Decoding stage-specific symbiotic programs in the Rhizophagus irregularis-tomato interaction using single-nucleus transcriptomics

Abstract

Arbuscular mycorrhizal fungi (AMF) establish a dynamic and asynchronous symbiosis with a wide range of land plants, involving distinct stages of root colonization and associated cellular responses that co-occur within the same root. Whilst decades of research have significantly advanced our understanding of the plants symbiotic gene repertoire, this spatial and temporal complexity has hindered a detailed dissection of the molecular mechanisms underlying fungal accommodation. Here, we present the first single-nucleus RNA-sequencing (snRNA-seq) dataset of Solanum lycopersicum roots colonized by Rhizophagus irregularis. Unsupervised subclustering of an AM-specific cell population resolves AM-responsive root epidermal cells as well as a developmental gradient of cortical cells across distinct stages of arbuscule formation, unveiling stage-specific transcriptional signatures during AMF colonization. Moreover, using Motif-Informed Network Inference based on single-cell EXpression data (MINI-EX), we put forward candidate transcription factors orchestrating these stage-specific transcriptional programs. Together, our data support novel hypotheses on how diverse plant developmental and physiological processes - including localized cell cycle reactivation and the integration of multiple nutritional cues - are coordinated to facilitate the establishment of a functional symbiosis. As such, this high-resolution dataset serves as a valuable resource for candidate gene prioritization and future reverse genetic studies.