Summary
There now is pervasive evidence of positive effects of biodiversity on plant community productivity and functioning1,2. Some progress has been made linking diversity effects to functional trait variation3, but progress towards a mechanistic understanding remains slow4 – in part because biodiversity effects are emergent properties of communities, and mechanisms might differ between cases or environmental conditions5. Here, we analyse non-additive interactions between divergent Arabidopsis accessions in experimental plant communities. By combining concepts and designs from ecology and plant breeding with genetic methods, we identified a major effect locus at which allelic diversity promotes community productivity. In further experiments with near-isogenic lines, this diversity effect locus was resolved to a single Mendelian factor and a region representing less than 0.3% of the genome. Using plant-soil-feedback experiments, we demonstrate that allelic diversity causes genotype-specific soil legacy responses in the growth of a subsequent plant generation. This suggests that asymmetric interactions of plants with soil-borne factors drive niche complementarity, and that the effects of allelic diversity at a single locus can extend from the plant to the system-level. Our work establishes a novel, fully reductionist approach to the study of a complex ecological process. It may also pave the way to novel crop breeding strategies, which focus on phenotypic properties that do not manifest at the individual-, but only at a higher level of biological organisation.