Summary Plants respond to phosphorus (P) limitation through an array of morphological, physiological and metabolic changes which are part of the phosphate (Pi) starvation response ( PSR ). This response influences the establishment of the arbuscular mycorrhizal ( AM ) symbiosis in most land plants. It is, however, unknown to what extent available P and the PSR redefine plant interactions with the fungal microbiota in soil. Using amplicon sequencing of the fungal taxonomic marker ITS 2, we examined the changes in root‐associated fungal communities in the AM nonhost species Arabidopsis thaliana in response to soil amendment with P and to genetic perturbations in the plant PSR . We observed robust shifts in root‐associated fungal communities of P‐replete plants in comparison with their P‐deprived counterparts, while bulk soil communities remained unaltered. Moreover, plants carrying mutations in the phosphate signaling network genes, phr1 , phl1 and pho2 , exhibited similarly altered root fungal communities characterized by the depletion of the chytridiomycete taxon Olpidium brassicae specifically under P‐replete conditions. This study highlights the nutritional status and the underlying nutrient signaling network of an AM nonhost plant as previously unrecognized factors influencing the assembly of the plant fungal microbiota in response to P in nonsterile soil.

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Mutualistic symbiotic associations between multicellular eukaryotes and their microbiota are driven by the exchange of nutrients in a quid pro quo manner. In the widespread arbuscular mycorrhizal (AM) symbiosis involving plant roots and Glomeromycotina fungi, the mycobiont is supplied with carbon through photosynthesis, which in return supplies the host plant with essential minerals such as phosphorus (P). Most terrestrial plants are largely dependent on AM fungi for nutrients, which raises the question of how plants that are unable to form a functional AM sustain their P nutrition. AM nonhost plants can form alternative, evolutionarily younger, mycorrhizal associations such as the ectomycorrhiza, ericoid and orchid mycorrhiza. However, it is unclear how plants such as the Brassicaceae species Arabidopsis thaliana, which do not form known mycorrhizal symbioses, have adapted to the loss of these essential mycorrhizal traits. Isotope tracing experiments with root-colonizing fungi have revealed the existence of new 'mycorrhizallike' fungi capable of transferring nutrients such as nitrogen (N) and P to plants, including Brassicaceae. Here, we provide an overview of the biology of trophic relationships between roots and fungi and how these associations might support plant adaptation to climate change.

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.

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