α-Galactosidase interacts with persistent organic pollutants to induce oxidative stresses in rice (Oryza sativa L.)

Persistent organic pollutants (POPs) in agricultural soil often triggered metabolic alterations and phytotoxicity in plants, ultimately threatening crop quality. Unraveling the phytotoxic mechanisms of POPs in crops is critical for evaluating their environmental risks. Herein, the molecular mechanism of POP-induced phytotoxicity in rice (Oryza sativa L.) was analyzed using metabolic profile, enzyme activity, and gene expression as linkages, including polycyclic aromatic hydrocarbons, polybrominated diphenyl ethers, polychlorinated biphenyls, and phthalate esters. Despite no observable changes in phenotypic traits (e.g., biomass and length of aboveground), the levels of reactive oxygen species (ROS) were promoted under stresses of the tested POPs, particularly 2,2',4,4'-tetrabromodiphenyl ether (BDE-47), dibutyl phthalate (DBP), and di(2-ethylhexyl) phthalate (DEHP). Metabolomics analysis revealed that ROS contents positively correlated with metabolic perturbation levels (r = 0.83), among which the galactose metabolism was significantly inhibited when exposed to DBP, DEHP, or BDE-47. The α-Galactosidase (α-Gal) involved in galactose metabolism was targeted as the key enzyme for the phytotoxicity of DBP, DEHP, and BDE-47, which was revealed by the inhibition of saccharide levels (45.5-82.1%), the catalytic activity of α-Gal (18.5-24.3%), and the gene expression (28.5-34.5%). Molecular docking simulation suggested that the three POPs occupied the active sites of α-Gal and formed a stable protein-ligand complex, thus inhibiting the catalytic activity of α-Gal. Partial least-squares regression analysis indicated that α-Gal activity was negatively associated with hydrogen bond acceptor, rotatable bond, and topological polar surface area of POPs. The results offered novel insights into the molecular mechanisms of phytotoxicity of POPs and provided important information for evaluating the environmental risk of POPs.