Assembly-dependent translational feedback regulation of photosynthetic proteins in land plants

In the green alga Chlamydomonas reinhardtii, the synthesis of chloroplast-encoded photosynthetic subunits is feedback regulated by their protein complex assembly state. This regulation is known as control by epistasy of synthesis (CES) and matches subunit synthesis with requirements of complex assembly in photosystem II (PSII), the cytochrome b6f complex (Cyt b6f), photosystem I (PSI), ATP synthase and Rubisco. In embryophytes, CES was only described for Rubisco, raising the question of whether CES exists for components of the photosynthetic electron transport chain in land plants. Here we systematically examined land plant mutants with assembly defects in PSII, Cyt b6f, PSI, ATP synthase, NAD(P)H dehydrogenase-like (NDH) complex and Rubisco for feedback regulation. We confirmed the CES in Rubisco and provide evidence for translational feedback regulation in PSII, involving psbA, psbB and psbD, and in Cyt b6f, connecting petA and petB. Our results also point to potential feedback regulation between ATP synthase subunits. Most of these regulatory connections are not conserved between algae and embryophytes. We did not find evidence for CES in land plant PSI or NDH complex assembly. Our results, however, indicate a regulatory connection between PSII and PSI. Overall, we revealed commonalities and differences in assembly-dependent feedback regulation of photosynthetic complexes between embryophytes and green algae. Algae fine-tune protein synthesis to assembly demands of photosynthetic complexes. In land plants, this feedback control is conserved in Rubisco and partly in photosystem II, but varies or is absent in other complexes, revealing divergent evolution.