FORKHEAD BOX1 promotes leaf senescence via the histone acetyltransferase HAC1 and the transcription factors TGA7 and ABF2/3

Abstract Leaf senescence is a tightly regulated developmental process influenced by complex genetic and epigenetic networks. Here, we identified AtFOX1, a previously uncharacterized forkhead box (FOX) protein in Arabidopsis (Arabidopsis thaliana), as a positive regulator of leaf senescence. Loss-of-function AtFOX1 mutants exhibit delayed senescence, whereas AtFOX1 overexpression accelerated this process. Mechanistically, AtFOX1 binds to the GTAAAA motif in the TGACG SEQUENCE-SPECIFIC BINDING PROTEIN 7 (TGA7) promoter, recruiting ARABIDOPSIS HISTONE ACETYLTRANSFERASE OF THE CBP FAMILY 1 (HAC1) to enhance histone H3 lysine 9 (H3K9) acetylation and promote TGA7 transcription. Genetic analyses demonstrated that AtFOX1-mediated senescence requires HAC1 function, while TGA7 acts downstream of HAC1. Furthermore, TGA7 directly activates ABA-RESPONSIVE ELEMENT BINDING FACTOR 2 (ABF2) and ABF3, key regulators of age- and ABA-induced leaf senescence. Disruption of ABF2/3/4 function mitigated the premature senescence phenotype resulting from TGA7 or AtFOX1 overexpression. Collectively, our findings reveal a AtFOX1-centered regulatory module controlling leaf senescence in Arabidopsis.