Proteostasis and protein quality control in chloroplasts: mechanisms and novel insights related to protein mislocalization
Nicolaj Jeran, M. Mercier, Paolo Pesaresi, Luca Tadini
Abstract
The dynamic rearrangement of the proteome and the maintenance of protein homeostasis (proteostasis) are crucial for the proper development and functionality of cellular compartments. Disruptions in proteostasis can severely compromise cellular health, leading to the accumulation of misfolded or mislocalized proteins prone to forming toxic aggregates. In chloroplasts, proteostasis presents unique challenges due to their endosymbiotic origin, complex subcompartmentalization, and constant exposure to reactive oxygen species (ROS) generated during photosynthesis. To counteract these challenges, chloroplasts employ sophisticated quality control systems, including chaperones, proteases, and protein degradation pathways such as ubiquitination and autophagy-related mechanisms. Additionally, cytosolic systems play a crucial role in regulating nuclear-encoded, plastid-targeted proteins, ensuring their proper delivery or degradation when defective. Within chloroplasts, specialized proteases, chaperones, and the chloroplast unfolded protein response (cpUPR) oversee protein quality and resolve aggregates to maintain functional integrity. This review critically examines mechanisms governing intracellular trafficking of plastid-targeted proteins, emphasizing key pathways and regulatory bottlenecks that, when disrupted, lead to the accumulation of mislocalized or orphan proteins. Particular focus is given to the signalling pathways that coordinate cytosolic and plastid effectors to sustain chloroplast function. Furthermore, we propose a novel role for PSBO, a subunit of the oxygen evolving complex associated with PSII, in linking proplastid-to-chloroplast differentiation with plastid quality control.