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Abstract Productivity benefits from diversity can arise when compatible pathogen hosts are buffered by unrelated neighbors, diluting pathogen impacts. However, the generality of pathogen dilution has been controversial and rarely tested within biodiversity manipulations. Here, we test whether soil pathogen dilution generates diversity- productivity relationships using a field biodiversity-manipulation experiment, greenhouse assays, and feedback modeling. We find that the accumulation of specialist pathogens in monocultures decreases host plant yields and that pathogen dilution predicts plant productivity gains derived from diversity. Pathogen specialization predicts the strength of the negative feedback between plant species in greenhouse assays. These feedbacks significantly predict the overyielding measured in the field the following year. This relationship strengthens when accounting for the expected dilution of pathogens in mixtures. Using a feedback model, we corroborate that pathogen dilution drives overyielding. Combined empirical and theoretical evidence indicate that specialist pathogen dilution generates overyielding and suggests that the risk of losing productivity benefits from diversity may be highest where environmental change decouples plant-microbe interactions. 

Abstract Although the importance of the soil microbiome in mediating plant community structures and functions has been increasingly emphasized in ecological studies, the biological processes driving crop diversity overyielding remain unexplained in agriculture. Based on the plant–soil feedback (PSF) theory and method, we quantified to what extent and how soil microbes contributed to intercropping overyielding.Soils were collected as inocula and sequenced from a unique 10‐year field experiment, consisting of monoculture, intercropping and rotation planted with wheat (Triticum aestivum), maize (Zea mays)or faba bean (Vicia faba). A PSF greenhouse study was conducted to test microbial effects on three crops' growth in monoculture or intercropping.In wheat & faba bean (W&F) and maize & faba bean (M&F) systems, soil microbes drove intercropping overyielding compared to monoculture, with 28%–51% of the overyielding contributed by microbial legacies. The overyielding effects resulted from negative PSFs in both systems, as crops, in particular faba bean grew better in soils conditioned by other crops than itself. Moreover, faba bean grew better in soils from intercropping or rotation than from the average of monocultures, indicating a strong positive legacy effect of multispecies cropping systems. However, with positive PSF and negative legacy benefit effect of intercropping/rotation, we did not observe significant overyielding in the W&M system.With more bacterial and fungal dissimilarities by metabarcoding in heterospecific than its own soil, the better it improved faba bean growth. More detailed analysis showed faba bean monoculture soil accumulated more putative pathogens with higherFusariumrelative abundance and moreFusarium oxysporumgene copies by qPCR, while in heterospecific soils, there were less pathogenic effects when cereals were engaged. Further analysis in maize/faba bean intercropping also showed an increase of rhizobia relative abundance.Synthesis and applications. Our results demonstrate a soil microbiome‐mediated advantage in intercropping through suppression of the negative PSF of pathogens and increasing beneficial microbes. As microbial mediation of overyielding is context‐dependent, we conclude that the dynamics of both beneficial and pathogenic microbes should be considered in designing cropping systems for sustainable agriculture, particularly including combinations of legumes and cereals. 

Abstract Which processes drive the productivity benefits of biodiversity remain a critical, but unanswered question in ecology. We tested whether the soil microbiome mediates the diversity‐productivity relationships among late successional plant species. We found that productivity increased with plant richness in diverse soil communities, but not with low‐diversity mixtures of arbuscular mycorrhizal fungi or in pasteurised soils. Diversity‐interaction modelling revealed that pairwise interactions among species best explained the positive diversity‐productivity relationships, and that transgressive overyielding resulting from positive complementarity was only observed with the late successional soil microbiome, which was both the most diverse and exhibited the strongest community differentiation among plant species. We found evidence that both dilution/suppression from host‐specific pathogens and microbiome‐mediated resource partitioning contributed to positive diversity‐productivity relationships and overyielding. Our results suggest that re‐establishment of a diverse, late successional soil microbiome may be critical to the restoration of the functional benefits of plant diversity following anthropogenic disturbance.