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

Journal Article · · Microbiome

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 /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.

Research Organization:
Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States)
Sponsoring Organization:
USDOE Office of Science (SC), Biological and Environmental Research (BER)
Grant/Contract Number:
AC05-00OR22725
OSTI ID:
1618948
Alternate ID(s):
OSTI ID: 1515698
Journal Information:
Microbiome, Journal Name: Microbiome Vol. 7 Journal Issue: 1; ISSN 2049-2618
Publisher:
Springer Science + Business MediaCopyright Statement
Country of Publication:
United Kingdom
Language:
English
Citation Metrics:
Cited by: 69 works
Citation information provided by
Web of Science

References (63)

Root colonization by arbuscular mycorrhizal fungi is affected by the salicylic acid content of the plant journal June 2003
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
Cutadapt removes adapter sequences from high-throughput sequencing reads journal May 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
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
Community analysis of arbuscular mycorrhizal fungi and bacteria in the maize mycorrhizosphere in a long-term fertilization trial: Soil microbial communities in arable fields journal August 2008
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
A Multifactor Analysis of Fungal and Bacterial Community Structure in the Root Microbiome of Mature Populus deltoides Trees journal October 2013
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
Impact of ectomycorrhizal colonization and rust infection on the secondary metabolism of poplar (Populus trichocarpa x deltoides) journal October 2012
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
Mycorrhizal colonization and seed treatment with salicylic acid to improve physiological traits and tolerance of flaxseed (Linum usitatissimum L.) plants grown under drought stress journal January 2016
The Genome of Black Cottonwood, Populus trichocarpa (Torr. & Gray) journal September 2006
Analysis of Soil Whole- and Inner-Microaggregate Bacterial Communities journal April 2004
Application of Natural Blends of Phytochemicals Derived from the Root Exudates of Arabidopsis to the Soil Reveal That Phenolic-related Compounds Predominantly Modulate the Soil Microbiome journal January 2013
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
Plant-specific effects of sunn hemp ( Crotalaria juncea ) and sudex ( Sorghum bicolor × Sorghum bicolor var. sudanense) on the abundance and composition of soil microbial community journal December 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
Growth and dry-matter partitioning of young Populus trichocarpa in response to carbon dioxide concentration and mineral nutrient availability journal August 2001
Manipulating the soil microbiome to increase soil health and plant fertility journal May 2012
Constitutively Elevated Salicylic Acid Levels Alter Photosynthesis and Oxidative State but Not Growth in Transgenic Populus journal July 2013
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
Hierarchical effects of environmental filters on the functional structure of plant communities: a case study in the French Alps journal July 2012
Ozone Sensitivity in Hybrid Poplar Correlates with Insensitivity to Both Salicylic Acid and Jasmonic Acid. The Role of Programmed Cell Death in Lesion Formation journal June 2000
Plant host and soil origin influence fungal and bacterial assemblages in the roots of woody plants journal June 2014
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
Role of Salicylic Acid in Plants journal January 1992

Cited By (4)



Figures / Tables (8)