Ribosomal protein bL31c interacts with translation elongation factor RAB8D to regulate chloroplast translation elongation and PSI-LHCI-LHCII assembly in Arabidopsis

Chloroplast translation systems have evolved specialized regulatory mechanisms distinct from those of their prokaryotic ancestors. However, critical gaps persist in understanding how these systems coordinate translation efficiency with photosynthetic apparatus assembly—a process central to plant development. Here, we identify Arabidopsis BACTERIAL LARGE RIBOSOMAL SUBUNIT PROTEIN 31 (bL31c) as a critical chloroplast ribosomal protein that interacts with the translation elongation factor RAB GTPASE HOMOLOG 8D (RAB8D) to ensure translation elongation efficiency. Knocking down bL31c disrupts chloroplast translation, causing preferential depletion of photosystem I (PSI) subunits, a functional imbalance between PSI and PSII, and paradoxical accumulation of the PSI-LHCI-LHCII supercomplex. Comparative analysis reveals evolutionary conservation of the bL31c-EF-Tu functional module in Cyanobacteria but not in E. coli, demonstrating lineage-specific adaptation of translation surveillance mechanisms. Crucially, pharmacological inhibition of translation elongation in wild-type plants phenocopies the photosystem stoichiometry defects observed in bl31c mutants, establishing defective ribosome processivity as the primary driver of photosystem imbalance. Our findings uncover a plant-specific ribosomal checkpoint mechanism that dynamically coordinates protein synthesis with photosynthetic complex assembly, providing important insights into the evolutionary rewiring of organellar gene expression systems in eukaryotes.