Belowground Fungal Volatile Exposure Induces Systemic Metabolic Reprogramming in Poplar

Although trees encounter diverse soil-associated fungi, it is unclear how they adjust their physiology in response to volatile organic compounds (VOCs) from fungi with contrasting ecological strategies before physical contact. Here, we tested whether VOCs emitted by fungi are sufficient to induce systemic, fungus-dependent metabolic responses in poplar. Populus × canescens roots were exposed to VOCs from a pathogen (Heterobasidion annosum), a saprotroph (Postia placenta), or an ectomycorrhizal mutualist (Laccaria bicolor) for 6 weeks in a contact-free pot-in-pot system. Untargeted LC-MS metabolomics was used to characterize VOC-induced metabolic reprogramming in roots and leaves. Fungal VOC exposure alone reconfigured root and leaf metabolomes, with both shared and fungus-dependent responses despite VOC exposure being restricted to the belowground compartment. Treatment-associated differences varied between tissues. H. annosum was associated with pronounced suppression of high-confidence features in leaves but a more balanced response in roots. P. placenta showed several uniquely upregulated root features together with selected lipid-associated changes, and L. bicolor produced comparatively few unique high-confidence changes. These results show that poplar can respond systemically and differentially to VOCs from contrasting fungal species before physical contact, while the extent to which these responses can be generalised across fungal lifestyles remains to be established.