A conserved mechanism controls translation of Rubisco LSU

We previously proposed a novel mechanism for control of ribulose-1,5 biphosphate carboxylase/oxygenase (Rubisco) expression and assembly during oxidative stress in Chlamydomonas reinhardtii. The N-terminus of the large subunit (LSU) comprises an RNA recognition motif (RRM) that is normally buried in the protein, but becomes exposed under oxidizing conditions, when the glutathione pool shifts towards its oxidized form. Thus, de-novo translation and assembly of Rubisco LSU stop with similar kinetics, and the unpaired small subunit (SSU) is rapidly degraded. Here we show that the structure of the N-terminal domain is highly conserved throughout evolution, despite its relatively low sequence similarity. Furthermore, Rubisco from a broad evolutionary range of photosynthetic organisms binds RNA under oxidizing conditions, with K d values in the nano-molar range. In line with these observations, oxidative stress indeed causes a translational arrest in land plants as well as in Rhodospirillum rubrum, a purple bacterium that lacks the SSU. We highlight an evolutionary conserved element located within α-helix B, which is located in the center of the RRM, and is also involved in the intramolecular interactions between two LSU chains. Thus, assembly masks the N-terminus of the LSU hiding the RRM. When assembly is interrupted due to structural changes that occur under oxidizing conditions, or in the absence of a dedicated chaperone, the N-terminal domain can become exposed, leading to the translational arrest of Rubisco LSU. Taken together, these results support a model by which LSU translation is governed by its dimerization. In case that regulation of type I and type II Rubisco is conserved, the SSU does not appear to be directly involved in LSU translation.