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Spike Formation Is a Turning Point Determining Wheat Root Microbiome Abundance, Structures and Functions

Root selection of their associated microbiome composition and activities is determined by the plant’s developmental stage and distance from the root. Total gene abundance, structure and functions of root-associated and rhizospheric microbiomes were studied throughout wheat growth season under field...

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Autores principales: Usyskin-Tonne, Alla, Hadar, Yitzhak, Minz, Dror
Formato: Online Artículo Texto
Lenguaje:English
Publicado: MDPI 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8585012/
https://www.ncbi.nlm.nih.gov/pubmed/34769377
http://dx.doi.org/10.3390/ijms222111948
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author Usyskin-Tonne, Alla
Hadar, Yitzhak
Minz, Dror
author_facet Usyskin-Tonne, Alla
Hadar, Yitzhak
Minz, Dror
author_sort Usyskin-Tonne, Alla
collection PubMed
description Root selection of their associated microbiome composition and activities is determined by the plant’s developmental stage and distance from the root. Total gene abundance, structure and functions of root-associated and rhizospheric microbiomes were studied throughout wheat growth season under field conditions. On the root surface, abundance of the well-known wheat colonizers Proteobacteria and Actinobacteria decreased and increased, respectively, during spike formation, whereas abundance of Bacteroidetes was independent of spike formation. Metagenomic analysis combined with functional co-occurrence networks revealed a significant impact of plant developmental stage on its microbiome during the transition from vegetative growth to spike formation. For example, gene functions related to biofilm and sensorial movement, antibiotic production and resistance and carbons and amino acids and their transporters. Genes associated with these functions were also in higher abundance in root vs. the rhizosphere microbiome. We propose that abundance of transporter-encoding genes related to carbon and amino acid, may mirror the availability and utilization of root exudates. Genes related to antibiotic resistance mechanisms were abundant during vegetative growth, while after spike formation, genes related to the biosynthesis of various antibiotics were enriched. This observation suggests that during root colonization and biofilm formation, bacteria cope with competitor’s antibiotics, whereas in the mature biofilm stage, they invest in inhibiting new colonizers. Additionally, there is higher abundance of genes related to denitrification in rhizosphere compared to root-associated microbiome during wheat growth, possibly due to competition with the plant over nitrogen in the root vicinity. We demonstrated functional and phylogenetic division in wheat root zone microbiome in both time and space: pre- and post-spike formation, and root-associated vs. rhizospheric niches. These findings shed light on the dynamics of plant–microbe and microbe–microbe interactions in the developing root zone.
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spelling pubmed-85850122021-11-12 Spike Formation Is a Turning Point Determining Wheat Root Microbiome Abundance, Structures and Functions Usyskin-Tonne, Alla Hadar, Yitzhak Minz, Dror Int J Mol Sci Article Root selection of their associated microbiome composition and activities is determined by the plant’s developmental stage and distance from the root. Total gene abundance, structure and functions of root-associated and rhizospheric microbiomes were studied throughout wheat growth season under field conditions. On the root surface, abundance of the well-known wheat colonizers Proteobacteria and Actinobacteria decreased and increased, respectively, during spike formation, whereas abundance of Bacteroidetes was independent of spike formation. Metagenomic analysis combined with functional co-occurrence networks revealed a significant impact of plant developmental stage on its microbiome during the transition from vegetative growth to spike formation. For example, gene functions related to biofilm and sensorial movement, antibiotic production and resistance and carbons and amino acids and their transporters. Genes associated with these functions were also in higher abundance in root vs. the rhizosphere microbiome. We propose that abundance of transporter-encoding genes related to carbon and amino acid, may mirror the availability and utilization of root exudates. Genes related to antibiotic resistance mechanisms were abundant during vegetative growth, while after spike formation, genes related to the biosynthesis of various antibiotics were enriched. This observation suggests that during root colonization and biofilm formation, bacteria cope with competitor’s antibiotics, whereas in the mature biofilm stage, they invest in inhibiting new colonizers. Additionally, there is higher abundance of genes related to denitrification in rhizosphere compared to root-associated microbiome during wheat growth, possibly due to competition with the plant over nitrogen in the root vicinity. We demonstrated functional and phylogenetic division in wheat root zone microbiome in both time and space: pre- and post-spike formation, and root-associated vs. rhizospheric niches. These findings shed light on the dynamics of plant–microbe and microbe–microbe interactions in the developing root zone. MDPI 2021-11-04 /pmc/articles/PMC8585012/ /pubmed/34769377 http://dx.doi.org/10.3390/ijms222111948 Text en © 2021 by the authors. https://creativecommons.org/licenses/by/4.0/Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
spellingShingle Article
Usyskin-Tonne, Alla
Hadar, Yitzhak
Minz, Dror
Spike Formation Is a Turning Point Determining Wheat Root Microbiome Abundance, Structures and Functions
title Spike Formation Is a Turning Point Determining Wheat Root Microbiome Abundance, Structures and Functions
title_full Spike Formation Is a Turning Point Determining Wheat Root Microbiome Abundance, Structures and Functions
title_fullStr Spike Formation Is a Turning Point Determining Wheat Root Microbiome Abundance, Structures and Functions
title_full_unstemmed Spike Formation Is a Turning Point Determining Wheat Root Microbiome Abundance, Structures and Functions
title_short Spike Formation Is a Turning Point Determining Wheat Root Microbiome Abundance, Structures and Functions
title_sort spike formation is a turning point determining wheat root microbiome abundance, structures and functions
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8585012/
https://www.ncbi.nlm.nih.gov/pubmed/34769377
http://dx.doi.org/10.3390/ijms222111948
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