A multi‐omics approach reveals a link between ribosomal protein alterations and proteome rebalancing in Arabidopsis thaliana seeds

SUMMARY The ability of seeds to restore their amino acid content and composition after the elimination of the most abundant seed storage proteins (SSPs) is well‐documented, yet the underlying mechanisms remain unclear. To better understand how seeds compensate for major proteomic disruptions, we conducted a comprehensive analysis on an Arabidopsis mutant lacking the three most abundant SSPs, the cruciferins. Our initial findings indicated that carbon, nitrogen, and sulfur levels, as well as total protein and oil content, remained unchanged in these mutants suggesting rebalanced seeds. Transcriptomics and proteomics performed during seed maturation of Col‐0 and the triple mutant revealed significant modulation in many components of the translational machinery, especially ribosomal proteins (RPs), and in the antioxidation response in the mutant. These findings suggest that RPs play a critical role in facilitating proteomic homeostasis during seed maturation when proteomic perturbation occurs. Biochemical and metabolic analyses of the triple mutant dry seeds revealed increased protein carbonylation and elevated glutathione levels further supporting the link between SSP accumulation and seed redox homeostasis. Overall, we propose that in response to significant proteomic perturbations, changes in the proteome and amino acid composition of seeds are accompanied by a broad remodeling of the translation apparatus. We postulate that these alterations are key elements in seed adaptability and robustness to large proteomic perturbations during seed maturation.