Horizontally acquired IbACS gene modulates rhizosphere microbiota and contributes to sweet potato growth

Abstract

Ipomoea batatas (sweet potato) exhibits tolerance to nutrient-poor environments and has historically been utilized as a staple crop during periods of food scarcity. Previously, genomic studies have identified Agrobacterium-derived sequences in the sweet potato genome. Among these, the IbACS (Agrocinopine Synthase) gene encodes an enzyme responsible for the biosynthesis of agrocinopine A, a sugar-phosphodiester opine that can be metabolized and utilized by specific microorganisms harboring the corresponding catabolic enzymes. Because IbACS has been conserved in cultivated sweet potato varieties, it is suggested that endogenous agrocinopine production by sweet potato contributes to interactions with environmental microbes, thereby supporting plant growth under nutrient-limited conditions. To test this hypothesis, we generated IbACS-disrupted lines using genome editing. Growth of the knockout plants was markedly reduced in non-sterile soil, while no difference was observed in sterile conditions. These results suggest that the role of IbACS is linked to interactions with the microbial community rather than to intrinsic plant development. Metagenomic analyses of rhizosphere communities revealed that IbACS disruption caused extensive remodeling of microbial composition, including strong reductions in Proteobacteria taxa such as Oxalobacteraceae and decreases in key genera like Massilia and Ensifer, along with lower community evenness and the expansion of opportunistic minor taxa. Together, these microbial shifts indicate that IbACS is required for the assembly of a functionally supportive rhizosphere microbiome that promotes sweet potato growth in soil environments.