Iwasaki, S.; Fujita, T.; Wakigawa, T.; Kawamoto, N.; Kurihara, Y.; Hirose, Y.; Hirayama, T.; Toh, H.; Kuriyama, T.; Hashimoto, A.; Matsuura-Suzuki, E.; Mochida, K.; Yoshida, M.; Matsui, M.

Through symbiosis, subunits of chloroplastic complexes are encoded in distinct genomes in the nucleus and organelles. For plant cells to maintain the stoichiometry of subunits and respond to environmental cues, orchestration of the nuclear and organellar gene expression systems is an essential task. However, the mechanism maintaining chloroplastic complexes remains largely enigmatic. Here, we simultaneously assessed the translatomes of the chloroplast and the cytoplasm via ribosome profiling and revealed the differential mechanisms employed by these two systems to cope with acute light/dark transitions: in chloroplasts, translational regulation is employed, whereas in the cytoplasm, control of the mRNA abundance is employed. This strategy is widely conserved in land plants (Arabidopsis and the grass plant Brachypodium) and green algae (Chlamydomonas). The translational control in chloroplasts may be established on the basis of organelle symbiosis; the primitive chloroplast in Glaucophyta (Cyanophora) was found to have already acquired translational control, whereas cyanobacteria (Synechocystis) employ control of the mRNA abundance. Moreover, treatment with photosynthetic electron transport inhibitors indicated that reduced plastoquinones may trigger translational activation in chloroplasts. Our work reveals an early origin of coordination of chloroplast and nuclear/cytoplasmic gene expression upon light exposure.