A WUSCHEL-Related Homeobox Transcription Factor SlWOX13 Is Involved in the Regulation of Tomato Fruit Ripening

Fruit ripening is a complex, genetically programmed process involving the action of critical transcription factors (TFs). Despite the established significance of WUSCHEL-related homeobox (WOX) TFs in plant development, the involvement of WOX and its underlying mechanism in the regulation of fruit ripening remain unclear. Here, we identified that SlWOX13 is a novel regulator of fruit ripening in tomato. Overexpression of SlWOX13 accelerates fruit ripening, whereas loss-of-function mutation in SlWOX13 delays this process. Moreover, ethylene synthesis and carotenoids accumulation are significantly inhibited in slwox13 mutant fruit, but accelerated in SlWOX13 transgenic fruit. Integrated analyses of RNA-seq and ChIP-seq identified 422 direct targets of SlWOX13, of which 243 genes are negatively regulated and 179 are positively regulated by SlWOX13. EMSA, RT-qPCR, DLR and ChIP-qPCR analyses demonstrated that SlWOX13 directly binds to the promoters of ACO1, ETR4, EIL1, ERF.B3, PSY1, PDS, and BCH, and activates their expression, thereby promoting ethylene synthesis and signaling, and carotenoids biosynthesis. Furthermore, SlWOX13 modulates tomato fruit ripening through key specific ripening-related TFs, such as RIN, NOR and NAC4. Consequently, these effects promote fruit ripening. Taken together, these results demonstrate that SlWOX13 positively regulates tomato fruit ripening via both ethylene synthesis and signaling, and key transcription factors-mediated transcriptional regulation.