Comparative phytotoxicity of phenanthrene and pyrene to Leymus chinensis: Insights from physiological and transcriptomic responses

Polycyclic aromatic hydrocarbons (PAHs), primarily generated from incomplete combustion of fossil fuels and biomass, are ubiquitous persistent organic pollutants in contaminated soils and pose significant risks to plant growth and ecosystem stability. Among these, phenanthrene (PHE) and pyrene (PYR) are two representative PAHs frequently detected at elevated concentrations in contaminated sites. In this study, we systematically investigated the differential phytotoxicity of PHE and PYR to Leymus chinensis , a dominant grass species in temperate grasslands, by comprehensively analyzing plant morphology, physiological and biochemical responses, and molecular mechanisms under gradient concentrations of the two pollutants. Both PHE and PYR induced phenotypic damage and growth inhibition in L. chinensis , but PHE exhibited significantly stronger phytotoxicity than PYR. The PHE treatment led to a marked accumulation of osmotic regulatory substances, significant reduction in the content of photosynthetic pigments, restricted gas exchange capacity, and more severe accumulation of reactive oxygen species and lipid peroxidation of the cell membranes, particularly in the roots. These factors indicated the presence of intense oxidative stress. A fluorescence kinetic analysis revealed that PHE more severely disrupted the structure of the Photosystem II reaction center and stability of the electron transport chain. At the transcriptional level, PHE significantly suppressed the expression of photosynthesis-related genes, key carbon assimilation enzymes, and core antioxidant enzymes. In contrast, PYR- treated plants better maintained photosynthetic function and activating the metabolic pathways involved in detoxification. A Weighted Gene Co-expression Network Analysis (WGCNA) revealed a coordinated regulatory network between photosynthesis and antioxidant defense systems and indicated that imbalance in root-leaf interactions was a key factor in PHE- induced cell death. In conclusion, L. chinensis exhibited distinct organ-specific responses and metabolic partitioning to PHE and PYR: roots primarily engaged antioxidant and detoxification systems to cope with stress, while leaves prioritized maintaining photosynthetic function integrity. PHE exerted its stronger phytotoxicity mainly through disrupting photosynthetic system structure and suppressing antioxidant defense, whereas PYR was more effectively processed by the plant through detoxification metabolic pathways. These findings provide important theoretical support for ecological risk assessment of PAH contamination and optimization of phytoremediation strategies. • PHE exceeds PYR in phytotoxicity by disrupting photosynthesis and antioxidant defense. • Roots degrade PHE; leaves metabolize PYR via organ-specific metabolic partitioning. • PHE triggers systemic oxidative stress; PYR causes localized photosynthetic impairment. • WGCNA reveals root-leaf interaction imbalance drives PHE-induced cell death.