Tree provenance legacy effect on belowground fungal community structure: Evidence from a Scots pine common garden experiment

Provenance effects in forest trees are well known for growth and productivity, but their influence on below-ground microbial partners remains underexplored. We investigated fungal communities associated with Scots pine from ten European provenances grown for 40 years in a common garden in Poland. Using high-throughput sequencing, we characterized both bulk-soil fungi and root endophytes and tested whether provenance identity shapes their taxonomic and functional composition. Additionally, to test the proposed provenance effect, we sourced provenance climatic conditions (PCC) data and investigated root traits and soil characteristics. Provenance explained up to 15 % of the variance in fungal community structure, with consistent effects in both soil and root-associated fractions. Fungal lifestyle groups also shifted with provenance. Soil saprotrophs were significantly less abundant in provenances originating from drier climates (spring: η 2 = 0.14, autumn: η 2 = 0.15). Ectomycorrhizal (ECM) fungi showed distinct lineage-level patterns (p < 0.001; spring: /boletus, /inocybe, /russula-lactarius, /tomentella-thelephora; autumn: /boletus, /cenococcum, /hydnotrya, /russula-lactarius, and /tomentella-thelephora). Indicator species analyses identified five ECM taxa associated with specific provenances, suggesting selective filtering by host origin. PCC variables, particularly precipitation, were significant predictors of fungal functional composition, suggesting legacy effects of seed origin environments. These findings demonstrate that tree provenance not only affects host growth performance but also shapes the composition and function of below-ground fungal communities. Considering the pivotal role of fungi in soil processes and forest resilience, provenance selection in reforestation and assisted migration strategies should account for below-ground biodiversity consequences, not solely above-ground growth traits. • Below-ground traits are key in Scots pine adaptation to distinct environments. • The community structure of below-ground fungi varies by the origin of the host tree. • Fungal community taxonomic structure drives variation in potential soil function. • Scots pines of various origins host communities with different ECM:saprotrophs ratios. • Forest management uses of provenance transfer should consider effects on soil ecology.