Soil microbial legacy drives crop diversity advantage: Linking ecological plant–soil feedback with agricultural intercropping

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 higher Fusarium relative abundance and more Fusarium oxysporum gene 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.