Inter-plant communication in broccoli (Brassica oleracea var. italica) through root colonization with the endophytic fungus Trichoderma hamatum: New findings in a “wired communication”

Inter-plant communication has emerged as a critical yet poorly understood component of plant defense strategies, particularly belowground and beyond mycorrhizal systems. Our work demonstrates that the endophytic fungus Trichoderma hamatum mediates effective “wired communication” between neighboring broccoli ( Brassica oleracea var. italica ) plants, enhancing resistance against the necrotrophic pathogen Sclerotinia sclerotiorum . Using a novel axenic culture system that allows controlled hyphal connections between plant roots, we show that foliar infection of one plant triggers systemic defense priming in an adjacent, non-infected plant, but only in the presence of T. hamatum . This inter-plant signaling resulted in a significant reduction of leaf lesion development, increased tissue vitality and reduced oxidative damage in the receiver plant. Mechanistically, fungal-mediated communication was associated with dynamic changes in root colonization patterns rather than with detectable metabolic reprogramming of the fungal mycelium. Defense activation in receiver plants involved strong hormonal rebalancing, characterized by local salicylic acid (SA)–mediated responses in roots and systemic jasmonic acid (JA)–dependent defenses in leaves. Untargeted metabolomics revealed the accumulation of defense-related metabolites, including neoglucobrassicin and lipid-derived compounds linked to SA and JA signaling, in plants that received the fungal-transmitted warning signal. Our findings extend the concept of inter-plant communication to non-mycorrhizal endophytic fungi and identify T. hamatum as an active biological conduit for defense signaling in an agriculturally relevant crop. This work highlights fungal-mediated plant connectivity as an ecologically and agronomically relevant mechanism with potential applications in sustainable disease management. • T. hamatum enables defense signaling between neighboring plants via root networks. • Interplant protection depends on fungal root colonization, not metabolites. • Foliar infection alters JA–SA crosstalk and Trichoderma root colonization. • SA-mediated root defenses limit Trichoderma spread and trigger systemic JA. • JA-driven lipid accumulation enhances broccoli resistance to S. sclerotiorum .