A Holistic Investigation of <i>Arabidopsis</i> Proteomes Altered in Chloroplast Biogenesis and Retrograde Signalling Identifies PsbO as a Key Regulator of Chloroplast Quality Control

Communication between the diverse compartments of plant cells relies on an intricate network of molecular interactions that orchestrate organellar development and adaptation to environmental conditions. Plastid-to-nucleus signalling pathways play a key role in relaying information from developing, mature, and damaged or disintegrating chloroplasts to the nucleus, which serves to coordinate gene expression between the two genomes. To shed light on these mechanisms, we performed a comprehensive analysis of the response of the Arabidopsis thaliana proteomes to perturbation of chloroplast biogenesis by the antibiotic lincomycin (Lin) in the absence of GENOMES UNCOUPLED 1 (GUN1), a key player in plastid-to-nucleus signalling. The topological analysis of protein-protein interactions (PPIs) and co-expression networks enabled the identification of protein hubs in each genotype and condition tested, and highlighted whole-cell adaptive responses to the disruption of chloroplast biogenesis. Our findings reveal a novel role for PsbO, a subunit of the oxygen-evolving complex (OEC), which behaves as an atypical photosynthetic protein upon inhibition of plastid protein synthesis. Notably, and unlike all other subunits of the thylakoid electron transport chain, PsbO accumulates in non-photosynthetic plastids, and is crucial for the breakdown of damaged chloroplasts.