Fruit ripening involves key transcription factors (TF). Despite the established importance of WRKY TFs in plant development, the involvement of WRKY and its underlying mechanism in the regulation of fruit ripening and color transformation remain unclear. Here, we discovered a phenomenon where SlWRKY80 is involved in the ripening and color transformation of tomato. Overexpression of SlWRKY80 shortened the color transition cycle of tomato fruit, whereas loss-of-function mutation in SlWRKY80 delays this process. On the 7th day after the color breakdown (Break+7), the fruit color was bright red in SlWRKY80-overexpression lines. SlWRKY80 could bind to downstream promoters of SlSGR1 and SlPSY1, thereby exerting a positive regulatory effect on the expression levels of SlSGR1 and SlPSY1. This regulatory activity led to the facilitation of chlorophyll a decomposition and carotenoid synthesis during the transition of fruit color, ultimately accelerating fruit ripening and color change. The SlWRKY80 knockout lines (slwrky80cr-3 and slwrky80cr-4) showed light red. Thr (The 69th amino acid) mutated to Ser of SlWRKY80 (slwrky80cr-46), SlHDA1 was recruited as a regulatory factor to enhance the regulation of downstream SlPSY1 by SlWRKY80, and inhibited the SlSGR1 expression by SlWRKY80 which maybe the reason why the slwrky80cr-46 knockout lines exhibited brown color. In conclusion, SlWRKY80 regulates the expression of SlSGR1 and SlPSY1 by recruiting SlHDA1, thereby regulating chlorophyll decomposition and carotenoid synthesis, and further participating in fruit maturation and related fruit color formation. This research has important guiding significance for breeding tomato germplasm with excellent commercial traits.

SlWRKY80 recruits SlHDA1 to regulates the tomato fruit ripening and color transformation