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Sugar transporters spatially organize microbiota colonization along the longitudinal root axis of Arabidopsis

Summary

Plant roots are functionally heterogeneous in cellular architecture, transcriptome profile, metabolic state, and microbial immunity. We hypothesized that axial differentiation may also impact spatial colonization by root microbiota along the root axis. We developed two growth systems, ArtSoil and CD-Rhizotron, to grow and then dissect Arabidopsis thaliana roots into three segments. We demonstrate that distinct endospheric and rhizosphere bacterial communities colonize the segments, supporting the hypothesis of microbiota differentiation along the axis. Root metabolite profiling of each segment reveals differential metabolite enrichment and specificity. Bioinformatic analyses and GUS histochemistry indicate microbe-induced accumulation of SWEET2, 4, and 12 sugar uniporters. Profiling of root segments from sweet mutants shows altered spatial metabolic profiles and reorganization of endospheric root microbiota. This work reveals the interdependency between root metabolites and microbial colonization and the contribution of SWEETs to spatial diversity and stability of microbial ecosystem.

Original Publication

Loo et al., 2024, Cell Host & Microbe 32, 543–556 April 10, 2024 ª 2024 The Author(s). Published by Elsevier Inc. https://doi.org/10.1016/j.chom.2024.02.014

License

Cell Host & Microbe 32, 543–556, April 10, 2024 ª 2024 The Author(s). Published by Elsevier Inc. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).

Data Availability

Raw 16S sequencing data have been deposited into the European Nucleotide Archive (ENA) under the accession number PRJEB63568. In addition, the scripts used for the computational analyses described in this study are available at GitHub https:// github.com/duranpa/sweet_collaboration. Raw metabolomics file is deposited at https://www.metabolomicsworkbench.org under the data track Study ID ST002779. Any additional information required to reanalyze the data reported in this paper is available from the lead contact upon request.