Mucoromycotina fine root endophyte engages in a nutritionally mutualistic symbiosis with Arabidopsis thaliana.

Abstract

Arabidopsis thaliana, a widely used genetic model species, is considered incapable of forming mycorrhizal associations, which support nutrient acquisition in most other land plants. Mucoromycotina "fine root endophytes" (MFREs) are a recently characterized group of mycorrhizal fungi capable of forming nutritional mutualisms with a wide range of plants, supplying nitrogen and phosphorus to host plants and gaining access to photosynthetically derived carbon. Here, we demonstrate that a wild-isolated MFRE strain, Lyc-1, successfully colonizes Arabidopsis roots under monoaxenic conditions without affecting plant growth. Using a combination of conventional light and epifluorescence microscopy, we demonstrate extensive extra- and intraradical colonization of the root cortex. Stable- and radio-isotope tracing further revealed bidirectional nutrient exchange between the host plant and the fungus. To our knowledge, this is the first demonstration of a functional, mycorrhiza-like nutritional mutualism in Arabidopsis. As Arabidopsis lacks a complete set of common symbiosis signaling pathway genes, our findings suggest that Arabidopsis-Lyc-1 symbiosis may be controlled by an alternative, so far uncharacterized, symbiotic pathway. Thus, our study not only supports the existence of multiple evolutionary routes to plant-fungal nutritional mutualisms but also establishes Arabidopsis as a genetically tractable model to study plant-fungal symbiosis, thereby opening new opportunities to dissect the molecular basis and evolution of mycorrhizal symbioses.