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The Sorghum bicolor Root Exudate Sorgoleone Shapes Bacterial Communities and Delays Network Formation

Primary and secondary metabolites exuded from roots are key drivers of root-soil microbe interactions that contribute to the structure and function of microbial communities. Studies with model plants have begun to reveal the complex interactions between root exudates and soil microbes, but little is...

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Autores principales: Wang, Peng, Chai, Yen Ning, Roston, Rebecca, Dayan, Franck E., Schachtman, Daniel P.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: American Society for Microbiology 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8546980/
https://www.ncbi.nlm.nih.gov/pubmed/33727394
http://dx.doi.org/10.1128/mSystems.00749-20
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author Wang, Peng
Chai, Yen Ning
Roston, Rebecca
Dayan, Franck E.
Schachtman, Daniel P.
author_facet Wang, Peng
Chai, Yen Ning
Roston, Rebecca
Dayan, Franck E.
Schachtman, Daniel P.
author_sort Wang, Peng
collection PubMed
description Primary and secondary metabolites exuded from roots are key drivers of root-soil microbe interactions that contribute to the structure and function of microbial communities. Studies with model plants have begun to reveal the complex interactions between root exudates and soil microbes, but little is known about the influence of specialized exudates from crop plants. The aims of this work were to understand whether sorgoleone, a unique lipophilic secondary benzoquinone exuded only from the root hairs of sorghum, influences belowground microbial community structure in the field, to assess the effect of purified sorgoleone on the cultured bacteria from field soils, and to determine whether sorgoleone inhibits nitrification under field conditions. Studies were conducted comparing wild-type sorghum and lines with genetically reduced sorgoleone exudation. In the soil near roots and rhizosphere, sorgoleone influenced microbial community structure as measured by β-diversity and network analysis. Under greenhouse conditions, the soil nitrogen content was an important factor in determining the impacts of sorgoleone. Sorgoleone delayed the formation of the bacterial and archaeal networks early in plant development and only inhibited nitrification at specific sampling times under field conditions. Sorgoleone was also shown to both inhibit and promote cultured bacterial isolate growth in laboratory tests. These findings provide new insights into the role of secondary metabolites in shaping the composition and function of the sorghum root-associated bacterial microbiomes. Understanding how root exudates modify soil microbiomes may potentially unlock an important tool for enhancing crop sustainability and yield in our changing environment. IMPORTANCE Plant roots exude a complex mixture of metabolites into the rhizosphere. Primary and secondary metabolites exuded from roots are key drivers of root-soil microbe interactions that contribute to the structure and function of microbial communities in agricultural and natural ecosystems. Previous work on plant root exudates and their influence on soil microbes has mainly been restricted to model plant species. Plant are a diverse group of organisms and produce a wide array of different secondary metabolites. Therefore, it is important to go beyond studies of model plants to fully understand the diverse repertoire of root exudates in crop plant species that feed human populations. Extending studies to a wider array of root exudates will provide a more comprehensive understanding of how the roots of important food crops interact with highly diverse soil microbial communities. This will provide information that could lead to tailoring root exudates for the development of more beneficial plant-soil microbe interactions that will benefit agroecosystem productivity.
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spelling pubmed-85469802021-10-27 The Sorghum bicolor Root Exudate Sorgoleone Shapes Bacterial Communities and Delays Network Formation Wang, Peng Chai, Yen Ning Roston, Rebecca Dayan, Franck E. Schachtman, Daniel P. mSystems Research Article Primary and secondary metabolites exuded from roots are key drivers of root-soil microbe interactions that contribute to the structure and function of microbial communities. Studies with model plants have begun to reveal the complex interactions between root exudates and soil microbes, but little is known about the influence of specialized exudates from crop plants. The aims of this work were to understand whether sorgoleone, a unique lipophilic secondary benzoquinone exuded only from the root hairs of sorghum, influences belowground microbial community structure in the field, to assess the effect of purified sorgoleone on the cultured bacteria from field soils, and to determine whether sorgoleone inhibits nitrification under field conditions. Studies were conducted comparing wild-type sorghum and lines with genetically reduced sorgoleone exudation. In the soil near roots and rhizosphere, sorgoleone influenced microbial community structure as measured by β-diversity and network analysis. Under greenhouse conditions, the soil nitrogen content was an important factor in determining the impacts of sorgoleone. Sorgoleone delayed the formation of the bacterial and archaeal networks early in plant development and only inhibited nitrification at specific sampling times under field conditions. Sorgoleone was also shown to both inhibit and promote cultured bacterial isolate growth in laboratory tests. These findings provide new insights into the role of secondary metabolites in shaping the composition and function of the sorghum root-associated bacterial microbiomes. Understanding how root exudates modify soil microbiomes may potentially unlock an important tool for enhancing crop sustainability and yield in our changing environment. IMPORTANCE Plant roots exude a complex mixture of metabolites into the rhizosphere. Primary and secondary metabolites exuded from roots are key drivers of root-soil microbe interactions that contribute to the structure and function of microbial communities in agricultural and natural ecosystems. Previous work on plant root exudates and their influence on soil microbes has mainly been restricted to model plant species. Plant are a diverse group of organisms and produce a wide array of different secondary metabolites. Therefore, it is important to go beyond studies of model plants to fully understand the diverse repertoire of root exudates in crop plant species that feed human populations. Extending studies to a wider array of root exudates will provide a more comprehensive understanding of how the roots of important food crops interact with highly diverse soil microbial communities. This will provide information that could lead to tailoring root exudates for the development of more beneficial plant-soil microbe interactions that will benefit agroecosystem productivity. American Society for Microbiology 2021-03-16 /pmc/articles/PMC8546980/ /pubmed/33727394 http://dx.doi.org/10.1128/mSystems.00749-20 Text en Copyright © 2021 Wang 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
Wang, Peng
Chai, Yen Ning
Roston, Rebecca
Dayan, Franck E.
Schachtman, Daniel P.
The Sorghum bicolor Root Exudate Sorgoleone Shapes Bacterial Communities and Delays Network Formation
title The Sorghum bicolor Root Exudate Sorgoleone Shapes Bacterial Communities and Delays Network Formation
title_full The Sorghum bicolor Root Exudate Sorgoleone Shapes Bacterial Communities and Delays Network Formation
title_fullStr The Sorghum bicolor Root Exudate Sorgoleone Shapes Bacterial Communities and Delays Network Formation
title_full_unstemmed The Sorghum bicolor Root Exudate Sorgoleone Shapes Bacterial Communities and Delays Network Formation
title_short The Sorghum bicolor Root Exudate Sorgoleone Shapes Bacterial Communities and Delays Network Formation
title_sort sorghum bicolor root exudate sorgoleone shapes bacterial communities and delays network formation
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8546980/
https://www.ncbi.nlm.nih.gov/pubmed/33727394
http://dx.doi.org/10.1128/mSystems.00749-20
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