Naphthenic Acid Fraction Compounds from Oil Sands Process-Affected Water Disrupt Plant Root Architecture and Auxin Signalling

Oil sands process-affected water (OSPW) contains naphthenic acid (NA) fraction compounds (NAFCs), structurally diverse organic acids regarded as a primary contributor to OSPW toxicity. Their persistence and complexity complicate characterization and risk assessment, while a no-discharge policy on OSPW makes reclamation an environmental priority. Phytoremediation represents a promising strategy for OSPW treatment, but its optimization requires a clearer mechanistic understanding of how NAFCs affect plant growth and development. An unresolved question is whether NAFCs act solely as toxicants or if they alter hormone signaling pathways in plants, particularly auxin signaling. Here, we demonstrate that exposure to model NAs and OSPW-derived NAFCs altered Arabidopsis thaliana seedling root development in a manner phenotypically similar to that observed in other plant species. NAFC-treated seedlings exhibited reduced primary and lateral root elongation, stimulated adventitious rooting, and disrupted gravitropic responses. Fluorescent transcriptional reporter assays confirmed that NAFC exposure enhanced auxin-responsive expression, while pharmacological experiments suggested that NAFC uptake and distribution involve auxin transporters. Auxin-induced changes in root development may limit water and nutrient acquisition and diminish plant fitness. However, variation in auxin metabolism, transport, and receptor sensitivity among plant species could offer opportunities to identify or develop genotypes better suited for remediation of OSPW-affected sites.