The metabolic landscape of tomato roots during arbuscular mycorrhizal symbiosis reveals lipid-related metabolic rewiring.

Abstract

Key message: This study reveals lipid-related metabolic rewiring in tomato roots during arbuscular mycorrhizal symbiosis, identifying potential candidate lipids for fungal carbon transfer and signaling. Arbuscular mycorrhizal (AM) symbiosis induces substantial metabolic rearrangement in host plants to facilitate nutrient exchange and symbiotic efficiency. While previous metabolomic studies have characterized metabolite shifts in AM symbiosis, the lipid-related metabolic rewiring underlying nutrient exchange in host plant roots remains poorly resolved. Here, we investigated the metabolic response in tomato roots colonized by AM fungi. A total of 219 differentially accumulated metabolites (DAMs) were identified by the ultra-high-performance liquid chromatography-tandem mass spectrometry analysis, with lipids and lipid-like molecules representing the predominant classes. The most significantly upregulated metabolite was 2-(14,15-epoxyeicosatrienoyl) glycerol, a 2-monoacylglycerols (2-MAGs) mapped to arachidonic acid metabolism. This compound represents a C20-based epoxy fatty acid-derived 2-MAG, distinct from the C16:0 2-MAG induced by AM symbiosis in legumes, thereby implying the possibility of transferring diverse lipid substrates from different host plants to AM fungi. Concurrently, enhanced accumulation of dihomo-γ-linolenic acid (DGLA) and arachidonic acid (ARA) in AM fungi colonized roots underscored alterations of arachidonic acid metabolism and unsaturated fatty acid pathway. Gene set enrichment analysis based on the transcriptome data revealed significant transition of the glycerophospholipid metabolism pathway, primarily driven by multiple lysophosphatidylcholine (LPC) species that showed significant upregulation. Integrated transcriptomic and metabolomic analysis identified 31 overlapping KEGG pathways, emphasizing the importance of lipid and amino acid metabolism. In summary, our integrated analysis demonstrates that lipid-related metabolic reprogramming, represented by the induction of 2-MAGs and LPCs, is a feature of AM symbiosis that enables cross-kingdom nutrient exchange and host metabolic adaptation.