A regulatory circuit involving the NADH dehydrogenase-like complex balances C4 photosynthetic carbon flow and cellular redox in maize

Abstract

O_LIC4 plants typically operate a CO2 concentration mechanism from mesophyll (M) cells into bundle sheath (BS) cells. NADH dehydrogenase-like (NDH) complex is enriched in the BS cells of many NADP-ME type C4 plants, and is more abundant in C4 than in C3 plants, but to what extent it is involved in the CO2 concentration mechanism remains to be experimentally investigated. C_LIO_LIWe created maize and rice mutants deficient in NDH function, and used a combination of transcriptomic, proteomic, and metabolomic approaches for comparative analysis. C_LIO_LIConsiderable decrease in growth, photosynthetic activities, and levels of key photosynthetic proteins were observed in maize but not rice mutants. However, gene expression for many cyclic electron transport and Calvin-Benson cycle components plus BS specific C4 enzymes, was up-regulated in maize mutants. Metabolite analysis of the maize ndh mutants revealed increased NADPH/NADP ratio, as well as malate, RuBP, FBP, and photorespiration components. C_LIO_LIWe suggest that by optimizing NADPH and malate levels, adjusting NADP-ME activity, NDH functions to balance metabolic and redox states in the BS cells of maize, coordinating photosynthetic gene expression and protein content, thus directly regulating the carbon flow in the two-celled C4 system of maize. C_LI