Cyclic electron flow around photosystem I provides energy production and photoprotection in C4 plants

Abstract C4 photosynthesis requires more ATP than C3 photosynthesis to drive the C4 cycle, which concentrates CO2 in the bundle sheath cells. This ATP demand is expected to be met by cyclic electron transport around photosystem I. Of the two cyclic electron transport pathways, PROTON GRADIENT REGULATION 5 (PGR5)/PGR5-like photosynthetic phenotype 1 (PGRL1)-dependent and chloroplast NADH dehydrogenase-like (NDH)-dependent, ATP is supplied primarily by the NDH-dependent pathway in NADP-malic enzyme-type C4 plants. However, the roles of these pathways in photoprotection of photosystem I have not been fully evaluated in C4 plants. In this study, we used Flaveria bidentis knockdown lines targeting PGRL1 or NdhO and their double-knockdown lines to investigate the redox state of the electron transport chain and high light sensitivity of photosystems. The double-knockdown line exhibited poorer growth than the FbNdhO-RNAi line, indicating that both pathways were essential for ATP production. The acceptor side of P700 was limited under high light conditions in the FbNdhO-RNAi line, while it was limited under lower to high light conditions in the FbPGRL1-RNAi and double-knockdown lines. Ferredoxin was reduced more in the FbPGRL1-RNAi line than in the wild type, and it was even more reduced in the double-knockdown line. Photoinhibition caused by high light exposure was more pronounced in photosystem I than in photosystem II in these lines. These results demonstrate that both cyclic electron transport pathways are essential not only for ATP production required for growth but also for protecting photosystem I from photoinhibition by alleviating the acceptor-side limitations of P700 in C4 plants.