Unravelling the mechanism of phytoremediation to Pb and Cd in Euonymus japonicus Thunb. using biophysiological, transcriptomic and metabolomic analyses

Urban heavy metals (HMs) contamination necessitates sustainable eco-remediation for ecological-health security. Urban green plants are overlooked sinks for heavy metals (HMs), yet their molecular remediation mechanisms remain elusive. Here, we elucidate the physiological and molecular responses of Euonymus japonicus Thunb. to lead (Pb) and cadmium (Cd). Results demonstrate that E. japonicus Thunb. exhibits high tolerance to Pb and Cd (tolerance index > 60), with predominant sequestration of these metals in root tissues (580.0 mg·kg⁻¹ and 83.1 mg·kg⁻¹, respectively, under high concentrations of HMs), inducing ultrastructural alterations. Detoxification under severe stress is mediated by catalase and peroxidase, rather than superoxide dismutase or glutathione. Transcriptomic analysis revealed upregulation of 15 core genes associated with detoxification, including ABCG4 , ZnT2 , and Nramp3 . Metabolomic analysis revealed that root cells remodeled their metabolic regulation, including the following three aspects: (I.) amino acids and peptides (such as glycyl-phenylalanine, glutamyltyrosine, and betonicine); (II.) flavonoids (including catechin, myricetin, and persiconin); and (III.) lignan glycosides (such as occidentoside and ramontoside), thereby orchestrating stress adaptation. Mult omics analysis indicates that protein synthesis, processing, and regulation, involving amino acids, ribosomes, and the endoplasmic reticulum, along with the reprogramming of the sugar co-metabolism network and plant adaptation and stress regulation, collectively contribute to the detoxification process under Pb and Cd stress. These findings indicate that E. japonicus Thunb. serves as a root-accumulating plant capable of stabilizing HMs in soils severely co-contaminated with Pb and Cd, highlighting its potential for sustainable phytostabilization in urban environments. • Innovative tolerance mechanisms in E. japonicus thunb. have been investigated. • The endoplasmic reticula, cell walls and vacuoles are critical for the detoxification of Pb and Cd. • Up regulation of fifteen detoxification genes ( ABCG4 , ZnT2 , Nramp3 , etc.) contributes to Pb and Cd tolerance. • Reprogramming of sugar metabolism and protein biosynthesis and degradation contribute to detoxification under Pb and Cd stress. • Amino acids and peptides, flavonoids, and lignan glycosides contribute to Pb/Cd detoxification.