A synthetic chlorophagy receptor promotes plant fitness by mediating chloroplast microautophagy

Chloroplasts are photosynthetic organelles and one of the major protein-containing organelles in green plants and algae. Although chloroplast contents or entire chloroplasts can be cleared by various vesicular pathways and autophagy, canonical chlorophagy receptors remain unidentified. Also, whether chlorophagy can be enhanced to benefit plants remains unknown. Here, we report the design and validation of a synthetic chlorophagy receptor that promotes plant fitness. The receptor LIR-SNT-BFP contains a fragment spanning the LIR/AIM of NBR1 and the N-terminal amphipathic helix of SFR2. The synthetic receptor localizes to chloroplasts and recruits ATG8a in planta. Induced expression of the synthetic receptor promotes microautophagy of entire chloroplasts, independent of ATG5 or ATG7. Meanwhile, it induces chloroplast fission. Notably, moderate induction of chlorophagy promotes rosette growth, whereas excessive chlorophagy appears detrimental. Induced chlorophagy also partially suppresses herbicide-induced leaf chlorosis. Our study provides proof of concept for controlling chloroplast degradation using a synthetic chlorophagy receptor.