Seed metabolites headstart haustoriogenesis and potentiate aggressiveness of parasitic weeds

Agricultural pests like parasitic broomrapes and witchweeds differentiate a haustorium that penetrates another plant's root for nutrient acquisition. We demonstrate that during imbibition and postgermination growth, parasite seeds produce bioactive haustorium-inducing factors (HIFs) to differentiate their haustorium independently of host signals, thereby challenging the paradigm of host-induced haustoriogenesis. Metabolome profiling of this seed "leachate" unraveled synergistic haustoriogenic potential of possibly canonical HIF classes at hormonal concentrations, including cytokinins, sterols, quinones, and flavonoids. We suggest that early lignin neosynthesis serves as a template for HIF production through postgerminative oxidative stress and microbial ligninolytic activity. Seedlings with host-independently formed haustoria attached faster to and produced more tubercles on compatible hosts. Thus, haustorium differentiation via a coopted autonomous developmental program potentiates the eco-evolutionary success of obligate parasitic plants.