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Functionally discrete fine roots differ in microbial assembly, microbial functional potential, and produced metabolites

Functionally discrete fine roots differ in microbial assembly, microbial functional potential, and produced metabolites
Functionally discrete fine roots differ in microbial assembly, microbial functional potential, and produced metabolites

Traditionally, fine roots were grouped using arbitrary size categories, rarely capturing the heterogeneity in physiology, morphology and functionality among different fine root orders. Fine roots with different functional roles are rarely separated in microbiome-focused studies and may result in confounding microbial signals and host-filtering across different root microbiome compartments. Using a 26-year-old common garden, we sampled fine roots from four temperate tree species that varied in root morphology and sorted them into absorptive and transportive fine roots. The rhizoplane and rhizosphere were characterized using 16S rRNA gene and internal transcribed spacer region amplicon sequencing and shotgun metagenomics for the rhizoplane to identify potential microbial functions. Fine roots were subject to metabolomics to spatially characterize resource availability. Both fungi and bacteria differed according to root functional type. We observed additional differences between the bacterial rhizoplane and rhizosphere compartments for absorptive but not transportive fine roots. Rhizoplane bacteria, as well as the root metabolome and potential microbial functions, differed between absorptive and transportive fine roots, but not the rhizosphere bacteria. Functional differences were driven by sugar transport, peptidases and urea transport. Our data highlights the importance of root function when examining root-microbial relationships, emphasizing different host selective pressures imparted on different root microbiome compartments.

microbial functions, rhizoplane, rhizosphere, root microbiome, root order, root physiology, spatial colonization
0140-7791
3919-3932
King, William L.
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Yates, Caylon F.
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Cao, Lily
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O'Rourke-Ibach, Sean
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Fleishman, Suzanne M.
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Richards, Sarah C.
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Centinari, Michela
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Hafner, Benjamin D.
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Goebel, Marc
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Bauerle, Taryn
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Kim, Young Mo
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Nicora, Carrie D.
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Anderton, Christopher R.
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Eissenstat, David M.
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Bell, Terrence H.
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King, William L.
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Yates, Caylon F.
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Cao, Lily
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O'Rourke-Ibach, Sean
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Fleishman, Suzanne M.
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Richards, Sarah C.
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Centinari, Michela
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Hafner, Benjamin D.
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Goebel, Marc
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Bauerle, Taryn
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Kim, Young Mo
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Nicora, Carrie D.
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Anderton, Christopher R.
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Eissenstat, David M.
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Bell, Terrence H.
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King, William L., Yates, Caylon F., Cao, Lily, O'Rourke-Ibach, Sean, Fleishman, Suzanne M., Richards, Sarah C., Centinari, Michela, Hafner, Benjamin D., Goebel, Marc, Bauerle, Taryn, Kim, Young Mo, Nicora, Carrie D., Anderton, Christopher R., Eissenstat, David M. and Bell, Terrence H. (2023) Functionally discrete fine roots differ in microbial assembly, microbial functional potential, and produced metabolites. Plant Cell and Environment, 46 (12), 3919-3932. (doi:10.1111/pce.14705).

Record type: Article

Abstract

Traditionally, fine roots were grouped using arbitrary size categories, rarely capturing the heterogeneity in physiology, morphology and functionality among different fine root orders. Fine roots with different functional roles are rarely separated in microbiome-focused studies and may result in confounding microbial signals and host-filtering across different root microbiome compartments. Using a 26-year-old common garden, we sampled fine roots from four temperate tree species that varied in root morphology and sorted them into absorptive and transportive fine roots. The rhizoplane and rhizosphere were characterized using 16S rRNA gene and internal transcribed spacer region amplicon sequencing and shotgun metagenomics for the rhizoplane to identify potential microbial functions. Fine roots were subject to metabolomics to spatially characterize resource availability. Both fungi and bacteria differed according to root functional type. We observed additional differences between the bacterial rhizoplane and rhizosphere compartments for absorptive but not transportive fine roots. Rhizoplane bacteria, as well as the root metabolome and potential microbial functions, differed between absorptive and transportive fine roots, but not the rhizosphere bacteria. Functional differences were driven by sugar transport, peptidases and urea transport. Our data highlights the importance of root function when examining root-microbial relationships, emphasizing different host selective pressures imparted on different root microbiome compartments.

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Plant Cell Environment - 2023 - King - Functionally discrete fine roots differ in microbial assembly microbial - Version of Record
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Accepted/In Press date: 18 August 2023
Published date: 7 September 2023
Additional Information: Funding Information: This research was supported by the USDA National Institute of Food and Agriculture (NIFA) Federal Appropriation under Project #PEN0 4628 (Accession #1014131), Project #PEN0 4744 (Accession #1023222) and Project #PEN0 4651 (Accession #1016233). Analysis and writing were partly supported by USDA ORG Project PENW‐2019‐03513 and the National Science Foundation (NSF) Centre for Research on Programmable Plant Systems (CROPPS; Grant number #DBI‐2019674). A portion of this research was performed on a project award (doi. org/10.46936/ltds. proj.2021.60134/60000418 awarded to WLK, THB and DME) from the Environmental Molecular Sciences Laboratory, a DOE Office of Science User Facility sponsored by the Biological and Environmental Research program under Contract No. DE‐AC05‐76RLO 1830. Pacific Northwest National Laboratory is a multiprogram national laboratory operated by Battelle for the US DOE under contract DE‐AC05‐76RLO 1830. Publisher Copyright: © 2023 The Authors. Plant, Cell & Environment published by John Wiley & Sons Ltd.
Keywords: microbial functions, rhizoplane, rhizosphere, root microbiome, root order, root physiology, spatial colonization

Identifiers

Local EPrints ID: 486536
URI: http://eprints.soton.ac.uk/id/eprint/486536
ISSN: 0140-7791
PURE UUID: 7e201026-813b-4364-85d9-edcb2a165cec
ORCID for William L. King: ORCID iD orcid.org/0000-0001-7272-8242

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Date deposited: 25 Jan 2024 17:35
Last modified: 18 Mar 2024 04:18

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Contributors

Author: William L. King ORCID iD
Author: Caylon F. Yates
Author: Lily Cao
Author: Sean O'Rourke-Ibach
Author: Suzanne M. Fleishman
Author: Sarah C. Richards
Author: Michela Centinari
Author: Benjamin D. Hafner
Author: Marc Goebel
Author: Taryn Bauerle
Author: Young Mo Kim
Author: Carrie D. Nicora
Author: Christopher R. Anderton
Author: David M. Eissenstat
Author: Terrence H. Bell

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