Rice ONAC039 Drives Leaf Senescence Through Direct Transcriptional Activation of Multiple Senescence-Associated Genes

Leaf senescence is a programmed cell death process that reallocates nutrients from aging leaves to developing parts of the plant, influencing crop yield and stress response. NAC transcription factors play a crucial role in this transition, but the upstream signals and downstream targets in rice remain largely unclear. In this study, we identify ONAC039 as a positive regulator that connects abscisic acid (ABA) signaling to chlorophyll degradation. Transcripts of ONAC039 increased during age-dependent and dark-induced senescence, as well as following ABA treatment. CRISPR-Cas9-generated mutants exhibited delayed yellowing and retained higher chlorophyll levels, whereas ONAC039 activation-tagged and overexpression lines showed accelerated senescence. ONAC039 upregulated key senescence-associated and chlorophyll catabolic genes, along with ABA signaling components. Yeast one-hybrid, chromatin immunoprecipitation, and dual-luciferase reporter assays demonstrated that ONAC039 directly binds to the promoters of three senescence-related genes and one ABA signaling gene, resulting in their transcriptional activation. Collectively, ONAC039 plays a crucial role in linking ABA signaling with senescence-associated genes in rice, providing a foundation for future studies aimed at modulating senescence timing.