Leaf senescence is a highly-programmed developmental process during the plant life cycle. ABA plays an important role in leaf senescence. However, the mechanism underlying ABA-mediated leaf senescence, particularly the upstream epigenetic regulatory network, remains largely unclear. Here, we demonstrated that SlJMJ4, a Jumonji C (jmjC) domain-containing protein in tomato (Solanum lycopersicum), specifically demethylates di- and trimethylations of lysine 27 of histone H3 (H3K27) in vitro and in vivo. Overexpression of SlJMJ4 results in a premature senescence phenotype and promotes dark- and ABA-induced leaf senescence in tomato. Under dark conditions, SlJMJ4-promoted leaf senescence is associated with upregulated expression of transcription factors (SlORE1 and SlNAP2) and senescence-associated genes (SlSAG113 and SlSAG12) via removal of H3K27me3. In response to ABA, overexpression of SlJMJ4 increases its binding at the loci of SlORE1, SlNAP2, SlSAG113, SlSAG12, SlABI5, and SlNCED3 and decreases their H3K27me3 levels, thereby activating their expression and mediating ABA-induced leaf senescence in tomato. Taken together, these results demonstrate that SlJMJ4 plays a positive role in leaf senescence in tomato and functions in ABA-induced leaf senescence by binding to many key genes related to ABA synthesis and signaling, transcription regulation, and senescence, thus promoting their H3K27me3 demethylation.

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