Temporal analysis of physiological phenotypes identifies metabolic and genetic underpinnings of senescence in maize

Delayed leaf senescence (staygreen) is an important agronomic trait associated with enhanced resilience to abiotic and biotic stresses and improved productivity. While senescence induces large-scale metabolomic changes, the characterization of metabolic shifts and the identification of key metabolites and pathways determining the staygreen trait remain limited. Here, we generated a temporal map of the physiological and metabolic variation in genetically diverse maize (Zea mays) inbred lines spanning the staygreen spectrum. Integrated analysis of the captured phenotypic variation revealed substantial metabolic perturbations and identified 42 primary and 141 specialized leaf metabolites. Non-staygreen inbred lines were enriched in primary metabolites represented by sugar alcohols (notably mannitol and erythritol), and amino acids including phenylalanine and arginine. In contrast, the staygreen inbred lines accumulated higher levels of specialized metabolites, primarily phenylpropanoids. Metabolome-to-genome mapping identified 56 candidate genes expressed in adult maize leaves responsible for the metabolic changes that occur during senescence. Reverse genetics validated the role of naringenin chalcone and eriodictyol in maize and Arabidopsis thaliana leaf senescence, demonstrating a conserved function of these flavonoids across monocots and dicots. Together, our results reveal the coordinated physiological and metabolic programs that govern senescence and provide a curated set of metabolites and genes underlying this complex process.