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Root Microbiome Modulates Plant Growth Promotion Induced by Low Doses of Glyphosate

Glyphosate is a commonly used herbicide with a broad action spectrum. However, at sublethal doses, glyphosate can induce plant growth, a phenomenon known as hormesis. Most glyphosate hormesis studies have been performed under microbe-free or reduced-microbial-diversity conditions; only a few were pe...

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Autores principales: Ramirez-Villacis, Dario X., Finkel, Omri M., Salas-González, Isai, Fitzpatrick, Connor R., Dangl, Jeffery L., Jones, Corbin D., Leon-Reyes, Antonio
Formato: Online Artículo Texto
Lenguaje:English
Publicado: American Society for Microbiology 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7426167/
https://www.ncbi.nlm.nih.gov/pubmed/32817451
http://dx.doi.org/10.1128/mSphere.00484-20
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author Ramirez-Villacis, Dario X.
Finkel, Omri M.
Salas-González, Isai
Fitzpatrick, Connor R.
Dangl, Jeffery L.
Jones, Corbin D.
Leon-Reyes, Antonio
author_facet Ramirez-Villacis, Dario X.
Finkel, Omri M.
Salas-González, Isai
Fitzpatrick, Connor R.
Dangl, Jeffery L.
Jones, Corbin D.
Leon-Reyes, Antonio
author_sort Ramirez-Villacis, Dario X.
collection PubMed
description Glyphosate is a commonly used herbicide with a broad action spectrum. However, at sublethal doses, glyphosate can induce plant growth, a phenomenon known as hormesis. Most glyphosate hormesis studies have been performed under microbe-free or reduced-microbial-diversity conditions; only a few were performed in open systems or agricultural fields, which include a higher diversity of soil microorganisms. Here, we investigated how microbes affect the hormesis induced by low doses of glyphosate. To this end, we used Arabidopsis thaliana and a well-characterized synthetic bacterial community of 185 strains (SynCom) that mimics the root-associated microbiome of Arabidopsis. We found that a dose of 3.6 × 10(−6) g acid equivalent/liter (low dose of glyphosate, or LDG) produced an ∼14% increase in the shoot dry weight (i.e., hormesis) of uninoculated plants. Unexpectedly, in plants inoculated with the SynCom, LDG reduced shoot dry weight by ∼17%. We found that LDG enriched two Firmicutes and two Burkholderia strains in the roots. These specific strains are known to act as root growth inhibitors (RGI) in monoassociation assays. We tested the link between RGI and shoot dry weight reduction in LDG by assembling a new synthetic community lacking RGI strains. Dropping RGI strains out of the community restored growth induction by LDG. Finally, we showed that individual RGI strains from a few specific phyla were sufficient to switch the response to LDG from growth promotion to growth inhibition. Our results indicate that glyphosate hormesis was completely dependent on the root microbiome composition, specifically on the presence of root growth inhibitor strains. IMPORTANCE Since the introduction of glyphosate-resistant crops, glyphosate has become the most common and widely used herbicide around the world. Due to its intensive use and ability to bind to soil particles, it can be found at low concentrations in the environment. The effect of these remnants of glyphosate in plants has not been broadly studied; however, glyphosate 1,000 to 100,000 times less concentrated than the recommended field dose promoted growth in several species in laboratory and greenhouse experiments. However, this effect is rarely observed in agricultural fields, where complex communities of microbes have a central role in the way plants respond to external cues. Our study reveals how root-associated bacteria modulate the responses of Arabidopsis to low doses of glyphosate, shifting between growth promotion and growth inhibition.
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spelling pubmed-74261672020-08-24 Root Microbiome Modulates Plant Growth Promotion Induced by Low Doses of Glyphosate Ramirez-Villacis, Dario X. Finkel, Omri M. Salas-González, Isai Fitzpatrick, Connor R. Dangl, Jeffery L. Jones, Corbin D. Leon-Reyes, Antonio mSphere Research Article Glyphosate is a commonly used herbicide with a broad action spectrum. However, at sublethal doses, glyphosate can induce plant growth, a phenomenon known as hormesis. Most glyphosate hormesis studies have been performed under microbe-free or reduced-microbial-diversity conditions; only a few were performed in open systems or agricultural fields, which include a higher diversity of soil microorganisms. Here, we investigated how microbes affect the hormesis induced by low doses of glyphosate. To this end, we used Arabidopsis thaliana and a well-characterized synthetic bacterial community of 185 strains (SynCom) that mimics the root-associated microbiome of Arabidopsis. We found that a dose of 3.6 × 10(−6) g acid equivalent/liter (low dose of glyphosate, or LDG) produced an ∼14% increase in the shoot dry weight (i.e., hormesis) of uninoculated plants. Unexpectedly, in plants inoculated with the SynCom, LDG reduced shoot dry weight by ∼17%. We found that LDG enriched two Firmicutes and two Burkholderia strains in the roots. These specific strains are known to act as root growth inhibitors (RGI) in monoassociation assays. We tested the link between RGI and shoot dry weight reduction in LDG by assembling a new synthetic community lacking RGI strains. Dropping RGI strains out of the community restored growth induction by LDG. Finally, we showed that individual RGI strains from a few specific phyla were sufficient to switch the response to LDG from growth promotion to growth inhibition. Our results indicate that glyphosate hormesis was completely dependent on the root microbiome composition, specifically on the presence of root growth inhibitor strains. IMPORTANCE Since the introduction of glyphosate-resistant crops, glyphosate has become the most common and widely used herbicide around the world. Due to its intensive use and ability to bind to soil particles, it can be found at low concentrations in the environment. The effect of these remnants of glyphosate in plants has not been broadly studied; however, glyphosate 1,000 to 100,000 times less concentrated than the recommended field dose promoted growth in several species in laboratory and greenhouse experiments. However, this effect is rarely observed in agricultural fields, where complex communities of microbes have a central role in the way plants respond to external cues. Our study reveals how root-associated bacteria modulate the responses of Arabidopsis to low doses of glyphosate, shifting between growth promotion and growth inhibition. American Society for Microbiology 2020-08-12 /pmc/articles/PMC7426167/ /pubmed/32817451 http://dx.doi.org/10.1128/mSphere.00484-20 Text en Copyright © 2020 Ramirez-Villacis et al. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Research Article
Ramirez-Villacis, Dario X.
Finkel, Omri M.
Salas-González, Isai
Fitzpatrick, Connor R.
Dangl, Jeffery L.
Jones, Corbin D.
Leon-Reyes, Antonio
Root Microbiome Modulates Plant Growth Promotion Induced by Low Doses of Glyphosate
title Root Microbiome Modulates Plant Growth Promotion Induced by Low Doses of Glyphosate
title_full Root Microbiome Modulates Plant Growth Promotion Induced by Low Doses of Glyphosate
title_fullStr Root Microbiome Modulates Plant Growth Promotion Induced by Low Doses of Glyphosate
title_full_unstemmed Root Microbiome Modulates Plant Growth Promotion Induced by Low Doses of Glyphosate
title_short Root Microbiome Modulates Plant Growth Promotion Induced by Low Doses of Glyphosate
title_sort root microbiome modulates plant growth promotion induced by low doses of glyphosate
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7426167/
https://www.ncbi.nlm.nih.gov/pubmed/32817451
http://dx.doi.org/10.1128/mSphere.00484-20
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