Spongy mesophyll cell death is induced by jasmonic acid during leaf senescence in chrysanthemum

Leaf senescence impacts crop yield, quality, and post-harvest performance; for example leaf senescence limits the shelf life of cut flowers. Although the senescence process has been extensively studied at the whole-leaf level, its regulation at the single-cell-type level remains largely unknown. Here, we tracked the cell death process during leaf senescence at the single-cell-type resolution through integrated anatomical, multiomics, molecular and genetic analyses in chrysanthemum (Chrysanthemum morifolium Ramat.). These analyses revealed that jasmonic acid (JA) induces spongy mesophyll cell death in the initial stage of leaf senescence, mediated by the transcription factors CmNAC055 and CmNAC087. These transcription factors regulate the acyl coenzyme A oxidase gene CmACX5, encoding a key JA biosynthetic enzyme. This regulatory module is functionally conserved across diverse species, including chrysanthemum, Arabidopsis thaliana, tomato (Solanum lycopersicum), and rice (Oryza sativa). Indeed, attenuating mesophyll cell death with a JA biosynthesis inhibitor delays tomato fruit de-greening and increases rice grain yield by approximately 6%. This study establishes a dynamic landscape of cell fate determination and hormonal regulation during leaf senescence, providing strategies to increase plant production by modulating leaf senescence.