Cyclic electron transport around photosystem I (PSI) is essential for the protection of the photosynthetic apparatus in plants under diverse light conditions. This process is primarily mediated by Proton Gradient Regulation 5 protein/Proton Gradient Regulation 5-like photosynthetic phenotype 1 protein (PGR5/PGRL1) and NADH dehydrogenase-like complex (NDH). In angiosperms, NDH interacts with two PSI complexes through distinct monomeric antennae, LHCA5 and LHCA6, which is crucial for its higher stability under variable light conditions. This interaction represents an advanced evolutionary stage and offers limited insight into the origin of the PSI-NDH supercomplex in evolutionarily older organisms. In contrast, the moss Physcomitrium patens (Pp), which retains the lhca5 gene but lacks the lhca6, offers a glimpse into an earlier evolutionary stage of the PSI-NDH supercomplex. Here we present structural evidence of the Pp PSI-NDH supercomplex formation by single particle electron microscopy, demonstrating the unique ability of Pp to bind a single PSI in two different configurations. One configuration closely resembles the angiosperm model, whereas the other exhibits a novel PSI orientation, rotated clockwise. This structural flexibility in Pp is presumably enabled by the variable incorporation of LHCA5 within PSI and is indicative of an early evolutionary adaptation that allowed for greater diversity at the PSI-NDH interface. Our findings suggest that this variability was reduced as the structural complexity of the NDH complex increased in vascular plants, primarily angiosperms. This study not only clarifies the evolutionary development of PSI-NDH supercomplexes but also highlights the dynamic nature of the adaptive mechanisms of plant photosynthesis.

• Keywords
• LHCA5, PSI‐NDH supercomplex, Physcomitrium patens, cyclic electron transport, single particle analysis, transmission electron microscopy,
• MeSH
• Photosynthesis MeSH
• Photosystem I Protein Complex * metabolism   genetics   MeSH
• Bryopsida * genetics   metabolism   MeSH
• NADH Dehydrogenase metabolism   genetics   MeSH
• Plant Proteins * metabolism   genetics   MeSH
• Light-Harvesting Protein Complexes metabolism   genetics   chemistry   MeSH
• Electron Transport MeSH
• Publication type
• Journal Article MeSH
• Names of Substances
• Photosystem I Protein Complex * MeSH
• NADH Dehydrogenase MeSH
• Plant Proteins * MeSH
• Light-Harvesting Protein Complexes MeSH

Photosynthetic light-harvesting antennae are pigment-binding proteins that perform one of the most fundamental tasks on Earth, capturing light and transferring energy that enables life in our biosphere. Adaptation to different light environments led to the evolution of an astonishing diversity of light-harvesting systems. At the same time, several strategies have been developed to optimize the light energy input into photosynthetic membranes in response to fluctuating conditions. The basic feature of these prompt responses is the dynamic nature of antenna complexes, whose function readily adapts to the light available. High-resolution microscopy and spectroscopic studies on membrane dynamics demonstrate the crosstalk between antennae and other thylakoid membrane components. With the increased understanding of light-harvesting mechanisms and their regulation, efforts are focusing on the development of sustainable processes for effective conversion of sunlight into functional bio-products. The major challenge in this approach lies in the application of fundamental discoveries in light-harvesting systems for the improvement of plant or algal photosynthesis. Here, we underline some of the latest fundamental discoveries on the molecular mechanisms and regulation of light harvesting that can potentially be exploited for the optimization of photosynthesis.

• MeSH
• Photosynthesis * physiology   MeSH
• Adaptation, Physiological MeSH
• Plants metabolism   MeSH
• Light-Harvesting Protein Complexes * metabolism   MeSH
• Thylakoids metabolism   MeSH
• Publication type
• Journal Article MeSH
• Research Support, Non-U.S. Gov't MeSH
• Names of Substances
• Light-Harvesting Protein Complexes * MeSH

Diatoms are a large group of marine algae that are responsible for about one-quarter of global carbon fixation. Light-harvesting complexes of diatoms are formed by the fucoxanthin chlorophyll a/c proteins and their overall organization around core complexes of photosystems (PSs) I and II is unique in the plant kingdom. Using cryo-electron tomography, we have elucidated the structural organization of PSII and PSI supercomplexes and their spatial segregation in the thylakoid membrane of the model diatom species Thalassiosira pseudonana. 3D sub-volume averaging revealed that the PSII supercomplex of T. pseudonana incorporates a trimeric form of light-harvesting antenna, which differs from the tetrameric antenna observed previously in another diatom, Chaetoceros gracilis. Surprisingly, the organization of the PSI supercomplex is conserved in both diatom species. These results strongly suggest that different diatom classes have various architectures of PSII as an adaptation strategy, whilst a convergent evolution occurred concerning PSI and the overall plastid structure.

• MeSH
• Photosynthesis * MeSH
• Photosystem I Protein Complex ultrastructure   MeSH
• Photosystem II Protein Complex ultrastructure   MeSH
• Diatoms metabolism   ultrastructure   MeSH
• Thylakoids ultrastructure   MeSH
• Publication type
• Journal Article MeSH
• Research Support, Non-U.S. Gov't MeSH
• Names of Substances
• Photosystem I Protein Complex MeSH
• Photosystem II Protein Complex MeSH

PSI is an essential component of the photosynthetic apparatus of oxygenic photosynthesis. While most of its subunits are conserved, recent data have shown that the arrangement of the light-harvesting complexes I (LHCIs) differs substantially in different organisms. Here we studied the PSI-LHCI supercomplex of Botryococccus braunii, a colonial green alga with potential for lipid and sugar production, using functional analysis and single-particle electron microscopy of the isolated PSI-LHCI supercomplexes complemented by time-resolved fluorescence spectroscopy in vivo. We established that the largest purified PSI-LHCI supercomplex contains 10 LHCIs (∼240 chlorophylls). However, electron microscopy showed heterogeneity in the particles and a total of 13 unique binding sites for the LHCIs around the PSI core. Time-resolved fluorescence spectroscopy indicated that the PSI antenna size in vivo is even larger than that of the purified complex. Based on the comparison of the known PSI structures, we propose that PSI in B. braunii can bind LHCIs at all known positions surrounding the core. This organization maximizes the antenna size while maintaining fast excitation energy transfer, and thus high trapping efficiency, within the complex.

• MeSH
• Arabidopsis chemistry   ultrastructure   MeSH
• Chlamydomonas reinhardtii chemistry   ultrastructure   MeSH
• Protein Conformation MeSH
• Models, Molecular MeSH
• Protein Subunits MeSH
• Light-Harvesting Protein Complexes chemistry   ultrastructure   MeSH
• Publication type
• Journal Article MeSH
• Research Support, Non-U.S. Gov't MeSH
• Names of Substances
• Protein Subunits MeSH
• Light-Harvesting Protein Complexes MeSH