α-Tomatine gradient across artificial roots recreates the recruitment of tomato root-associated Sphingobium

Abstract

α-Tomatine is a major saponin that accumulates in tomatoes (Solanum lycopersicum). We previously reported that α-tomatine secreted from tomato roots modulates root-associated bacterial communities, particularly by enriching the abundance of Sphingobium belonging to the family Sphingomonadaceae. To further characterize the α-tomatine-mediated interactions between tomato plants and soil bacterial microbiota, we first cultivated tomato plants in pots containing different microbial inoculants originating from three field soils. Four bacterial genera, namely, Sphingobium, Bradyrhizobium, Cupriavidus, and Rhizobacter, were found to be commonly enriched in tomato root-associated bacterial communities. We constructed a pseudo-rhizosphere system using a mullite ceramic tube as an artificial root to investigate the influence of α-tomatine in modifying bacterial communities. The addition of α-tomatine from the artificial root resulted in the formation of a concentration gradient of α-tomatine that mimicked the tomato rhizosphere, and distinctive bacterial communities were observed in the soil close to the artificial root. Sphingobium was enriched according to the α-tomatine concentration gradient, whereas Bradyrhizobium, Cupriavidus, and Rhizobacter were not enriched in α-tomatine-treated soil. The tomato root-associated bacterial communities were similar to the soil bacterial communities in the vicinity of artificial root-secreting exudates; however, hierarchical cluster analysis revealed a distinction between root-associated and pseudo-rhizosphere bacterial communities. These results suggest that the pseudo-rhizosphere device at least partially creates a rhizosphere environment in which α-tomatine enhances the abundance of Sphingobium in the vicinity of the root. Enrichment of Sphingobium in the tomato rhizosphere was also apparent in publicly available microbiota data, further supporting the tight association between tomato roots and Sphingobium mediated by α-tomatine.