Effect of plant-derived microbial soil legacy in a grafting system—a turn for the better

Abstract Background Plant-soil feedback arises from microbial legacies left by plants in the soil. Grafting is a common technique used to prevent yield declines in monocultures. Yet, our understanding of how grafting alters the composition of soil microbiota and how these changes affect subsequent crop performance remains limited. Our experiment involved monoculturing ungrafted and grafted watermelons to obtain conditioned soils, followed by growing the watermelons on the conditioned soils to investigate plant-soil feedback effects. Results Ungrafted plants grew better in soil previously conditioned by a different plant (heterospecific soil) while grafted plants grew better in soil conditioned by the same plant (conspecific soil). We demonstrated experimentally that these differences in growth were linked to changes in microorganisms. Using a supervised machine learning algorithm, we showed that differences in the relative abundance of certain genera, such as Rhizobium, Chryseobacterium, Fusarium, and Aspergillus, significantly influenced the conspecific plant-soil feedback. Metabolomic analyses revealed that ungrafted plants in heterospecific soil enriched arginine biosynthesis, whereas grafted plants in conspecific soil increased sphingolipid metabolism. Elsewhere, the metagenome-assembled genomes (MAGs) of ungrafted plants identified in heterospecific soil include Chryseobacterium and Lysobacter, microorganisms having been prominently identified in earlier research as contributors to plant growth. Metabolic reconstruction revealed the putative ability of Chryseobacterium to convert D-glucono-1,5-lactone to gluconic acid, pointing to distinct disease-suppressive mechanisms and hence distinct microbial functional legacies between grafted and ungrafted plants. Conclusions Our findings show a deep impact of the soil microbial reservoir on plant growth and suggest the necessity to protect and improve this microbial community in agricultural soils. The work also suggests possibilities of optimizing microbiota-mediated benefits through grafting herein, a way that “engineered” soil microbial communities for better plant growth. Video Abstract