Flooding-induced rhizosphere Clostridium assemblage prevents root-to-shoot cadmium translocation in rice by promoting the formation of root apoplastic barriers

Water managements are the most effective agricultural practices for restraining cadmium (Cd) uptake and translocation in rice, which closely correlated with rhizosphere assembly of beneficial microbiome. However, the role of the assemblage of specific microbiota in controlling root-to-shoot Cd translocation in rice remains scarcely clear. The aim of this study was to ascertain how water managements shaped rhizosphere microbiome and mediated root-to-shoot Cd translocation. To disentangle the acting mechanisms of water managements, we performed an experiment monitoring Cd uptake and transport in rice and changes in soil microbial communities in response to continuously flooding and moistening irrigation. Continuously flooding changed rhizosphere microbial communities, leading to the increased abundance of anaerobic bacteria such as Clostridium populations. Weighted gene co-expression network analysis (WGCNA) showed that a dominant OTU163, corresponding to Clostridium sp. CSP1, exhibited a strong negative correlation with root-to-shoot Cd translocation. An integrated analysis of transcriptome and metabolome further indicated that the Clostridium-secreted butyric acid was involved in the regulation of phenylpropanoid pathway in rice roots. The formation of endodermal suberized barriers and lignified xylems was remarkably enhanced in the Clostridium-treated roots, which led to more Cd retained in root cell wall and less Cd in the xylem sap. Collectively, our results indicate that the development of root apoplastic barriers can be orchestrated by beneficial Clostridium strains that are assembled by host plants grown under flooding regime, thereby inhibiting root-to-shoot Cd translocation.