Field-informed simulation of perfluoroalkyl substances-contaminated irrigation water alters soybean phenotype and root transcriptome

Surface water bodies such as irrigation ponds and ditches are vital irrigation sources but can carry per- and polyfluoroalkyl substances (PFAS) from biosolid-amended fields. Field sampling showed decreasing PFAS levels from soils to ponds, with ditches serving as transport pathways; long-chain PFAS were retained in soils, while short-chain PFAS were more mobile. To test crop responses under realistic conditions, soybean plants were irrigated throughout their lifecycle with a 10-PFAS mixture (25-25,000 ppt) in a pulsed-chronic regime mimicking agricultural watering patterns. Early growth reductions were observed only at higher exposures (≥2500 ppt), with little inhibition at lower levels. All plants recovered by mid-season with no overt phytotoxicity. At maturity, reproductive output was enhanced, with bean counts and protein/carbohydrate content significantly increased, most notably at 25,000 ppt. Root transcriptome analysis revealed upregulation of aquaporins, nutrient transporters, and oxidative stress pathways, indicating coordinated shifts in water balance, metabolism, and defense. These responses align with hormesis, where early stress primes adaptive mechanisms enhancing later performance. PFAS accumulation showed distinct partitioning: short-chain PFAS, especially PFBA, dominated in beans (10.01-314.25 ng/g), while long-chain PFAS remained in roots. At the environmentally relevant 250 ppt treatment, bean PFAS concentrations were within a range where even modest dietary consumption could contribute to exceeding the European Food Safety Authority's tolerable weekly intake (4.4 ng/kg bw/week for select PFAS). While further work is needed to translate these values to dietary exposure scenarios, the results highlight the importance of considering crop resilience and food safety implications in PFAS-contaminated agricultural systems.