Perturbation of protein homeostasis brings plastids at the crossroad between repairment and dismantling

The chloroplast proteome is a dynamic mosaic of plastid- and nuclear-encoded proteins, and plastid protein homeostasis is maintained through the balance between de novo protein synthesis and proteolysis. Intracellular communication pathways, including the pastid-to-nucleus retrograde communication, and the protein homeostasis machinery shape the chloroplast proteome based on developmental and physiological needs. However, the maintenance of fully functional chloroplasts is costly and under specific stress conditions the degradation of damaged chloroplasts is functional to the maintenance of a heathy population of photosynthesising organelles while promoting nutrient redistribution to sink tissues. In this study, we have addressed this complex regulatory chloroplast quality-control pathway by modulating the expression of two nuclear genes encoding the plastid ribosomal proteins PRPS1 and PRPL4. By transcriptomics, proteomics and transmission electron microscopy analyses, we show that the increased expression of PRPS1 gene leads to chloroplast degradation and early flowering, as an escaping strategy from stress conditions. On the contrary, the overaccumulation of PRPL4 protein is kept under control by the increased accumulation of plastid chaperones and other components of the unfolded protein response (cpUPR) regulatory mechanism. This study advances our understanding of the molecular mechanisms underlying chloroplast retrograde communication and provides new insight into cellular responses to impaired plastid protein homeostasis.