Populus trichocarpa and Populus deltoides Exhibit Different Metabolomic Responses to Colonization by the Symbiotic Fungus Laccaria bicolor

Within boreal and temperate forest ecosystems, the majority of trees and shrubs form beneficial relationships with mutualistic ectomycorrhizal (ECM) fungi that support plant health through increased access to nutrients as well as aiding in stress and pest tolerance. The intimate interaction between fungal hyphae and plant roots results in a new symbiotic “organ” called the ECM root tip. Little is understood concerning the metabolic reprogramming that favors the formation of this hybrid tissue in compatible interactions and what prevents the formation of ECM root tips in incompatible interactions. We show here that the metabolic changes during favorable colonization between the ECM fungus Laccaria bicolor and its compatible host, Populus trichocarpa, are characterized by shifts in aromatic acid, organic acid, and fatty acid metabolism. We demonstrate that this extensive metabolic reprogramming is repressed in incompatible interactions and that more defensive compounds are produced or retained. We also demonstrate that L. bicolor can metabolize a number of secreted defensive compounds and that the degradation of some of these compounds produces immune response metabolites (e.g., salicylic acid from salicin). Therefore, our results suggest that the metabolic responsiveness of plant roots to L. bicolor is a determinant factor in fungus–host interactions.