Cation-π Interactions with Coexisting Heavy Metals Enhanced the Uptake and Accumulation of Polycyclic Aromatic Hydrocarbons in Spinach

Few studies have considered the effect of co-occurring heavy metals on plant accumulation of hydrophobic organic compounds (HOCs), and less is known about the role of intermolecular interactions. This study investigated the molecular mechanisms of Cu/Zn effects on hydroponic uptake of four deuterated polycyclic aromatic hydrocarbons (PAHs-d(10)) by spinach (Spinacia oleracea L.). Both solubility enhancement experiment and quantum mechanical calculations demonstrated the existence of [PAH-Cu(H2O)(0-4)](2+) and [2.PAH-Cu(H2O)(0-2)](2+) via cation-pi interactions when Cu2+ concentration was <= 100 mu mol/L. Notably, PAH-d(10) concentrations in both roots and shoots increased significantly with Cu2+ concentration. This was because the formation of phytoavailable PAH-Cu2+ complexes decreased PAH-d(10) hydrophobicity and consequently decreased their sorption onto dissolved organic carbon (DOC, i.e., root exudates), thereby increasing phytoavailable concentrations and uptake of PAHs-d(10). X-ray absorption near-edge structure analysis showed that PAH-Cu2+ complexes could enter defective spinach roots via apoplastic pathway. However, Zn2+ and PAHs-d(10) cannot form the cation-pi interactions because of the high desolvation penalty of Zn2+. Actually, Zn2+ decreased the spinach uptake of PAHs-d(10) due to the increase of DOC induced by Zn. This work provides molecular insights into how metals could selectively affect the plant uptake of HOCs and highlights the importance of considering the HOC phytoavailability with coexisting metals.