Microbial colonisation rewires the composition and content of poplar root exudates, root and shoot metabolomes

F. Fracchia, F. Guinet, N. L. Engle, T. J. Tschaplinski, C. Veneault-Fourrey, A. Deveau

Research output: Contribution to journalArticlepeer-review

Abstract

Background: Trees are associated with a broad range of microorganisms colonising the diverse tissues of their host. However, the early dynamics of the microbiota assembly microbiota from the root to shoot axis and how it is linked to root exudates and metabolite contents of tissues remain unclear. Here, we characterised how fungal and bacterial communities are altering root exudates as well as root and shoot metabolomes in parallel with their establishment in poplar cuttings (Populus tremula x tremuloides clone T89) over 30 days of growth. Sterile poplar cuttings were planted in natural or gamma irradiated soils. Bulk and rhizospheric soils, root and shoot tissues were collected from day 1 to day 30 to track the dynamic changes of fungal and bacterial communities in the different habitats by DNA metabarcoding. Root exudates and root and shoot metabolites were analysed in parallel by gas chromatography-mass spectrometry. Results: Our study reveals that microbial colonisation triggered rapid and substantial alterations in both the composition and quantity of root exudates, with over 70 metabolites exclusively identified in remarkably high abundances in the absence of microorganisms. Noteworthy among these were lipid-related metabolites and defence compounds. The microbial colonisation of both roots and shoots exhibited a similar dynamic response, initially involving saprophytic microorganisms and later transitioning to endophytes and symbionts. Key constituents of the shoot microbiota were also discernible at earlier time points in the rhizosphere and roots, indicating that the soil constituted a primary source for shoot microbiota. Furthermore, the microbial colonisation of belowground and aerial compartments induced a reconfiguration of plant metabolism. Specifically, microbial colonisation predominantly instigated alterations in primary metabolism in roots, while in shoots, it primarily influenced defence metabolism. Conclusions: This study highlighted the profound impact of microbial interactions on metabolic pathways of plants, shedding light on the intricate interplay between plants and their associated microbial communities. 2SWtA3_gUD-Xt4Z7N25436Video Abstract.

Original languageEnglish
Article number173
JournalMicrobiome
Volume12
Issue number1
DOIs
StatePublished - Dec 2024

Funding

FF was supported by \u201CContrat Doctoral\u201D from the Lorraine Universit\u00E9 d\u2019Excellence. This research was sponsored by the Plant\u2013Microbe Interfaces Scientific Focus Area in the Genomic Science Program, the Office of Biological and Environmental Research in the U.S. Department of Energy, Office of Science. Oak Ridge National Laboratory is managed by UT-Battelle, LLC, for the U.S. Department of Energy, Office of Science (DE-AC05-00OR22725), LABEX ARBRE (ANR- 11-LABX-0002\u201301).

Keywords

  • Metabolomics
  • Microbiota
  • Populus tremula x tremuloides
  • Root exudate

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