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

Veach, Allison M.; Morris, Reese; Yip, Daniel Z.; Yang, Zamin K.; Engle, Nancy L.; Cregger, Melissa A.; Tschaplinski, Timothy J.; Schadt, Christopher W.

doi:10.1186/s40168-019-0668-8

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

Journal Article · 18 May 2019 · Microbiome

DOI: https://doi.org/10.1186/s40168-019-0668-8 · OSTI ID:1618948

Veach, Allison M. ^[1]; Morris, Reese ^[1]; Yip, Daniel Z. ^[1]; Yang, Zamin K. ^[1]; Engle, Nancy L. ^[1]; Cregger, Melissa A. ^[1]; Tschaplinski, Timothy J. ^[1];

^[2]

Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States); Univ. of Tennessee, Knoxville, TN (United States)

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.

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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, Vol. 7, Issue 1; ISSN 2049-2618

Publisher:: BioMed CentralCopyright Statement

Country of Publication:: United States

Language:: English

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Resistance of pea roots to endomycorrhizal fungus or Rhizobium correlates with enhanced levels of endogenous salicylic acid Blilou, I.; Ocampo, J. A.; Garcia-Garrido, J. M. . Journal of Experimental Botany, Vol. 50, Issue 340 https://doi.org/10.1093/jxb/50.340.1663	journal	November 1999
Salicylic acid beyond defence: its role in plant growth and development Rivas-San Vicente, M.; Plasencia, J. Journal of Experimental Botany, Vol. 62, Issue 10 https://doi.org/10.1093/jxb/err031	journal	February 2011
Growth and dry-matter partitioning of young Populus trichocarpa in response to carbon dioxide concentration and mineral nutrient availability Sigurdsson, B. D.; Thorgeirsson, H.; Linder, S. Tree Physiology, Vol. 21, Issue 12-13 https://doi.org/10.1093/treephys/21.12-13.941	journal	August 2001
Impact of ectomycorrhizal colonization and rust infection on the secondary metabolism of poplar (Populus trichocarpa x deltoides) Pfabel, C.; Eckhardt, K. -U.; Baum, C. Tree Physiology, Vol. 32, Issue 11 https://doi.org/10.1093/treephys/tps093	journal	October 2012
Salicylic Acid in Rice (Biosynthesis, Conjugation, and Possible Role) Silverman, P.; Seskar, M.; Kanter, D. Plant Physiology, Vol. 108, Issue 2 https://doi.org/10.1104/pp.108.2.633	journal	June 1995
Ozone Sensitivity in Hybrid Poplar Correlates with Insensitivity to Both Salicylic Acid and Jasmonic Acid. The Role of Programmed Cell Death in Lesion Formation Koch, Jennifer Riehl; Creelman, Robert A.; Eshita, Steven M. Plant Physiology, Vol. 123, Issue 2 https://doi.org/10.1104/pp.123.2.487	journal	June 2000
Constitutively Elevated Salicylic Acid Levels Alter Photosynthesis and Oxidative State but Not Growth in Transgenic Populus Xue, L. -J.; Guo, W.; Yuan, Y. The Plant Cell, Vol. 25, Issue 7 https://doi.org/10.1105/tpc.113.112839	journal	July 2013
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Related Subjects

59 BASIC BIOLOGICAL SCIENCES
Metabolomics
Salicylic acid
Populus trichocarpa
16S rRNA
ITS2
Rhizosphere

Additional file 1: of Rhizosphere microbiomes diverge among Populus trichocarpa plant-host genotypes and chemotypes, but it depends on soil origin Veach, Allison; Morris, Reese; Yip, Daniel https://doi.org/10.6084/m9.figshare.8148878 The current record is supplemented by this text	text	January 2019
Additional file 1: of Rhizosphere microbiomes diverge among Populus trichocarpa plant-host genotypes and chemotypes, but it depends on soil origin Veach, Allison; Morris, Reese; Yip, Daniel https://doi.org/10.6084/m9.figshare.8148878.v1 The current record is supplemented by this text	text	January 2019
Rhizosphere microbiomes diverge among Populus trichocarpa plant-host genotypes and chemotypes, but it depends on soil origin Veach, Allison; Morris, Reese; Yip, Daniel https://doi.org/10.6084/m9.figshare.c.4509980 The current record is supplemented by this collection	collection	January 2019
Rhizosphere microbiomes diverge among Populus trichocarpa plant-host genotypes and chemotypes, but it depends on soil origin Veach, Allison; Morris, Reese; Yip, Daniel https://doi.org/10.6084/m9.figshare.c.4509980.v1 The current record is supplemented by this collection	collection	January 2019