A conserved mechanism controls translation of Rubisco large subunit in different photosynthetic organisms.
We previously proposed a mechanism for control of 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 toward 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 dissociation constant values in the nanomolar 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 alpha-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 the case that regulation of type I and type II Rubisco is conserved, the SSU does not appear to be directly involved in LSU translation.
Cohen
Idan
I
Department of Life Sciences, Ben-Gurion University of the Negev, Beer-Sheva 84105, Israel.
Sapir
Yair
Y
Shapira
Michal
M
D000388:Air; D000818:Animals; D005075:Biological Evolution; D016825:Chlamydomonas reinhardtii / Q000378:metabolism*; D017124:Conserved Sequence; D015964:Gene Expression Regulation, Bacterial; D018506:Gene Expression Regulation, Plant; D018384:Oxidative Stress / Q000502:physiology; D014176:Protein Biosynthesis / Q000502:physiology; D017434:Protein Structure, Tertiary; D012313:RNA / Q000378:metabolism; D012247:Rhodospirillum rubrum / Q000378:metabolism*; D012273:Ribulose-Bisphosphate Carboxylase / Q000378:metabolism*; D018724:Spinacia oleracea / Q000378:metabolism*; D014026:Nicotiana / Q000378:metabolism*
D012313:RNA; D012273:Ribulose-Bisphosphate Carboxylase