Interspecific allelopathic interaction primes direct and indirect resistance in neighboring plants within agroforestry systems

The agroforestry system with high biodiversity enhances ecosystem stability and reduces vulnerability to environmental disturbances and diseases. Investigating the mechanisms of interspecies allelopathic interactions for disease suppression in agroforestry offers a sustainable strategy for plant disease management. Here, we used Panax ginseng cultivated under Pinus koraiensis forests, which have low occurrences of Alternaria leaf spot, as a model to explore the role of allelochemicals in disease suppression. Our findings demonstrate that foliar application of P. koraiensis needle leachates effectively enhanced the resistance of P. ginseng against Alternaria leaf spot. Using gas chromatography-mass spectrometry, we identified and quantified endo-borneol as a key compound in P. koraiensis leachates and confirmed its ability to prime resistance in neighboring P. ginseng plants. We discovered that endo-borneol not only directly activates defense-related pathways in P. ginseng to confer resistance but also indirectly recruits its beneficial rhizospheric microbiota by promoting the secretion of ginsenosides, thereby triggering induced systemic resistance. Notably, higher concentrations of endo-borneol, ranging from 10 to 100 mg/l, have a greater capacity to induce plant resistance and enhance root secretion, thereby recruiting more microbiota compared to lower concentrations ranging from 0.01 to 1 mg/l. Additionally, endo-borneol exhibits antifungal activities against the growth of the pathogen Alternaria panax when concentrations exceeded 10 mg/l. These results reveal the multifaceted functions of allelochemical endo-borneol in disease suppression within agroforestry systems and highlight its potential as an environmentally friendly agent for sustainable agriculture.