Volatile cues from pathogenic, mutualistic and saprotrophic fungi cause specific, fungus-dependent responses in poplar

Plants are exposed to complex interactions with belowground organisms, yet how they differentiate between mutualistic and pathogenic fungi before physical contact remains largely unknown. We exposed the roots of young Populus x canescens to volatile organic compounds (VOCs) emitted by either a pathogenic (Heterobasidion annosum), a saprotrophic (Postia placenta), or an ectomycorrhizal (Laccaria bicolor) fungus. VOC analysis of the shared rhizosphere headspace and leaf emissions revealed that poplar plants could perceive and respond to fungal identity solely through airborne cues. The root-zone headspace contained fungus-specific sesquiterpene fingerprints that remained similar after three and six weeks of co-cultivation: Pathogen-derived VOCs induced constant high sesquiterpene emissions from the root-zone, whereas mycorrhiza caused low but targeted emissions of specific sesquiterpenes. In contrast, saprotrophic VOCs caused a temporal shift in root-zone VOC pattern, with increased sesquiterpene emissions after six weeks. Fungal VOC exposure also altered leaf VOC emissions, enriching alkanes, esters and monoterpenes. Initially, leaf VOC emissions were fungal lifestyle-specific but they converged over time, indicating systemic signal integration of belowground signals. These findings demonstrate that trees can discriminate "friend-versus-foe" through VOCs alone, extending pattern-recognition theory beyond contact-dependent cues. Multivariate analyses suggested organ-specific chemical strategies: roots function as chemosensors decoding fungal volatilomes, while systemic adjustments shape aboveground VOC profiles. Understanding the plant response to fungal VOCs may offer potential for developing early pathogen diagnostics and further elucidate the volatile-mediated plant-fungal interactions.