decreased thermotolerance of overexpressing BAG9 plants, which was related to decreased photosynthetic rate, increased damage to photosystem I and photosystem II, decreased activity of antioxidant enzymes, and decreased expression of key genes encoding antioxidant enzymes. Taken together, the present study identified that HSP70 is involved in BAG9-mediated thermotolerance by protecting the photosystem stability and improving the efficiency of the antioxidant system in tomato. This knowledge can be helpful to breed improved crop cultivars that are better equipped with thermotolerance.
Topics: Thermotolerance; Solanum lycopersicum; Antioxidants; HSP70 Heat-Shock Proteins; Plant Breeding; Heat-Shock Response; Plant Proteins; Gene Expression Regulation, Plant
PubMed: 38219426
DOI: 10.1016/j.plaphy.2024.108353 -
Nature Communications Jun 2024Classical photochemistry requires nanosecond excited-state lifetimes for diffusion-controlled reactions. Excited radicals with picosecond lifetimes have been implied by...
Classical photochemistry requires nanosecond excited-state lifetimes for diffusion-controlled reactions. Excited radicals with picosecond lifetimes have been implied by numerous photoredox studies, and controversy has arisen as to whether they can actually be catalytically active. We provide direct evidence for the elusive pre-association between radical ions and substrate molecules, enabling photoinduced electron transfer beyond the diffusion limit. A strategy based on two distinct light absorbers, mimicking the natural photosystems I and II, is used to generate excited radicals, unleashing extreme reduction power and activating C(sp)-Cl and C(sp)-F bonds. Our findings provide a long-sought mechanistic understanding for many previous synthetically-oriented works and permit more rational future photoredox reaction development. The newly developed excitation strategy pushes the current limits of reactions based on multi-photon excitation and very short-lived but highly redox active species.
PubMed: 38834625
DOI: 10.1038/s41467-024-49006-5