Architecture of the chloroplast PSI-NDH supercomplex in Hordeum vulgare

Oxygen-containing photosynthesis uses solar energy to drive the oxidation of water and the reduction of carbon dioxide (CO₂) to produce oxygen and carbohydrates, which are essential for most life on earth. In the photoreaction, photosystem I (PSI) and photosystem II (PSII) convert light energy into ATP and NADPH, which are used to fix CO₂ to form carbohydrates in the Calvin-Benson cycle. There are two types of photosynthetic electron transfer pathways in the photoreaction process: linear and cyclic electron transfer. NDH-mediated PSI cyclic electron transfer generates a transmembrane proton gradient for synthesizing more ATP without producing NADPH, playing an important role in supplying sufficient ATP for carbon fixation. Dr.Zhang's group determined the high-resolution structure of higher plant PSI-NDH complex, which reveals the structural basis of PSI-NDH-mediated regulation of photosynthetic cyclic electron transport. Our results show that the PSI-NDH complex contains 2 PSI-LHCI, 1 NDH, and an unknown protein USP. It contains 55 protein subunits, 298 chlorophyll molecules, 67 carotenoid molecules, and 25 lipid molecules. The molecular weight is about 1.6 MDa; The results also reveal the precise location and structural characteristics of the special antenna subunits Lhca5 and Lhca6 in PSI-LHCI. These two unique LHCI subunits mediate the interactions between PSI-LHCI and NDH; The new subunits interact tightly with the intramembrane subunits of NDH, maintaining the structural stability of PSI-LHCI-NDH which are essential for complex assembly; in addition, since the chloroplast NDH complex accepts electrons from Fd, the combination of NDH and two PSIs will increase number of Fd may promote the transfer of electrons from PSI to NDH. Especially under low light conditions, such combination can increase efficiency of electron transfer. These results are not only important for understanding the mechanism of photosynthetic cyclic electron transfer, for studying the adaptation of angiosperms to the terrestrial light environment during evolution, but also for improving the light energy conversion, efficiency of CO₂ fixation and stress resistance of plants.