Phenylpropanoid- and Flavonoid-Centered Metabolic Adaptation to Continuous Cropping Stress in Ornamental Gourd

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.

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.

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.

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.