Dysfunction in the arbuscular mycorrhizal symbiosis has consistent but small effects on the establishment of the fungal microbiota in Lotus japonicus

Summary Most land plants establish mutualistic interactions with arbuscular mycorrhizal (AM) fungi. Intracellular accommodation of AM fungal symbionts remodels important host traits like root morphology and nutrient acquisition. How mycorrhizal colonization impacts plant microbiota is unclear. To understand the impact of AM symbiosis on fungal microbiota, ten Lotus japonicus mutants impaired at different stages of AM formation were grown in non‐sterile natural soil and their root‐associated fungal communities were studied. Plant mutants lacking the capacity to form mature arbuscules (arb−) exhibited limited growth performance associated with altered phosphorus (P) acquisition and reduction–oxidation (redox) processes. Furthermore, arb− plants assembled moderately but consistently different root‐associated fungal microbiota, characterized by the depletion of Glomeromycota and the concomitant enrichment of Ascomycota, including Dactylonectria torresensis. Single and co‐inoculation experiments showed a strong reduction of root colonization by D. torresensis in the presence of AM fungus Rhizophagus irregularis, particularly in arbuscule‐forming plants. Our results suggest that impairment of central symbiotic functions in AM host plants leads to specific changes in root microbiomes and in tripartite interactions between the host plant, AM and non‐AM fungi. This lays the foundation for mechanistic studies on microbe–microbe and microbe–host interactions in AM symbiosis of the model L. japonicus.