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

Title: Rhizosphere microbiomes diverge among Populus trichocarpa plant-host genotypes and chemotypes, but it depends on soil origin

Abstract

Background: Plants have developed defense strategies for phytopathogen and herbivore protection via coordinated metabolic mechanisms. Low-molecular weight metabolites produced within plant tissues, such as salicylic acid, represent one such mechanism which likely mediates plant – microbe interactions above and below ground. Salicylic acid is a ubiquitous phytohormone at low levels in most plants, yet are concentrated defense compounds in Populus, likely acting as a selective filter for rhizosphere microbiomes. We propagated twelve Populus trichocarpa genotypes which varied an order of magnitude in salicylic acid (SA)-related secondary metabolites, in contrasting soils from two different origins. After four months of growth, plant properties (leaf growth, chlorophyll content, and net photosynthetic rate) and plant root metabolomics specifically targeting SA metabolites were measured via GC-MS. In addition, rhizosphere microbiome composition was measured via Illumina MiSeq sequencing of 16S and ITS2 rRNA-genes.Results: Soil origin was the primary filter causing divergence in bacterial/archaeal and fungal communities with plant genotype secondarily influential. Both bacterial/archaeal and fungal evenness varied between soil origins and bacterial/archaeal diversity and evenness correlated with at least one SA metabolite (diversity: populin; evenness: total phenolics). The production of individual salicylic acid derivatives that varied by host genotype resulted in compositional differences for bacteria /archaeamore » (tremuloidin) and fungi (salicylic acid) within one soil origin (Clatskanie) whereas soils from Corvallis did not illicit microbial compositional changes due to salicylic acid derivatives. Several dominant bacterial (e.g., Betaproteobacteria, Acidobacteria, Verrucomicrobia, Chloroflexi, Gemmatimonadete, Firmicutes) and one fungal phyla ( Mortierellomycota) also correlated with specific SA secondary metabolites; bacterial phyla exhibited more negative interactions (declining abundance with increasing metabolite concentration) than positive interactions.Conclusions: These results indicate microbial communities diverge most among soil origin. However, within a soil origin, bacterial/archaeal communities are responsive to plant SA production within greenhouse-based rhizosphere microbiomes. Fungal microbiomes are impacted by root SA-metabolites, but overall to a lesser degree within this experimental context. These results suggest plant defense strategies, such as SA and its secondary metabolites, may partially drive patterns of both bacterial/archaeal and fungal taxa-specific colonization and assembly.« less

Authors:
; ; ; ; ; ; ; ORCiD logo
Publication Date:
Research Org.:
Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER)
OSTI Identifier:
1618948
Alternate Identifier(s):
OSTI ID: 1515698
Grant/Contract Number:  
AC05-00OR22725
Resource Type:
Journal Article: Published Article
Journal Name:
Microbiome
Additional Journal Information:
Journal Name: Microbiome Journal Volume: 7 Journal Issue: 1; Journal ID: ISSN 2049-2618
Publisher:
Springer Science + Business Media
Country of Publication:
United Kingdom
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; Metabolomics; Salicylic acid; Populus trichocarpa; 16S rRNA; ITS2; Rhizosphere

Citation Formats

Veach, Allison M., Morris, Reese, Yip, Daniel Z., Yang, Zamin K., Engle, Nancy L., Cregger, Melissa A., Tschaplinski, Timothy J., and Schadt, Christopher W. Rhizosphere microbiomes diverge among Populus trichocarpa plant-host genotypes and chemotypes, but it depends on soil origin. United Kingdom: N. p., 2019. Web. doi:10.1186/s40168-019-0668-8.
Veach, Allison M., Morris, Reese, Yip, Daniel Z., Yang, Zamin K., Engle, Nancy L., Cregger, Melissa A., Tschaplinski, Timothy J., & Schadt, Christopher W. Rhizosphere microbiomes diverge among Populus trichocarpa plant-host genotypes and chemotypes, but it depends on soil origin. United Kingdom. https://doi.org/10.1186/s40168-019-0668-8
Veach, Allison M., Morris, Reese, Yip, Daniel Z., Yang, Zamin K., Engle, Nancy L., Cregger, Melissa A., Tschaplinski, Timothy J., and Schadt, Christopher W. Sat . "Rhizosphere microbiomes diverge among Populus trichocarpa plant-host genotypes and chemotypes, but it depends on soil origin". United Kingdom. https://doi.org/10.1186/s40168-019-0668-8.
@article{osti_1618948,
title = {Rhizosphere microbiomes diverge among Populus trichocarpa plant-host genotypes and chemotypes, but it depends on soil origin},
author = {Veach, Allison M. and Morris, Reese and Yip, Daniel Z. and Yang, Zamin K. and Engle, Nancy L. and Cregger, Melissa A. and Tschaplinski, Timothy J. and Schadt, Christopher W.},
abstractNote = {Background: Plants have developed defense strategies for phytopathogen and herbivore protection via coordinated metabolic mechanisms. Low-molecular weight metabolites produced within plant tissues, such as salicylic acid, represent one such mechanism which likely mediates plant – microbe interactions above and below ground. Salicylic acid is a ubiquitous phytohormone at low levels in most plants, yet are concentrated defense compounds in Populus, likely acting as a selective filter for rhizosphere microbiomes. We propagated twelve Populus trichocarpa genotypes which varied an order of magnitude in salicylic acid (SA)-related secondary metabolites, in contrasting soils from two different origins. After four months of growth, plant properties (leaf growth, chlorophyll content, and net photosynthetic rate) and plant root metabolomics specifically targeting SA metabolites were measured via GC-MS. In addition, rhizosphere microbiome composition was measured via Illumina MiSeq sequencing of 16S and ITS2 rRNA-genes.Results: Soil origin was the primary filter causing divergence in bacterial/archaeal and fungal communities with plant genotype secondarily influential. Both bacterial/archaeal and fungal evenness varied between soil origins and bacterial/archaeal diversity and evenness correlated with at least one SA metabolite (diversity: populin; evenness: total phenolics). The production of individual salicylic acid derivatives that varied by host genotype resulted in compositional differences for bacteria /archaea (tremuloidin) and fungi (salicylic acid) within one soil origin (Clatskanie) whereas soils from Corvallis did not illicit microbial compositional changes due to salicylic acid derivatives. Several dominant bacterial (e.g., Betaproteobacteria, Acidobacteria, Verrucomicrobia, Chloroflexi, Gemmatimonadete, Firmicutes) and one fungal phyla (Mortierellomycota) also correlated with specific SA secondary metabolites; bacterial phyla exhibited more negative interactions (declining abundance with increasing metabolite concentration) than positive interactions.Conclusions: These results indicate microbial communities diverge most among soil origin. However, within a soil origin, bacterial/archaeal communities are responsive to plant SA production within greenhouse-based rhizosphere microbiomes. Fungal microbiomes are impacted by root SA-metabolites, but overall to a lesser degree within this experimental context. These results suggest plant defense strategies, such as SA and its secondary metabolites, may partially drive patterns of both bacterial/archaeal and fungal taxa-specific colonization and assembly.},
doi = {10.1186/s40168-019-0668-8},
url = {https://www.osti.gov/biblio/1618948}, journal = {Microbiome},
issn = {2049-2618},
number = 1,
volume = 7,
place = {United Kingdom},
year = {2019},
month = {5}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record at https://doi.org/10.1186/s40168-019-0668-8

Citation Metrics:
Cited by: 5 works
Citation information provided by
Web of Science

Figures / Tables:

Fig. 1 Fig. 1: Mean plant metabolites (± standard errors) – total phenolics (Panel a), salicylic acid (Panel b), tremuloidin (Panel c), and populin (Panel d) concentrations ($μg g$ −1 fresh weight (FW)) in root tissues among genotypes and soil origin. X-axes are ordered based on rank of salicylate concentrations in descendingmore » order (BESC-289 > BESC-414). Orange bars denote secondary metabolites from genotypes grown in Clatskanie soils, whereas green bars denote Corvallis soils. Letters denote significant differences calculated from Tukey HSD tests among genotypes and soil origins. Tremuloidin only differed between soil origins therefore additional panel is included representing the mean tremuloidin concentrations across all genotypes grown in Clatskanie versus Corvallis soils (Panel c). Note Panel d Y-axis is on a logarithmic scale« less

Save / Share:

Works referenced in this record:

UCHIME improves sensitivity and speed of chimera detection
journal, June 2011


Distinct Microbial Communities within the Endosphere and Rhizosphere of Populus deltoides Roots across Contrasting Soil Types
journal, July 2011


Assembly and response rules: two goals for predictive community ecology
journal, April 1992


Salicylic Acid and Abiotic Stress Responses in Rice
journal, August 2013


Host genotype and age shape the leaf and root microbiomes of a wild perennial plant
journal, July 2016


Biosynthesis and metabolism of salicylic acid.
journal, May 1995


Dynamic root exudate chemistry and microbial substrate preferences drive patterns in rhizosphere microbial community assembly
journal, March 2018


Driving forces of soil bacterial community structure, diversity, and function in temperate grasslands and forests
journal, September 2016


Taxonomic and functional shifts in the beech rhizosphere microbiome across a natural soil toposequence
journal, August 2017


An improved Greengenes taxonomy with explicit ranks for ecological and evolutionary analyses of bacteria and archaea
journal, December 2011


Practical innovations for high-throughput amplicon sequencing
journal, September 2013


Changes in Bacterial and Archaeal Community Structure and Functional Diversity along a Geochemically Variable Soil Profile
journal, January 2008


Naive Bayesian Classifier for Rapid Assignment of rRNA Sequences into the New Bacterial Taxonomy
journal, June 2007


Age-Related Shifts in Leaf Chemistry of Clonal Aspen (Populus tremuloides)
journal, May 2006


From Genes to Ecosystems: The Genetic Basis of Condensed Tannins and Their Role in Nutrient Regulation in a Populus Model System
journal, August 2008


The UNITE database for molecular identification of fungi - recent updates and future perspectives: Letters
journal, March 2010


Defining the core Arabidopsis thaliana root microbiome
journal, August 2012


Salicylic Acid in Rice (Biosynthesis, Conjugation, and Possible Role)
journal, June 1995


Metabolic profiling reveals altered sugar and secondary metabolism in response to UGPase overexpression in Populus
journal, October 2014


Fungal Communities and Functional Guilds Shift Along an Elevational Gradient in the Southern Appalachian Mountains
journal, December 2017


Search and clustering orders of magnitude faster than BLAST
journal, August 2010


Salicylic acid beyond defence: its role in plant growth and development
journal, February 2011


Regulation of water, salinity, and cold stress responses by salicylic acid
journal, January 2014


Simplified Method for Soil Particle-Size Determination to Accompany Soil-Quality Analyses
journal, January 2001


Resistance of pea roots to endomycorrhizal fungus or Rhizobium correlates with enhanced levels of endogenous salicylic acid
journal, November 1999


The Genome of Black Cottonwood, Populus trichocarpa (Torr. & Gray)
journal, September 2006


Analysis of Soil Whole- and Inner-Microaggregate Bacterial Communities
journal, April 2004


Plant–Soil–Microorganism Interactions: Heritable Relationship Between Plant Genotype and Associated soil Microorganisms
journal, March 2008


Salicylic acid modulates colonization of the root microbiome by specific bacterial taxa
journal, July 2015


MICROBIAL DIVERSITY IN SOIL: Selection of Microbial Populations by Plant and Soil Type and Implications for Disease Suppressiveness
journal, September 2004


Genetically based trait in a dominant tree affects ecosystem processes: Plant genetics impact ecosystems
journal, February 2004


Development of specific rhizosphere bacterial communities in relation to plant species, nutrition and soil type
journal, April 2004


The rhizosphere microbiome and plant health
journal, August 2012


The plant microbiome
journal, June 2013


Salicylic Acid: A Likely Endogenous Signal in the Resistance Response of Tobacco to Viral Infection
journal, November 1990


Salicylic acid-induced abiotic stress tolerance and underlying mechanisms in plants
journal, June 2015


QIIME allows analysis of high-throughput community sequencing data
journal, April 2010


Basic local alignment search tool
journal, October 1990


The Populus holobiont: dissecting the effects of plant niches and genotype on the microbiome
journal, February 2018


Manipulating the soil microbiome to increase soil health and plant fertility
journal, May 2012


Microbiome Datasets Are Compositional: And This Is Not Optional
journal, November 2017


The Effect of Soil Texture on Richness and Diversity of Bacterial Communities
journal, December 2011


Aspen Defense Chemicals Influence Midgut Bacterial Community Composition of Gypsy Moth
journal, December 2014


Plant root-microbe communication in shaping root microbiomes
journal, January 2016


Salicylic acid in plant defence—the players and protagonists
journal, October 2007


Revealing structure and assembly cues for Arabidopsis root-inhabiting bacterial microbiota
journal, August 2012


The diversity and biogeography of soil bacterial communities
journal, January 2006


Role of Salicylic Acid in Plants
journal, June 1992


Plant host and soil origin influence fungal and bacterial assemblages in the roots of woody plants
journal, June 2014


Salicylic Acid and Jasmonic Acid Signaling Defense Pathways Reduce Natural Bacterial Diversity on Arabidopsis thaliana
journal, December 2007


Effects of Jasmonic Acid, Ethylene, and Salicylic Acid Signaling on the Rhizosphere Bacterial Community of Arabidopsis thaliana
journal, April 2011


Structure and Functions of the Bacterial Microbiota of Plants
journal, April 2013


Basic Local Alignment Search Tool
journal, October 1990


Role of Salicylic Acid in Plants
journal, January 1992


    Works referencing / citing this record:

      Figures/Tables have been extracted from DOE-funded journal article accepted manuscripts.