Photosynthetically produced electrons provide energy for various metabolic pathways, including carbon reduction. Four Calvin-Benson cycle enzymes and several other plastid proteins are activated in the light by reduction of specific cysteines via thioredoxins, a family of electron transporters operating in redox regulation networks. How does this network link the photosynthetic chain with cellular metabolism? Using a time-resolved redox proteomic method, we have investigated the redox network in vivo during the dark–to–low light transition. We show that redox states of some thioredoxins follow the photosynthetic linear electron transport rate. While some redox targets have kinetics compatible with an equilibrium with one thioredoxin (TRXf), reduction of other proteins shows specific kinetic limitations, allowing fine-tuning of each redox-regulated step of chloroplast metabolism. We identified five new redox-regulated proteins, including proteins involved in Mg2+ transport and 1O2 signaling. Our results provide a system-level functional view of the photosynthetic redox regulation network.