Transcriptome analysis of wheat roots reveals a differential regulation of stress responses related to arbuscular mycorrhizal fungi and soil disturbance

Abstract

Symbioses with soil microorganisms are central in shaping the diversity and productivity of land plants and provide protection against a diversity of stresses, including metal toxicity. Arbuscular mycorrhizal fungi (AMF) can form extensive extraradical mycelial networks (ERM), which are very efficient in colonizing a new host. We quantified the responses of transcriptomes of wheat and one AMF partner, Rhizoglomus irregulare, to soil disturbance (Undisturbed vs. Disturbed) and to two different preceding mycotrophic species (Ornithopus compressus and Lolium rigidum). Soil disturbance and preceding plant species engender different AMF communities in wheat roots, resulting in a differential tolerance to soil manganese (Mn) toxicity. Soil disturbance negatively impacted wheat growth under manganese toxicity, probably due to the disruption of the ERM, and activated a large number of stress and starvation-related genes. The O. compressus treatment, which induces a greater Mn protection in wheat than L. rigidum, activated processes related to cellular division and growth, and very few related to stress. The L. rigidum treatment mostly induced genes that were related to oxidative stress, disease protection, and metal ion binding. R. irregulare cell division and molecular exchange between nucleus and cytoplasm were increased by O. compressus. These findings are highly relevant for sustainable agricultural systems, when considering a fit-for-purpose symbiosis.