Soil history strengthens plant diversity effects on fungal diversity and community assembly across the plant-soil continuum

The effects of plant species richness on soil microbial diversity and the associated ecosystem functions strengthen over time. However, the mechanisms underlying the plant diversity effects on fungal diversity and community composition along the plant-soil continuum remain largely unknown. Here, we established a plant diversity gradient (species richness level 1, 2, 3 and 6 plant species), factorially crossed with plant community-specific soil- and plant history treatments derived from a long-term field biodiversity experiment, in an Ecotron experiment. We studied the effect of plant species richness on fungal community diversity and composition across different compartments: bulk soil, rhizosphere, and roots. Using ITS amplicon sequencing, we determined fungal diversity, community composition, and assembly processes across the compartments. Fungal diversity increased significantly with plant species diversity, to varying degrees according to the compartments and history treatments. While plant history did not affect fungal community composition, shared soil history markedly increased fungal richness and affected community composition. Notably, the effect of soil and plant history on the relationship between plant species richness and the fungal diversity depended on the studied compartment, with the strongest positive plant diversity effect on fungal diversity in roots and rhizosphere soil in treatments with shared soil history. Key environmental variables were considered for exploring possible mechanisms responsible for plant species richness and history treatment effects on fungal community diversity and composition, with only plant biomass being a significant mediator. Our findings indicate that plant species richness leaves a legacy in soil, and this plant community-specific soil legacy is a significant driver of fungal diversity and community composition, but only in the compartments directly influenced by roots.