NDH complex-mediated cyclic electron flow in bundle sheath cells enables C4photosynthesis

Abstract

AbstractThe superior productivity of C4plants is achieved via a metabolic C4cycle which acts as a CO2pump across mesophyll and bundle sheath (BS) cells and requires an additional input of energy in the form of ATP. Chloroplast NADH dehydrogenase-like complex (NDH) increases ATP production in C3plants by operating cyclic electron flow (CEF) around Photosystem I (PSI), and its importance for C4photosynthesis has been proposed from evolutionary and reverse genetics studies. We used the gene-edited C4speciesSetaria viridiswith nullndhOalleles lacking NDH to study a contribution of the complex to the cell-level electron transport. Our results indicate that NDH is the primary PSI electron acceptor mediating the majority of CEF in BS cells whilst the contribution of the complex to CEF in mesophyll cells is minimal. Moreover, the reduced leaf CO2assimilation rate and growth of plants lacking the complex cannot be rescued by supplying additional CO2, indicating that NDH is essential for generating ATP required for CO2fixation by the C3cycle. Hereby we resolve a cell-level mechanism for the contribution of NDH to supporting high CO2assimilation rates in C4photosynthesis.