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

Cell Host Microbe. 2024 Apr 10;32(4):543-556.e6. doi: 10.1016/j.chom.2024.02.014. Epub 2024 Mar 12.

Abstract

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.

Keywords: SWEET sugar transporter; microbe-metabolite interdependency; root microbiota; spatial metabolite patterning; spatial rhizobiota organization.

MeSH terms

  • Arabidopsis Proteins* / genetics
  • Arabidopsis Proteins* / metabolism
  • Arabidopsis* / microbiology
  • Bacteria / metabolism
  • Microbiota*
  • Monosaccharide Transport Proteins / metabolism
  • Plant Roots / microbiology
  • Rhizosphere
  • Sugars / metabolism

Substances

  • Sugars
  • SWEET2 protein, Arabidopsis
  • Monosaccharide Transport Proteins
  • Arabidopsis Proteins