Agricultural irrigation water serves as a critical vector for the co-transport of emerging contaminants like nanoplastics and organophosphate flame retardants, posing a poorly understood risk to crop safety and water quality. This study employed a combination of hydroponic exposure (simulating contaminated irrigation), long-term cultivation, multi-omics (transcriptomics and metabolomics), physiological assays, and computational simulations to elucidate the multiscale toxic mechanisms of aminated polystyrene nanoplastics (NPs-NH₂) and tris(1,3-dichloro-2-propyl) phosphate (TEP) in rye. We deciphered a clear toxic pathway: In the aqueous phase, van der Waals forces drove the formation of a stable NP-TEP complex with enhanced bioavailability. This complex accumulated in roots and was translocated to seeds, inducing synergistic oxidative burst (H₂O₂ increased >600%) and direct physical damage to cellular structures (e.g., starch granules and chloroplasts). Molecular docking confirmed NPs-NH₂ binding to photosystem I proteins, while TEP inhibited key metabolic enzymes (PAL, nsLTP2). Multi-omics revealed systemic reprogramming, where energy metabolism was disrupted and resources were reallocated to defense pathways (e.g., phenylpropanoid biosynthesis), at the cost of growth and nutrient storage. Consequently, co-exposure via irrigation water led to severe phenotypic injuries: synergistic inhibition of photosynthesis (net photosynthetic rate reduced by 64.9%), biomass, and seed yield (thousand-grain weight decreased), with both pollutants detected within seeds. This work defines a concrete pathway from molecular interaction in water to phenotypic damage, demonstrating that combined pollutant exposure via agricultural water poses a greater threat to crop productivity and food safety than individual contaminants, underscoring the urgent need to consider interaction mechanisms in water quality risk assessment.
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