Background: Continuous cropping severely restricts ornamental gourd productivity through yield decline, microbial dysbiosis, and rhizosphere autotoxin production. This study characterized rhizosphere–root–leaf metabolic reorganization under three-year monoculture, identifying key metabolites, pathways, and a hierarchical cascade for stress adaptation. Methods: Ornamental gourd seedlings were potted in three-year monoculture soil exhibiting replanting disorders. At the seven-leaf stage, rhizosphere soil, roots, and leaves were sampled for untargeted UHPLC-MS/MS metabolomics, followed by PCA, OPLS-DA, differential analysis (VIP > 1, p < 0.05), and KEGG pathway enrichment analysis. Results: A total of 10,792 metabolic features were detected in positive mode and 8992 in negative mode. PCA explained 83.84% of the variance, with PC1 at 56.35% and PC2 at 27.49%, clearly separating the compartments of the study. A total of 1132 shared metabolites were suppressed, with log2 fold changes exceeding −1. Roots displayed activation, with upregulated metabolites outnumbering downregulated ones, and log2 fold changes frequently exceeding +3. Leaves exhibited mean log2 fold changes of approximately +1 for phenylpropanoid intermediates, indole, and terpenoid biosynthesis. The enriched pathways included amino acid metabolism, phenylpropanoid and flavonoid biosynthesis, lipid metabolism, and hormone signaling. Conclusions: Continuous cropping induces a hierarchical rhizosphere–root–leaf metabolic cascade, linking suppressed soil activity with reinforced root defense and coordinated leaf signaling, centered on the phenylpropanoid and flavonoid pathways as key drivers of adaptation.
Li et al. (2026) studied this question.