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- Title
Perturbation of protein homeostasis brings plastids at the crossroad between repair and dismantling.
- Authors
Tadini, Luca; Jeran, Nicolaj; Domingo, Guido; Zambelli, Federico; Masiero, Simona; Calabritto, Anna; Costantini, Elena; Forlani, Sara; Marsoni, Milena; Briani, Federica; Vannini, Candida; Pesaresi, Paolo
- Abstract
The chloroplast proteome is a dynamic mosaic of plastid- and nuclear-encoded proteins. Plastid protein homeostasis is maintained through the balance between de novo synthesis and proteolysis. Intracellular communication pathways, including the plastid-to-nucleus signalling and the protein homeostasis machinery, made of stromal chaperones and proteases, shape 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 essential to the maintenance of a healthy population of photosynthesising organelles while promoting nutrient redistribution to sink tissues. In this work, we have addressed this complex regulatory chloroplast-quality-control pathway by modulating the expression of two nuclear genes encoding 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 escape strategy from stress. On the contrary, the overaccumulation of PRPL4 protein is kept under control by increasing the amount of plastid chaperones and components of the unfolded protein response (cpUPR) regulatory mechanism. This study advances our understanding of molecular mechanisms underlying chloroplast retrograde communication and provides new insight into cellular responses to impaired plastid protein homeostasis. Author summary: Chloroplast protein composition requires the contribution of both nuclear and plastid genomes. The homeostasis of the plastid proteome is preserved through the balance between de novo protein synthesis and protein degradation, while plastid-to-nucleus communication mechanisms ensure the correct coordination of the two genomes. Chloroplast maintenance is costly; therefore, the degradation of damaged chloroplasts allows nutrient redistribution, which contributes to the essential requirement to sustain a population of healthy chloroplasts able to perform photosynthesis. In this work, we studied chloroplast quality-control mechanisms by modulating the expression of two nuclear genes encoding the plastid ribosomal proteins PRPS1 and PRPL4. By a multidisciplinary approach, we show that the increased expression of PRPS1 leads to chloroplast degradation and early flowering, as a stress-escaping strategy. On the contrary, the over-accumulation of PRPL4 protein activates the unfolded protein response mechanisms. Overall, this study provides further hints toward the comprehension of the molecular mechanisms underlying chloroplast retrograde communication and plastid protein homeostasis.
- Subjects
CHLOROPLASTS; UNFOLDED protein response; PLASTIDS; HOMEOSTASIS; RIBOSOMAL proteins; GENE expression
- Publication
PLoS Genetics, 2023, Vol 19, Issue 7, p1
- ISSN
1553-7390
- Publication type
Article
- DOI
10.1371/journal.pgen.1010344