Abstract
Plant microbiomes are assembled and modified through a complex milieu of biotic and abiotic factors. Despite dynamic and fluctuating contributing variables, specific host metabolites are consistently identified as important mediators of microbial interactions. We combine information from a large-scale metatranscriptomic dataset from natural poplar trees and experimental genetic manipulation assays in seedlings of the model plant Arabidopsis thaliana to converge on a conserved role for transport of the plant metabolite myo-inositol in mediating host-microbe interactions. While microbial catabolism of this compound has been linked to increased host colonization, we identify bacterial phenotypes that occur in both catabolism-dependent and -independent manners, suggesting that myo-inositol may additionally serve as a eukaryotic-derived signaling molecule to modulate microbial activities. Our data suggest host control of this compound and resulting microbial behavior are important mechanisms at play surrounding the host metabolite myo-inositol.
Original language | English |
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Pages (from-to) | 3111-3124.e5 |
Journal | Current Biology |
Volume | 33 |
Issue number | 15 |
DOIs | |
State | Published - Aug 7 2023 |
Funding
Several isolates used in this study were originally isolated in the laboratory of Jeffery Dangl at the University of North Carolina. We would like to thank the labs of Dr. Erik Zinser and Dr. Gladys Alexandre, as well as Elise Phillips, Trevor Hancock, and Alexandra Gates, for generously providing important strains, reagents, and discussion for this work. This work is supported by the National Science Foundation grants DGE-1938092 to B.S.O. and IOS-1750717 and DEB-1638922 to S.L.L. Any opinions, findings, and conclusions or recommendations expressed in this material are those of the author(s) and do not necessarily reflect the views of the National Science Foundation. This work was additionally supported by the Science Alliance Joint Directed Research and Development Funding at Oak Ridge National Laboratory (awarded to S.L.L. and D.J.) and the Tennessee Plant Research Center (awarded to B.S.O.). This material is based upon work supported in part by the Great Lakes Bioenergy Research Center, US Department of Energy, Office of Science, Office of Biological and Environmental Research under award number DE-SC0018409. This research used resources of the Oak Ridge Leadership Computing Facility, which is a DOE Office of Science User Facility supported under contract DE-AC05-00OR22725. Funding was provided by the Plant-Microbe Interfaces (PMI) and by the Center for Bioenergy Innovation (CBI); both are supported by the Genomic Sciences Program of the Office of Biological and Environmental Research in the DOE Office of Science. The metatranscriptome sequencing conducted by the US Department of Energy Joint Genome Institute is supported by the Office of Science of the US Department of Energy under contract no. DE-AC02-05CH11231. Support for the poplar GWAS SNP dataset is provided by the US Department of Energy, Office of Science Biological and Environmental Research (BER) via the Bioenergy Science Center (BESC) under contract no. DE-PS02-06ER64304. The Poplar GWAS Project used resources of the Oak Ridge Leadership Computing Facility and the Compute and Data Environment for Science at Oak Ridge National Laboratory, which is supported by the Office of Science of the US Department of Energy under contract no. DE-AC05-00OR22725. This manuscript has been co-authored by UT-Battelle, LLC under contract no. DE-AC05-00OR22725 with the US Department of Energy. The United States Government retains and the publisher, by accepting the article for publication, acknowledges that the United States Government retains a nonexclusive, paid-up, irrevocable, world-wide license to publish or reproduce the published form of this manuscript, or allow others to do so, for United States Government purposes. The Department of Energy will provide public access to these results of federally sponsored research in accordance with the DOE Public Access Plan (http://energy.gov/downloads/doe-public-access-plan, last accessed September 16, 2020). Conceptualization, B.S.O. D.J. and S.L.L.; methodology, B.S.O. P.J. D.J. and S.L.L.; software, P.J. and D.J.; formal analysis, B.S.O. and P.J.; investigation, B.S.O. P.J. A.A.D. A.S.W. L.H.K. and B.R.K.; resources, J.-G.C. W.M. T.B.R. D.J. and S.L.L.; data curation, B.S.O. and P.J.; writing – original draft, B.S.O. and S.L.L.; writing – review & editing, B.S.O. P.J. A.A.D. A.S.W. B.R.K. T.B.R. D.J. and S.L.L.; visualization, B.S.O.; supervision, T.B.R. D.J. and S.L.L.; funding acquisition, B.S.O. D.J. and S.L.L. The authors declare no competing interests. Several isolates used in this study were originally isolated in the laboratory of Jeffery Dangl at the University of North Carolina. We would like to thank the labs of Dr. Erik Zinser and Dr. Gladys Alexandre, as well as Elise Phillips, Trevor Hancock, and Alexandra Gates, for generously providing important strains, reagents, and discussion for this work. This work is supported by the National Science Foundation grants DGE-1938092 to B.S.O. and IOS-1750717 and DEB-1638922 to S.L.L. Any opinions, findings, and conclusions or recommendations expressed in this material are those of the author(s) and do not necessarily reflect the views of the National Science Foundation. This work was additionally supported by the Science Alliance Joint Directed Research and Development Funding at Oak Ridge National Laboratory (awarded to S.L.L. and D.J.) and the Tennessee Plant Research Center (awarded to B.S.O.). This material is based upon work supported in part by the Great Lakes Bioenergy Research Center , US Department of Energy , Office of Science , Office of Biological and Environmental Research under award number DE-SC0018409 . This research used resources of the Oak Ridge Leadership Computing Facility, which is a DOE Office of Science User Facility supported under contract DE-AC05-00OR22725 . Funding was provided by the Plant-Microbe Interfaces (PMI) and by the Center for Bioenergy Innovation (CBI); both are supported by the Genomic Sciences Program of the Office of Biological and Environmental Research in the DOE Office of Science. The metatranscriptome sequencing conducted by the US Department of Energy Joint Genome Institute is supported by the Office of Science of the US Department of Energy under contract no. DE-AC02-05CH11231 . Support for the poplar GWAS SNP dataset is provided by the US Department of Energy , Office of Science Biological and Environmental Research (BER) via the Bioenergy Science Center (BESC) under contract no. DE-PS02-06ER64304 . The Poplar GWAS Project used resources of the Oak Ridge Leadership Computing Facility and the Compute and Data Environment for Science at Oak Ridge National Laboratory, which is supported by the Office of Science of the US Department of Energy under contract no. DE-AC05-00OR22725 . This manuscript has been co-authored by UT-Battelle, LLC under contract no. DE-AC05-00OR22725 with the US Department of Energy . The United States Government retains and the publisher, by accepting the article for publication, acknowledges that the United States Government retains a nonexclusive, paid-up, irrevocable, world-wide license to publish or reproduce the published form of this manuscript, or allow others to do so, for United States Government purposes. The Department of Energy will provide public access to these results of federally sponsored research in accordance with the DOE Public Access Plan ( http://energy.gov/downloads/doe-public-access-plan , last accessed September 16, 2020).
Keywords
- Arabidopsis
- GWAS
- host-microbe interactions
- myo-inositol
- poplar
- root colonization