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 × canescens (Aiton) Sm. plants to volatile organic compounds (VOCs) emitted by fungi with contrasting lifestyles: the pathogenic Heterobasidion annosum (Fr.) Bref., the saprotrophPostia placenta (Fr.) M.J. Larsen & Lombard and the ectomycorrhizal fungus Laccaria bicolor (Maire) P.D. Orton. Volatile organic compound 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 3 and 6 weeks of co-cultivation: Pathogen-derived VOCs induced constantly high sesquiterpene emissions from the root-zone, whereas mycorrhizal VOCs 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 6 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.