Fungal volatiles drive lifestyle-dependent, systemic metabolic reprogramming in poplar

Abstract

O_LIRationale: Although trees encounter diverse fungal communities, it is unclear how they adjust their physiology in response to fungal ecological strategies before physical contact. We tested whether volatile organic compounds (VOCs) emitted by fungi are sufficient to induce systemic, lifestyle-consistent metabolic states in poplar roots and leaves. C_LIO_LIMethods: Populus x canescens roots were exposed to VOCs from a pathogen (Heterobasidion annosum), a saprotroph (Postia placenta) or an ectomycorrhizal mutualist (Laccaria bicolor) for six weeks in a contact-free pot-in-pot system. Untargeted LC-MS metabolomics characterized VOC-induced metabolic reprogramming in roots and leaves. C_LIO_LIKey results: Fungal VOC exposure alone reconfigured the metabolomes of roots and leaves, with strong discrimination between treatments despite belowground exposure. Poplar revealed a shared VOC-responsive component, but also fungus-specific programmes: pathogen VOCs produced a suppression-dominated systemic phenotype; saprotroph VOCs promoted lipid-centred metabolic activation; and mutualist VOCs elicited restrained, compatibility-consistent shifts with targeted pathway modulation. C_LIO_LIMain conclusion: Volatile-mediated surveillance allows trees to anticipate fungal lifestyle-associated cues and adjust systemic metabolism before physical contact occurs. This links airborne fungal cues to whole-plant physiological configuration and extends plant-fungal recognition beyond contact-dependent mechanisms. C_LI One-sentence summaryVolatile-mediated surveillance allows trees to anticipate fungal lifestyle and adjust systemic metabolism before physical contact occurs.