skip to main content
OSTI.GOV title logo U.S. Department of Energy
Office of Scientific and Technical Information

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

Journal Article · · Plant, Cell and Environment
DOI:https://doi.org/10.1111/pce.14705· OSTI ID:2229533

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.

Research Organization:
Pacific Northwest National Laboratory (PNNL), Richland, WA (United States)
Sponsoring Organization:
USDOE Office of Science (SC), Biological and Environmental Research (BER); USDOE Office of Science (SC), Basic Energy Sciences (BES). Scientific User Facilities (SUF); National Science Foundation (NSF)
Grant/Contract Number:
AC05-76RL01830; DBI-2019674
OSTI ID:
2229533
Report Number(s):
PNNL-SA-181002
Journal Information:
Plant, Cell and Environment, Vol. 46, Issue 12; ISSN 0140-7791
Publisher:
WileyCopyright Statement
Country of Publication:
United States
Language:
English

References (72)

MultiQC: summarize analysis results for multiple tools and samples in a single report journal June 2016
Accurate read-based metagenome characterization using a hierarchical suite of unique signatures journal March 2015
Influence of root structure on root survivorship: an analysis of 18 tree species using a minirhizotron method journal May 2011
Root anatomy, morphology, and longevity among root orders in Vaccinium corymbosum (Ericaceae) journal December 2008
QUAST: quality assessment tool for genome assemblies journal February 2013
DRAM for distilling microbial metabolism to automate the curation of microbiome function journal August 2020
Differential microbial assembly processes and co‐occurrence networks in the soil‐root continuum along an environmental gradient journal April 2022
Associations between species and groups of sites: indices and statistical inference journal December 2009
Phylogenetically and functionally diverse microorganisms reside under the Ross Ice Shelf journal January 2022
Nutrient Concentrations in fine Roots journal January 2000
Nitrogen storage forms in nine boreal understorey plant species journal May 1997
Huanglongbing impairs the rhizosphere-to-rhizoplane enrichment process of the citrus root-associated microbiome journal August 2017
Influence of Plant Fraction, Soil, and Plant Species on Microbiota: a Multikingdom Comparison journal February 2020
Structure, variation, and assembly of the root-associated microbiomes of rice journal January 2015
Redefining fine roots improves understanding of below-ground contributions to terrestrial biosphere processes journal March 2015
Resource availability influences the diversity of a functional group of heterotrophic soil bacteria journal September 2008
WGCNA: an R package for weighted correlation network analysis journal December 2008
Assembly and ecological function of the root microbiome across angiosperm plant species journal January 2018
Diel metabolomics analysis of a hot spring chlorophototrophic microbial mat leads to new hypotheses of community member metabolisms journal April 2015
MPLEx: a Robust and Universal Protocol for Single-Sample Integrative Proteomic, Metabolomic, and Lipidomic Analyses journal May 2016
Hydrocarbon substrate richness impacts microbial abundance, microbiome composition, and hydrocarbon loss journal September 2021
MEGAHIT: an ultra-fast single-node solution for large and complex metagenomics assembly via succinct de Bruijn graph journal January 2015
Slow decomposition of lower order roots: a key mechanism of root carbon and nutrient retention in the soil journal January 2010
Minor revision to V4 region SSU rRNA 806R gene primer greatly increases detection of SAR11 bacterioplankton journal June 2015
Heterogeneity of individual roots within the fine root architecture: causal links between physiological and ecosystem functions journal April 2007
Defining the core Arabidopsis thaliana root microbiome journal August 2012
Predicting fine root lifespan from plant functional traits in temperate trees journal June 2012
Rhizosphere size and shape: Temporal dynamics and spatial stationarity journal August 2019
Functionally discrete fine roots differ in microbial assembly, microbial functional potential, and produced metabolites - code and sequence analysis text January 2023
mdatools – R package for chemometrics journal March 2020
phyloseq: An R Package for Reproducible Interactive Analysis and Graphics of Microbiome Census Data journal April 2013
Tree‐induced alterations to soil properties and rhizoplane‐associated bacteria following 23 years in a common garden journal January 2021
Normalization and microbial differential abundance strategies depend upon data characteristics journal March 2017
The SILVA ribosomal RNA gene database project: improved data processing and web-based tools journal November 2012
KBase: The United States Department of Energy Systems Biology Knowledgebase journal July 2018
Fungal-specific PCR primers developed for analysis of the ITS region of environmental DNA extracts journal May 2005
Resource Availability Drives Responses of Soil Microbial Communities to Short-term Precipitation and Nitrogen Addition in a Desert Shrubland journal February 2018
Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2 journal July 2019
Nitrification and nitrogen removal journal January 1977
Every base matters: assessing small subunit rRNA primers for marine microbiomes with mock communities, time series and global field samples: Primers for marine microbiome studies journal October 2015
Fast gapped-read alignment with Bowtie 2 journal March 2012
FiehnLib: Mass Spectral and Retention Index Libraries for Metabolomics Based on Quadrupole and Time-of-Flight Gas Chromatography/Mass Spectrometry journal December 2009
ITS primers with enhanced specificity for basidiomycetes - application to the identification of mycorrhizae and rusts journal April 1993
Water Uptake and Hydraulics of the Root Hair Rhizosphere journal August 2008
Roots Shaping Their Microbiome: Global Hotspots for Microbial Activity journal August 2015
DADA2: High-resolution sample inference from Illumina amplicon data journal May 2016
Rhizoplane Bacteria and Plant Species Co-determine Phosphorus-Mediated Microbial Legacy Effect journal December 2019
Structural and functional differentiation of the root-associated bacterial microbiomes of perennial ryegrass journal July 2016
Methods for normalizing microbiome data: An ecological perspective journal November 2018
Endogenous and exogenous controls of root life span, mortality and nitrogen flux in a longleaf pine forest: root branch order predominates journal July 2008
Fine root morphological traits determine variation in root respiration of Quercus serrata journal February 2009
Taxonomy, Physiology, and Natural Products of Actinobacteria journal November 2015
Fine root Architecture of nine North American Trees journal May 2002
Decay rates of leaf litters from arbuscular mycorrhizal trees are more sensitive to soil effects than litters from ectomycorrhizal trees journal October 2015
Revealing structure and assembly cues for Arabidopsis root-inhabiting bacterial microbiota journal August 2012
Species- and community-level patterns in fine root traits along a 120 000-year soil chronosequence in temperate rain forest: Root trait shifts along soil chronosequence journal March 2011
The hierarchy of root branching order determines bacterial composition, microbial carrying capacity and microbial filtering journal April 2021
Physiological implications of arginine metabolism in plants journal July 2015
Rhizosphere bacteriome structure and functions journal February 2022
Anatomical traits associated with absorption and mycorrhizal colonization are linked to root branch order in twenty-three Chinese temperate tree species journal November 2008
PERMANOVA, ANOSIM, and the Mantel test in the face of heterogeneous dispersions: What null hypothesis are you testing? journal November 2013
MetaboliteDetector: Comprehensive Analysis Tool for Targeted and Nontargeted GC/MS Based Metabolome Analysis journal May 2009
UNITE: a database providing web-based methods for the molecular identification of ectomycorrhizal fungi: Methods journal March 2005
Diversity and heritability of the maize rhizosphere microbiome under field conditions journal April 2013
Functionally-explicit sampling can answer key questions about the specificity of plant–microbe interactions journal October 2022
Physical and microbial mechanisms of decomposition vary in importance among root orders and tree species with differing chemical and morphological traits journal September 2018
Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2 journal December 2014
Structure and Functions of the Bacterial Microbiota of Plants journal April 2013
fastp: an ultra-fast all-in-one FASTQ preprocessor journal September 2018
Toward an Ecological Classification of soil Bacteria journal June 2007
Root exudate metabolites drive plant-soil feedbacks on growth and defense by shaping the rhizosphere microbiota journal July 2018
Root exudates increased arsenic mobility and altered microbial community in paddy soils journal May 2023