Intraspecific chemical cues drive informed germination bet-hedging in an invasive plant

Abstract Optimizing germination timing in unpredictable environments is critical for invasive annual plant populations to balance range expansion against intraspecific competition. However, the chemical mechanisms by which soil seed banks perceive population density and regulate dormancy accordingly remain poorly understood. Using the globally invasive Ambrosia trifida L. as a model, this study integrates concentration-response bioassays with combined metabolomic and transcriptomic analyses to elucidate the intraspecific chemical signaling pathways regulating seed germination. We identified four key secondary metabolites forming a functionally differentiated regulatory network (P < 0.01). Vanillin exhibits a biphasic concentration–response, promoting germination at low concentrations while inhibiting it at high levels. Umbelliferone acts as a linear germination inhibitor, whereas Trifolin serves as a linear promoter. Notably, Angelicin is exclusively seed-derived and functions as a concentration-dependent promoter, representing a seed bank-specific density signal. Integrated multi-omics analysis reveals that Angelicin upregulates ribosome biogenesis and hormone signaling while concurrently enriching nucleotide and lipid metabolism. This robust gene-metabolite co-regulation signifies a coordinated molecular reprogramming that primes seeds for rapid establishment, extending the signal's function beyond simple dormancy release. These findings provide evidence for a chemically mediated density-dependent regulatory system that integrates legacy signals from senesced vegetation with real-time cues from the seed bank, which may allow populations to dynamically modulate germination fractions in response to intraspecific density. This study offers a new perspective on bet-hedging strategies in invasive species and identifies candidate targets for management interventions based on disrupting intraspecific chemical communication.