Foliar herbivory-enhanced mycorrhization is associated with increased levels of lipids in root and root exudates

1. Insect herbivory can affect interactions between plants and arbuscular mycorrhizal (AM) fungi through herbivore-modified root carbon pools, while the specific metabolic changes underlying fungal responses to herbivory are poorly understood. 2. Here we explored the impacts of foliar herbivory and mechanical wounding on AM colonisation and AM community composition of common ragweed (Ambrosia artemisiifolia) and the role of root metabolites in mediating these effects. 3. Foliar insect herbivory enhanced AM colonisation, whereas mechanical wounding only enhanced AM colonisation in combination with application of caterpillar oral secretions. Meanwhile, the relative abundance of Glomus species was increased in root endosphere, rhizoplane and rhizosphere soils after foliar herbivory. Foliar herbivory also increased the concentrations of fatty acids in roots but decreased phenolics, and their concentrations were significantly correlated with AM colonisation. Addition of exudates from plants exposed to herbivory resulted in increases in AM colonisation of plants without herbivory. Moreover, widely targeted metabolomic analyses revealed that foliar herbivory enhanced the relative abundance of lipids and decreased phenols in root exudates. 4. Synthesis. We show that plants can enhance their associations with arbuscular mycorrhizal (AM) fungi when subject to above-ground herbivory, possibly mediated by herbivore-induced increases in the levels of root lipids. Our findings highlight the role of root lipids in above-below-ground biological interactions, providing novel insights into plant-AM fungi integrative responses to biotic stresses.