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

microbial functions rhizoplane rhizosphere root microbiome root order root physiology spatial colonization

Journal

Plant, cell & environment
ISSN: 1365-3040
Titre abrégé: Plant Cell Environ
Pays: United States
ID NLM: 9309004

Informations de publication

Date de publication:
Dec 2023
Historique:
revised: 12 07 2023
received: 19 01 2023
accepted: 18 08 2023
medline: 3 11 2023
pubmed: 7 9 2023
entrez: 7 9 2023
Statut: ppublish

Résumé

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.

Identifiants

pubmed: 37675977
doi: 10.1111/pce.14705
doi:

Substances chimiques

RNA, Ribosomal, 16S 0

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

3919-3932

Subventions

Organisme : USDA National Institute of Food and Agriculture
Organisme : DOE Biological and Environmental Research program
Organisme : DOE Environmental Molecular Sciences Laboratory
Organisme : NSF Centre for Research on Programmable Plant Systems

Informations de copyright

© 2023 The Authors. Plant, Cell & Environment published by John Wiley & Sons Ltd.

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Auteurs

William L King (WL)

Department of Plant Pathology and Environmental Microbiology, The Pennsylvania State University, University Park, Pennsylvania, USA.
School of Integrative Plant Science, Cornell University, Ithaca, New York, USA.

Caylon F Yates (CF)

Department of Plant Pathology and Environmental Microbiology, The Pennsylvania State University, University Park, Pennsylvania, USA.
Intercollege Graduate Degree Program in Ecology, The Pennsylvania State University, University Park, Pennsylvania, USA.

Lily Cao (L)

Department of Plant Pathology and Environmental Microbiology, The Pennsylvania State University, University Park, Pennsylvania, USA.
Intercollege Graduate Degree Program in Ecology, The Pennsylvania State University, University Park, Pennsylvania, USA.
Department of Plant Science, The Pennsylvania State University, University Park, Pennsylvania, USA.

Sean O'Rourke-Ibach (S)

Department of Plant Pathology and Environmental Microbiology, The Pennsylvania State University, University Park, Pennsylvania, USA.

Suzanne M Fleishman (SM)

Intercollege Graduate Degree Program in Ecology, The Pennsylvania State University, University Park, Pennsylvania, USA.
Department of Plant Science, The Pennsylvania State University, University Park, Pennsylvania, USA.
Department of Ecosystem Science and Management, The Pennsylvania State University, University Park, Pennsylvania, USA.

Sarah C Richards (SC)

Department of Plant Pathology and Environmental Microbiology, The Pennsylvania State University, University Park, Pennsylvania, USA.
Intercollege Graduate Degree Program in Ecology, The Pennsylvania State University, University Park, Pennsylvania, USA.
Intercollege Graduate Degree Program in International Agriculture and Development, The Pennsylvania State University, University Park, Pennsylvania, USA.

Michela Centinari (M)

Intercollege Graduate Degree Program in Ecology, The Pennsylvania State University, University Park, Pennsylvania, USA.
Department of Plant Science, The Pennsylvania State University, University Park, Pennsylvania, USA.

Benjamin D Hafner (BD)

School of Integrative Plant Science, Cornell University, Ithaca, New York, USA.

Marc Goebel (M)

Department of Natural Resources and the Environment, Cornell University, Ithaca, New York, USA.

Taryn Bauerle (T)

School of Integrative Plant Science, Cornell University, Ithaca, New York, USA.

Young-Mo Kim (YM)

Biological Sciences Division, Pacific Northwest National Laboratory, Richland, Washington, USA.

Carrie D Nicora (CD)

Biological Sciences Division, Pacific Northwest National Laboratory, Richland, Washington, USA.

Christopher R Anderton (CR)

Environmental Molecular Sciences Laboratory, Pacific Northwest National Laboratory, Richland, Washington, USA.

David M Eissenstat (DM)

Intercollege Graduate Degree Program in Ecology, The Pennsylvania State University, University Park, Pennsylvania, USA.
Department of Ecosystem Science and Management, The Pennsylvania State University, University Park, Pennsylvania, USA.

Terrence H Bell (TH)

Department of Plant Pathology and Environmental Microbiology, The Pennsylvania State University, University Park, Pennsylvania, USA.
Intercollege Graduate Degree Program in Ecology, The Pennsylvania State University, University Park, Pennsylvania, USA.
Intercollege Graduate Degree Program in International Agriculture and Development, The Pennsylvania State University, University Park, Pennsylvania, USA.
Department of Physical & Environmental Sciences, University of Toronto Scarborough, Toronto, Ontario, Canada.

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