A spatiotemporal single-cell atlas reveals coordinated immune, metabolic, and nutrient exchange programs and a coumarin-centered metabolic switch during soybean arbusular mycorrhizal symbiosis

Authors

D'Agostino, L., Ghose, K., Yong, L., Herrera Estrella, L., Patil, G.

Abstract

Arbuscular mycorrhizal fungi (AMF) establish intimate symbiosis with plant roots, yet the cell-type-specific regulatory and metabolic programs governing this interaction remain poorly resolved. Here, we integrate single-nucleus RNA sequencing (snRNA-seq) with spatial metabolomics across a temporal gradient of soybean root colonization (2-8 weeks post inoculation) to construct a high-resolution, multi-omic atlas of AMF symbiosis. Profiling 33,410 nuclei spanning all major root cell types, we uncover dynamic, cell-type-resolved transcriptional reprogramming coupled to spatially localized metabolite accumulation. Early colonization triggers a robust, epidermis-localized immune response alongside cortex-specific epigenetic reprogramming, mediated by RNA-directed DNA methylation machinery, suggesting active suppression of defense in fungal accommodation zones. Spatial metabolomics reveals a biphasic metabolic transition from flavonoid- and terpenoid-rich signaling states to lipid-dominated nutrient exchange, aligned with colonization progression. In parallel, coordinated carbon allocation and lipid biosynthesis pathways were activated in cortex and vascular tissues, supporting fungal dependence on host-derived fatty acids and sugars. Nutrient exchange programs, particularly nitrogen and phosphorus transport, exhibit strong pericycle and phloem specificity, highlighting systemic integration of symbiotic benefits. Through co-expression network analysis, we identify a previously uncharacterized coumarin-centered metabolic switch, governed by GmF6H1-2, that is essential for efficient colonization, as validated by natural loss-of-function variants. Collectively, this study provides a comprehensive, spatially resolved framework linking gene regulation, metabolism, and cell identity, revealing that AMF symbiosis is orchestrated through coordinated immune modulation, metabolic rewiring, and nutrient flux partitioning at single-cell resolution.

Preprint server: bioRxiv
The authors list and abstract were imported from bioRxiv on 09 Jul 2026.

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