Beauveria bassiana triggers the tomato 'cry for help' mechanism to assemble pest-suppressing rhizomicrobiome.

Plants can specifically assemble beneficial rhizosphere microbiota through the 'cry for help' mechanism triggered by non-pathogenic elicitors, thereby promoting plant health. However, it remains unknown whether non-pathogenic strains can be used to induce plants to form a rhizomicrobiome capable of resisting herbivores. Here, we investigated how tomatoes enhance their defense capacity via the 'cry for help' response triggered by the entomopathogenic fungus Beauveria bassiana. Our findings show that B. bassiana induces the formation of beneficial soil legacy in tomatoes, which significantly impacts the performance of whitefly (Bemisia tabaci) on tomatoes. Amplicon sequencing revealed a specific enrichment of Pseudomonas in the soil legacy. Supplementing soils with Pseudomonas isolates reduced whitefly performance on tomatoes and increased the whitefly-induced levels of salicylic acid (SA) and jasmonic acid (JA) in the plants. Moreover, metabolomic and in vitro experiments demonstrated that the increased abundance of rhizosphere Pseudomonas, induced by enhanced root exudation of o-anisic acid, is responsible for the pest-suppressive effect of the soil legacy. This research uncovers a 'cry for help' mechanism whereby tomatoes, through interactions with a non-pathogenic strain, reshape their rhizosphere microbiome to bolster defense. It also deepens our understanding of microbiota-mediated plant defense and offers insights for biological control of herbivores.