STAY-GREEN overexpression in dark-incubated leaves promotes the formation of transitional chromoplast-like plastids

The transition of chloroplasts into chromoplasts and gerontoplasts during fruit ripening and leaf senescence, respectively, involves chlorophyll breakdown and chloroplast deterioration. Chlorophyll removal is carried out by several enzymes. Among them, the Mg-dechelatase STAY-GREEN (SGR) catalyzes the first step of chlorophyll degradation. The tomato green-flesh (gf) and pepper chlorophyll retainer (cl) mutants are SGR loss-of-function mutants that maintain high levels of thylakoid structures during chromoplast development in ripening fruits. Here, by overexpressing SGR in nonilluminated Nicotiana benthamiana leaves, we demonstrated that SGR triggers the onset of chloroplast deterioration, resulting in the formation of orange-leaf sectors containing plastids with carotenoid-bearing structures, although carotenoid production is not induced. Metabolite, microscopy, and transcriptome analyses suggested the onset of chloroplast senescence, indicating a possible transitional plastid stage in SGR-overexpressing regions. Overall, our work demonstrates the remarkable ability of plant plastids to adapt their ultrastructure to accommodate the precise metabolic composition of various developmental and environmental contexts.