Metabolomic reprogramming drives the invasion success of Anthemis cotula L.

Plant invasions are increasingly recognised as mechanisms driven by biochemical adaptations, yet the role of metabolomic reprogramming facilitating invasion success remains underexplored. To investigate this, we cultivated Anthemis cotula from seeds collected across its native Mediterranean and non-native Himalayan ranges under controlled conditions and compared their growth traits and metabolomic profiles. While growth parameters showed no significant differences (p > 0.05), non-native plants exhibited higher metabolite richness, particularly in root exudates. Untargeted metabolomic profiling detected 14,224 metabolites in non-native and 13,066 in native plants. Leaves, flowers, and roots shared most metabolites with similar chemical diversity (richness, inverse Simpson, Shannon, and Pielou’s evenness indices; all p > 0.5), clustering closely in PCA and NMDS analyses. Root exudates, however, showed the strongest biogeographic divergence (PERMANOVA, p = 0.008), with non-native plants producing unique compounds and native exudates exhibiting greater chemical evenness (Shannon, p = 0.036). Annotated metabolites were largely tissue-conserved, while unannotated metabolites showed pronounced geographic divergence. Non-native plants maintained ancestral above-ground chemistry but displayed significant divergence below ground, reflecting an adaptive shift in rhizosphere interactions. Molecular networking revealed denser shikimate–flavonoid clusters in non-native plants, with leaves and flowers rich in flavonoids and terpenoids, and roots and exudates featuring unique alkaloids, terpenoids, and shikimate-derived compounds. Hill diversity profiling showed non-native plants favoured rare metabolites, while native plants prioritized dominant, evenly distributed compounds. This dual strategy-conserving above-ground metabolism while diversifying below-ground chemistry, without phenotypic shifts, indicates A. cotula remodels key metabolomic modules for invasion success. Our study offers new insights into invasion biology and identifies promising biochemical markers for predicting invasion potential.