Integrated proteomic and metabolomic analyses revealed molecular adjustments in Populus × canescens colonized with the ectomycorrhizal fungus Paxillus involutus, which limited plant host growth.

Ectomycorrhizae (ECMs) are a highly context-dependent interactions that are not always beneficial for the plant host, sometimes leading to a decrease in plant growth. However, the molecular status of these plants remains unknown. We studied Populus × canescens microcuttings characterized by impaired growth in response to colonization by a Paxillus involutus strain via integrative proteomics-metabolomics analyses. The analysed strain was characterized by low compatibility and formed only mantles, not a Hartig net, in the majority of root tips. The increased abundance of photosynthetic proteins and foliar carbohydrates co-occurred with signals of intensified resource exchange via the stems of colonized plants. In the roots, intensified C metabolism resulted in the biosynthesis of secondary C compounds unavailable to the fungal partner but also C skeletons necessary to increase insufficient N uptake from the hyphae. The stress response was also detected in colonized plants but was similar to that reported previously during mutualistic ECM interactions. In colonized poplar plants, mechanisms to prevent imbalanced C/N trade-offs were activated. Root metabolism strongly depended on features of the whole plant, especially the foliar C/N budget. However, despite ECM-triggered growth impairment and the foliar nutrient status, the fungal partner was recognized to be a symbiotic partner.