Interspecific plant interaction via root exudates structures the disease suppressiveness of rhizosphere microbiomes

Terrestrial plants can affect the growth and health of adjacent plants via interspecific interaction. Here, we studied the mechanism by which plant root exudates affect the recruitment of the rhizosphere microbiome in adjacent plants—with implications for plant protection—using a tomato (Solanum lycopersicum)–potatoonion (Allium cepa var. agrogatum) intercropping system. First, we showed that the intercropping system results in a disease-suppressive rhizosphere microbiome that protects tomato plants against Verticillium wilt disease caused by the soilborne pathogen Verticillium dahliae. Second, 16S rRNA gene sequencing revealed that intercropping with potatoonion altered the composition of the tomato rhizosphere microbiome by promoting the colonization of specific Bacillus sp. This taxon was isolated and shown to inhibit V. dahliae growth and induce systemic resistance in tomato plants. Third, a belowground segregation experiment found that root exudates mediated the interspecific interaction between potatoonion and tomato. Moreover, experiments using split-root tomato plants found that root exudates from potatoonion, especially taxifolin—a flavonoid compound—stimulate tomato plants to recruit plant-beneficial bacteria, such as Bacillus sp. Lastly, ultra-high-pressure liquid chromatography–mass spectrometry analysis found that taxifolin alters tomato root exudate chemistry; thus, this compound acts indirectly in modulating root colonization by Bacillus sp. Our results revealed that this intercropping system can improve tomato plant fitness by changing rhizosphere microbiome recruitment via the use of signaling chemicals released by root exudates of potatoonion. This study revealed a novel mechanism by which interspecific plant interaction modulates the establishment of a disease-suppressive microbiome, thus opening up new avenues of research for precision plant microbiome manipulations.