Flooding Causes Dramatic Compositional Shifts and Depletion of Putative Beneficial Bacteria on the Spring Wheat Microbiota

Flooding affects both above- and below-ground ecosystem processes, and it represents a substantial threat for crop and cereal productivity under climate change. Plant-associated microbiota play a crucial role in plant growth and fitness, but we still have a limited understanding of the response of t...

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Autores principales:	Davide Francioli, Geeisy Cid, Saranya Kanukollu, Andreas Ulrich, Mohammad-Reza Hajirezaei, Steffen Kolb
Formato:	article
Lenguaje:	EN
Publicado:	Frontiers Media S.A. 2021
Materias:	plant-microbe interactions flooding metabarcoding bacteria spring wheat plant traits Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/f0da461aaa3a424e9f83de5ca4ee3508
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spelling	oai:doaj.org-article:f0da461aaa3a424e9f83de5ca4ee35082021-11-05T06:55:46ZFlooding Causes Dramatic Compositional Shifts and Depletion of Putative Beneficial Bacteria on the Spring Wheat Microbiota1664-302X10.3389/fmicb.2021.773116https://doaj.org/article/f0da461aaa3a424e9f83de5ca4ee35082021-11-01T00:00:00Zhttps://www.frontiersin.org/articles/10.3389/fmicb.2021.773116/fullhttps://doaj.org/toc/1664-302XFlooding affects both above- and below-ground ecosystem processes, and it represents a substantial threat for crop and cereal productivity under climate change. Plant-associated microbiota play a crucial role in plant growth and fitness, but we still have a limited understanding of the response of the crop-microbiota complex under extreme weather events, such as flooding. Soil microbes are highly sensitive to abiotic disturbance, and shifts in microbial community composition, structure and functions are expected when soil conditions are altered due to flooding events (e.g., anoxia, pH alteration, changes in nutrient concentration). Here, we established a pot experiment to determine the effects of flooding stress on the spring wheat-microbiota complex. Since plant phenology could be an important factor in the response to hydrological stress, flooding was induced only once and at different plant growth stages (PGSs), such as tillering, booting and flowering. After each flooding event, we measured in the control and flooded pots several edaphic and plant properties and characterized the bacterial community associated to the rhizosphere and roots of wheat plant using a metabarcoding approach. In our study, flooding caused a significant reduction in plant development and we observed dramatic shifts in bacterial community composition at each PGS in which the hydrological stress was induced. However, a more pronounced disruption in community assembly was always shown in younger plants. Generally, flooding caused a (i) significant increase of bacterial taxa with anaerobic respiratory capabilities, such as members of Firmicutes and Desulfobacterota, (ii) a significant reduction in Actinobacteria and Proteobacteria, (iii) depletion of several putative plant-beneficial taxa, and (iv) increases of the abundance of potential detrimental bacteria. These significant differences in community composition between flooded and control samples were correlated with changes in soil conditions and plant properties caused by the hydrological stress, with pH and total N as the soil, and S, Na, Mn, and Ca concentrations as the root properties most influencing microbial assemblage in the wheat mircobiota under flooding stress. Collectively, our findings demonstrated the role of flooding on restructuring the spring wheat microbiota, and highlighted the detrimental effect of this hydrological stress on plant fitness and performance.Davide FrancioliGeeisy CidSaranya KanukolluAndreas UlrichMohammad-Reza HajirezaeiSteffen KolbSteffen KolbFrontiers Media S.A.articleplant-microbe interactionsfloodingmetabarcodingbacteriaspring wheatplant traitsMicrobiologyQR1-502ENFrontiers in Microbiology, Vol 12 (2021)
institution	DOAJ
collection	DOAJ
language	EN
topic	plant-microbe interactions flooding metabarcoding bacteria spring wheat plant traits Microbiology QR1-502
spellingShingle	plant-microbe interactions flooding metabarcoding bacteria spring wheat plant traits Microbiology QR1-502 Davide Francioli Geeisy Cid Saranya Kanukollu Andreas Ulrich Mohammad-Reza Hajirezaei Steffen Kolb Steffen Kolb Flooding Causes Dramatic Compositional Shifts and Depletion of Putative Beneficial Bacteria on the Spring Wheat Microbiota
description	Flooding affects both above- and below-ground ecosystem processes, and it represents a substantial threat for crop and cereal productivity under climate change. Plant-associated microbiota play a crucial role in plant growth and fitness, but we still have a limited understanding of the response of the crop-microbiota complex under extreme weather events, such as flooding. Soil microbes are highly sensitive to abiotic disturbance, and shifts in microbial community composition, structure and functions are expected when soil conditions are altered due to flooding events (e.g., anoxia, pH alteration, changes in nutrient concentration). Here, we established a pot experiment to determine the effects of flooding stress on the spring wheat-microbiota complex. Since plant phenology could be an important factor in the response to hydrological stress, flooding was induced only once and at different plant growth stages (PGSs), such as tillering, booting and flowering. After each flooding event, we measured in the control and flooded pots several edaphic and plant properties and characterized the bacterial community associated to the rhizosphere and roots of wheat plant using a metabarcoding approach. In our study, flooding caused a significant reduction in plant development and we observed dramatic shifts in bacterial community composition at each PGS in which the hydrological stress was induced. However, a more pronounced disruption in community assembly was always shown in younger plants. Generally, flooding caused a (i) significant increase of bacterial taxa with anaerobic respiratory capabilities, such as members of Firmicutes and Desulfobacterota, (ii) a significant reduction in Actinobacteria and Proteobacteria, (iii) depletion of several putative plant-beneficial taxa, and (iv) increases of the abundance of potential detrimental bacteria. These significant differences in community composition between flooded and control samples were correlated with changes in soil conditions and plant properties caused by the hydrological stress, with pH and total N as the soil, and S, Na, Mn, and Ca concentrations as the root properties most influencing microbial assemblage in the wheat mircobiota under flooding stress. Collectively, our findings demonstrated the role of flooding on restructuring the spring wheat microbiota, and highlighted the detrimental effect of this hydrological stress on plant fitness and performance.
format	article
author	Davide Francioli Geeisy Cid Saranya Kanukollu Andreas Ulrich Mohammad-Reza Hajirezaei Steffen Kolb Steffen Kolb
author_facet	Davide Francioli Geeisy Cid Saranya Kanukollu Andreas Ulrich Mohammad-Reza Hajirezaei Steffen Kolb Steffen Kolb
author_sort	Davide Francioli
title	Flooding Causes Dramatic Compositional Shifts and Depletion of Putative Beneficial Bacteria on the Spring Wheat Microbiota
title_short	Flooding Causes Dramatic Compositional Shifts and Depletion of Putative Beneficial Bacteria on the Spring Wheat Microbiota
title_full	Flooding Causes Dramatic Compositional Shifts and Depletion of Putative Beneficial Bacteria on the Spring Wheat Microbiota
title_fullStr	Flooding Causes Dramatic Compositional Shifts and Depletion of Putative Beneficial Bacteria on the Spring Wheat Microbiota
title_full_unstemmed	Flooding Causes Dramatic Compositional Shifts and Depletion of Putative Beneficial Bacteria on the Spring Wheat Microbiota
title_sort	flooding causes dramatic compositional shifts and depletion of putative beneficial bacteria on the spring wheat microbiota
publisher	Frontiers Media S.A.
publishDate	2021
url	https://doaj.org/article/f0da461aaa3a424e9f83de5ca4ee3508
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Flooding Causes Dramatic Compositional Shifts and Depletion of Putative Beneficial Bacteria on the Spring Wheat Microbiota

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