Abiotic Stress Reorganizes Rhizosphere and Endosphere Network Structure of Sorghum bicolor

Sorghum bicolor is a promising bioenergy feedstock with high biomass production and unusual tolerance for stresses, such as water and nutrient limitation. Although the membership of the sorghum microbiome in response to stress has been explored, relatively little is known about how microbe–microbe n...

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Main Authors: Elle M. Barnes, Kyle Hartman, Dawn Chiniquy, Wenting Zhao, Peng Liu, Cody Creech, Daniel P. Schachtman, Susannah G. Tringe
Format: Article
Language:English
Published: The American Phytopathological Society 2024-11-01
Series:Phytobiomes Journal
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Online Access:https://apsjournals.apsnet.org/doi/10.1094/PBIOMES-02-24-0012-R
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author Elle M. Barnes
Kyle Hartman
Dawn Chiniquy
Wenting Zhao
Peng Liu
Cody Creech
Daniel P. Schachtman
Susannah G. Tringe
author_facet Elle M. Barnes
Kyle Hartman
Dawn Chiniquy
Wenting Zhao
Peng Liu
Cody Creech
Daniel P. Schachtman
Susannah G. Tringe
author_sort Elle M. Barnes
collection DOAJ
description Sorghum bicolor is a promising bioenergy feedstock with high biomass production and unusual tolerance for stresses, such as water and nutrient limitation. Although the membership of the sorghum microbiome in response to stress has been explored, relatively little is known about how microbe–microbe networks change under water- or nutrient-limited conditions. This is important because network changes can indicate impacts on the functionality and stability of microbial communities. We performed network-based analysis on the core bacterial and archaeal community of an agronomically promising high biomass bioenergy genotype, Grassl, grown under nitrogen and water stress. Stress caused relatively minor changes in bacterial abundances within soil, rhizosphere, and endosphere communities but led to significant changes in bacterial network structure and modularity. We found a complete reorganization of network roles in all plant compartments, as well as an increase in the modularity and proportion of positive associations, which potentially could represent coexistence and cooperation in the sorghum bacterial/archaeal community under stress. Although stressors are often believed to be destabilizing, we found stressed networks were as or more stable than non-stressed networks, likely due to their redundancy and compartmentalization. Together, these findings support the idea that both sorghum and its bacterial/archaeal community can be resilient to future environmental stressors. [Figure: see text] Copyright © 2024 The Author(s). This is an open access article distributed under the CC BY 4.0 International license.
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spelling doaj-art-4f3c1003bd9f44bb884b9d758caf0a9d2024-11-23T17:01:49ZengThe American Phytopathological SocietyPhytobiomes Journal2471-29062024-11-018449951110.1094/PBIOMES-02-24-0012-RAbiotic Stress Reorganizes Rhizosphere and Endosphere Network Structure of Sorghum bicolorElle M. Barnes0Kyle Hartman1Dawn Chiniquy2Wenting Zhao3Peng Liu4Cody Creech5Daniel P. Schachtman6Susannah G. Tringe7Department of Energy Joint Genome Institute, Lawrence Berkeley National Laboratory, Berkeley, CADepartment of Energy Joint Genome Institute, Lawrence Berkeley National Laboratory, Berkeley, CAEnvironmental Genomics and Systems Biology Division, Lawrence Berkeley National Laboratory, Berkeley, CADepartment of Statistics, Iowa State University, Ames, IADepartment of Statistics, Iowa State University, Ames, IADepartment of Agronomy and Horticulture and Center for Plant Science Innovation, University of Nebraska-Lincoln, Lincoln, NEDepartment of Agronomy and Horticulture and Center for Plant Science Innovation, University of Nebraska-Lincoln, Lincoln, NEDepartment of Energy Joint Genome Institute, Lawrence Berkeley National Laboratory, Berkeley, CASorghum bicolor is a promising bioenergy feedstock with high biomass production and unusual tolerance for stresses, such as water and nutrient limitation. Although the membership of the sorghum microbiome in response to stress has been explored, relatively little is known about how microbe–microbe networks change under water- or nutrient-limited conditions. This is important because network changes can indicate impacts on the functionality and stability of microbial communities. We performed network-based analysis on the core bacterial and archaeal community of an agronomically promising high biomass bioenergy genotype, Grassl, grown under nitrogen and water stress. Stress caused relatively minor changes in bacterial abundances within soil, rhizosphere, and endosphere communities but led to significant changes in bacterial network structure and modularity. We found a complete reorganization of network roles in all plant compartments, as well as an increase in the modularity and proportion of positive associations, which potentially could represent coexistence and cooperation in the sorghum bacterial/archaeal community under stress. Although stressors are often believed to be destabilizing, we found stressed networks were as or more stable than non-stressed networks, likely due to their redundancy and compartmentalization. Together, these findings support the idea that both sorghum and its bacterial/archaeal community can be resilient to future environmental stressors. [Figure: see text] Copyright © 2024 The Author(s). This is an open access article distributed under the CC BY 4.0 International license.https://apsjournals.apsnet.org/doi/10.1094/PBIOMES-02-24-0012-Rabiotic stressbioenergydroughtmicrobe–microbe associationsnitrogen limitationplant microbiome
spellingShingle Elle M. Barnes
Kyle Hartman
Dawn Chiniquy
Wenting Zhao
Peng Liu
Cody Creech
Daniel P. Schachtman
Susannah G. Tringe
Abiotic Stress Reorganizes Rhizosphere and Endosphere Network Structure of Sorghum bicolor
Phytobiomes Journal
abiotic stress
bioenergy
drought
microbe–microbe associations
nitrogen limitation
plant microbiome
title Abiotic Stress Reorganizes Rhizosphere and Endosphere Network Structure of Sorghum bicolor
title_full Abiotic Stress Reorganizes Rhizosphere and Endosphere Network Structure of Sorghum bicolor
title_fullStr Abiotic Stress Reorganizes Rhizosphere and Endosphere Network Structure of Sorghum bicolor
title_full_unstemmed Abiotic Stress Reorganizes Rhizosphere and Endosphere Network Structure of Sorghum bicolor
title_short Abiotic Stress Reorganizes Rhizosphere and Endosphere Network Structure of Sorghum bicolor
title_sort abiotic stress reorganizes rhizosphere and endosphere network structure of sorghum bicolor
topic abiotic stress
bioenergy
drought
microbe–microbe associations
nitrogen limitation
plant microbiome
url https://apsjournals.apsnet.org/doi/10.1094/PBIOMES-02-24-0012-R
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