Interspecific transfer of specialized metabolites in root exudates coincides with root chromatin regulation and systemic chemical defenses in rice

Benzoxazinoids are a paradigmatic class of indole-derived specialized metabolites released into the soil through root exudates and originally studied for their allelopathic and toxic effects on neighboring plants, herbivores, and microorganisms. They are now recognized as regulators of diverse plant-organism interactions, with beneficial effects such as in microbiome-mediated resistance to pathogens in plant successions. However, the mechanisms by which benzoxazinoid-containing root exudates contribute to pathogen control beyond microbiome structuring remain unclear. Here, using an agriculturally relevant rice-maize co-culture system, we show that benzoxazinoids naturally exuded by maize roots are taken up by rice roots and are associated with reduced rice blast disease in leaves. This protection occurs without detectable benzoxazinoids accumulation, constitutive immune activation, or growth penalty in rice leaves. Instead, maize-derived benzoxazinoids uptake in rice roots is associated with chromatin hyperacetylation at, and increased expression of key phenylpropanoid biosynthetic genes, and broad metabolome reconfiguration. These effects extend systemically to leaves, where rice establishes a defense-related chemical state distinct from systemic acquired resistance as observed in benzoxazinoid-dependent, microbiome-mediated plant-soil feedbacks. Our findings support a model in which specialized metabolites released through root exudation by one crop species can be acquired by a neighboring species and trigger chromatin-associated metabolic reprogramming linked to systemic chemical defenses. This work provides a molecular framework connecting plant-plant interaction, root exudates, chromatin regulation, systemic chemical defense, and disease suceptibility, opening new perspectives for exploiting natural plant-plant chemical interactions in sustainable and resilient agroecosystems. Significance statementHormesis, whereby low or moderate exposure to otherwise harmful compounds stimulates adaptive beneficial responses, has rarely been used as a conceptual framework for understanding interactions between organisms. Here, we show that naturally exuded benzoxazinoids, specialized metabolites historically viewed mainly as broadly toxic coumpounds in exogenous treatments, can trigger beneficial systemic responses in a neighboring crop species. In rice, root acquisition of maize-derived benzoxazinoids is associated with histone hyperacetylation, defense-related metabolome reprogramming, and reduced susceptibility to rice blast disease in leaves without obvious growth penalty. These findings reveal a hormesis-like process in plant-plant interactions, in which interspecific chemical exposure modulates receiver physiology rather than simply causing toxicity. More broadly, this work suggests that beneficial responses to natural-dose chemical cocktails may be an underexplored driver of adaptive responses in complex biological systems, with implications for agroecology, ecotoxicology, and exposome research.