Autophagy plays a dual role in chromoplast transition and degradation and is essential for fruit coloration and ripening.

The color of tomato fruits is determined by carotenoids. The process involves removing chloroplast-related components and the biogenesis of chromoplast membranes where carotenoids are stored, but how these events are coordinated is unknown. Here, we demonstrated that part of this mechanism involves macroautophagy/autophagy playing dual roles in chromoplast transition and degradation. We have used fluorescence lifetime imaging microscopy (FLIM) to show that autophagosomes containing chloroplast-derived-vesicles increased significantly during early fruit ripening, which is an essential part of a pathway to the formation of chromoplasts. Interestingly, we also showed that autophagy controls the degradation of the chromoplasts containing carotenoids at the late ripening stage through a process we named chromophagy. This affects fruit color and ABA levels, which were higher in autophagy mutants with a slower turnover of chromoplasts. We concluded that autophagy is a determinant of both fruit coloration and ripening through degrading different plastid-related cargo.Abbreviation: ABA: abscisic acid; ATG: autophagy related; AP: autophagosome; BR: breaker stage; BR + 3: 3 days after breaker stage; BR + 7: 7 days after breaker stage; CV: coefficient of variation; FLIM: fluorescence lifetime imaging microscopy; IG: immature green; LR: light red; MG: mature green; PDVs: plastid-derived-vesicles; RhB: rhodamine B; RNAi: RNA interference; RR: ripe red; TEM: transmission electron microscopy; WLL: white-light laser.