Rootstock rescues watermelon from Fusarium wilt disease by shaping protective root"‘associated microbiomes and metabolites in continuous cropping soils

Aims: The use of rootstock is effective at protecting plants from soil-borne diseases, however, the underlying mechanisms remain to be elucidated. Methods: In this study, the root-associated microbiomes and root exudate profiles of rootstock (grafted) and self-rooted (ungrafted) watermelon plants grown in plastic shelters heavily infected with Fusarium oxysporum f. sp. niveum (FON) were characterized. Results: We showed that grafting markedly controlled Fusarium wilt disease, greatly reduced FON abundance in the rhizoplane and endosphere, and improved microbial diversity across rhizosphere to endosphere in continuous cropping soils. We further found that grafting significantly changed the composition of root-associated microbiomes, improved microbial association network complexity, and had potential beneficial bacterial taxa like Streptomycetales and Sphingomonadales, and fungal taxa like Capnodiales and Sebacinales significantly enriched in grafted watermelon. The grafted watermelon also possessed a distinct root exudate profile from the ungrafted watermelon and rootstock plants, with organic acids (potential autotoxins) significantly depleted but more plant defense-related metabolites such as organosulfur compounds and benzenoids enriched in comparison to ungrafted watermelon. Conclusion: Together, our results suggest that grafting facilitates plant disease resistance potentially by direct antagonism effect through root exudates and indirectly by shaping the protective root-associated microbiomes.