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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:
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. 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., and Schadt, Christopher W. Sat . "Rhizosphere microbiomes diverge among Populus trichocarpa plant-host genotypes and chemotypes, but it depends on soil origin". United Kingdom. doi: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},
journal = {Microbiome},
number = 1,
volume = 7,
place = {United Kingdom},
year = {2019},
month = {5}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record
DOI: 10.1186/s40168-019-0668-8

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Cited by: 5 works
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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 descending ordermore » (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

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