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Root Hair Mutations Displace the Barley Rhizosphere Microbiota

The rhizosphere, the thin layer of soil surrounding and influenced by plant roots, defines a distinct and selective microbial habitat compared to unplanted soil. The microbial communities inhabiting the rhizosphere, the rhizosphere microbiota, engage in interactions with their host plants which span...

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Autores principales: Robertson-Albertyn, Senga, Alegria Terrazas, Rodrigo, Balbirnie, Katharin, Blank, Manuel, Janiak, Agnieszka, Szarejko, Iwona, Chmielewska, Beata, Karcz, Jagna, Morris, Jenny, Hedley, Pete E., George, Timothy S., Bulgarelli, Davide
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2017
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5483447/
https://www.ncbi.nlm.nih.gov/pubmed/28694814
http://dx.doi.org/10.3389/fpls.2017.01094
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author Robertson-Albertyn, Senga
Alegria Terrazas, Rodrigo
Balbirnie, Katharin
Blank, Manuel
Janiak, Agnieszka
Szarejko, Iwona
Chmielewska, Beata
Karcz, Jagna
Morris, Jenny
Hedley, Pete E.
George, Timothy S.
Bulgarelli, Davide
author_facet Robertson-Albertyn, Senga
Alegria Terrazas, Rodrigo
Balbirnie, Katharin
Blank, Manuel
Janiak, Agnieszka
Szarejko, Iwona
Chmielewska, Beata
Karcz, Jagna
Morris, Jenny
Hedley, Pete E.
George, Timothy S.
Bulgarelli, Davide
author_sort Robertson-Albertyn, Senga
collection PubMed
description The rhizosphere, the thin layer of soil surrounding and influenced by plant roots, defines a distinct and selective microbial habitat compared to unplanted soil. The microbial communities inhabiting the rhizosphere, the rhizosphere microbiota, engage in interactions with their host plants which span from parasitism to mutualism. Therefore, the rhizosphere microbiota emerges as one of the determinants of yield potential in crops. Studies conducted with different plant species have unequivocally pointed to the host plant as a driver of the microbiota thriving at the root–soil interface. Thus far, the host genetic traits shaping the rhizosphere microbiota are not completely understood. As root hairs play a critical role in resource exchanges between plants and the rhizosphere, we hypothesized that they can act as a determinant of the microbiota thriving at the root–soil interface. To test this hypothesis, we took advantage of barley (Hordeum vulgare) mutant lines contrasting for their root hair characteristics. Plants were grown in two agricultural soils, differentiating in their organic matter contents, under controlled environmental conditions. At early stem elongation rhizosphere specimens were collected and subjected to high-resolution 16S rRNA gene profiling. Our data revealed that the barley rhizosphere microbiota is largely dominated by members of the phyla Bacteroidetes and Proteobacteria, regardless of the soil type and the root hair characteristics of the host plant. Conversely, ecological indices calculated using operational taxonomic units (OTUs) presence, abundance, and phylogeny revealed a significant impact of root hair mutations on the composition of the rhizosphere microbiota. In particular, our data indicate that mutant plants host a reduced-complexity community compared to wild-type genotypes and unplanted soil controls. Congruently, the host genotype explained up to 18% of the variation in ecological distances computed for the rhizosphere samples. Importantly, this effect is manifested in a soil-dependent manner. A closer inspection of the sequencing profiles revealed that the root hair-dependent diversification of the microbiota is supported by a taxonomically narrow group of bacteria, with a bias for members of the orders Actinomycetales, Burkholderiales, Rhizobiales, Sphingomonadales, and Xanthomonadales. Taken together, our results indicate that the presence and function of root hairs are a determinant of the bacterial community thriving in the rhizosphere and their perturbations can markedly impact on the recruitment of individual members of the microbiota.
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spelling pubmed-54834472017-07-10 Root Hair Mutations Displace the Barley Rhizosphere Microbiota Robertson-Albertyn, Senga Alegria Terrazas, Rodrigo Balbirnie, Katharin Blank, Manuel Janiak, Agnieszka Szarejko, Iwona Chmielewska, Beata Karcz, Jagna Morris, Jenny Hedley, Pete E. George, Timothy S. Bulgarelli, Davide Front Plant Sci Plant Science The rhizosphere, the thin layer of soil surrounding and influenced by plant roots, defines a distinct and selective microbial habitat compared to unplanted soil. The microbial communities inhabiting the rhizosphere, the rhizosphere microbiota, engage in interactions with their host plants which span from parasitism to mutualism. Therefore, the rhizosphere microbiota emerges as one of the determinants of yield potential in crops. Studies conducted with different plant species have unequivocally pointed to the host plant as a driver of the microbiota thriving at the root–soil interface. Thus far, the host genetic traits shaping the rhizosphere microbiota are not completely understood. As root hairs play a critical role in resource exchanges between plants and the rhizosphere, we hypothesized that they can act as a determinant of the microbiota thriving at the root–soil interface. To test this hypothesis, we took advantage of barley (Hordeum vulgare) mutant lines contrasting for their root hair characteristics. Plants were grown in two agricultural soils, differentiating in their organic matter contents, under controlled environmental conditions. At early stem elongation rhizosphere specimens were collected and subjected to high-resolution 16S rRNA gene profiling. Our data revealed that the barley rhizosphere microbiota is largely dominated by members of the phyla Bacteroidetes and Proteobacteria, regardless of the soil type and the root hair characteristics of the host plant. Conversely, ecological indices calculated using operational taxonomic units (OTUs) presence, abundance, and phylogeny revealed a significant impact of root hair mutations on the composition of the rhizosphere microbiota. In particular, our data indicate that mutant plants host a reduced-complexity community compared to wild-type genotypes and unplanted soil controls. Congruently, the host genotype explained up to 18% of the variation in ecological distances computed for the rhizosphere samples. Importantly, this effect is manifested in a soil-dependent manner. A closer inspection of the sequencing profiles revealed that the root hair-dependent diversification of the microbiota is supported by a taxonomically narrow group of bacteria, with a bias for members of the orders Actinomycetales, Burkholderiales, Rhizobiales, Sphingomonadales, and Xanthomonadales. Taken together, our results indicate that the presence and function of root hairs are a determinant of the bacterial community thriving in the rhizosphere and their perturbations can markedly impact on the recruitment of individual members of the microbiota. Frontiers Media S.A. 2017-06-26 /pmc/articles/PMC5483447/ /pubmed/28694814 http://dx.doi.org/10.3389/fpls.2017.01094 Text en Copyright © 2017 Robertson-Albertyn, Alegria Terrazas, Balbirnie, Blank, Janiak, Szarejko, Chmielewska, Karcz, Morris, Hedley, George and Bulgarelli. http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Plant Science
Robertson-Albertyn, Senga
Alegria Terrazas, Rodrigo
Balbirnie, Katharin
Blank, Manuel
Janiak, Agnieszka
Szarejko, Iwona
Chmielewska, Beata
Karcz, Jagna
Morris, Jenny
Hedley, Pete E.
George, Timothy S.
Bulgarelli, Davide
Root Hair Mutations Displace the Barley Rhizosphere Microbiota
title Root Hair Mutations Displace the Barley Rhizosphere Microbiota
title_full Root Hair Mutations Displace the Barley Rhizosphere Microbiota
title_fullStr Root Hair Mutations Displace the Barley Rhizosphere Microbiota
title_full_unstemmed Root Hair Mutations Displace the Barley Rhizosphere Microbiota
title_short Root Hair Mutations Displace the Barley Rhizosphere Microbiota
title_sort root hair mutations displace the barley rhizosphere microbiota
topic Plant Science
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5483447/
https://www.ncbi.nlm.nih.gov/pubmed/28694814
http://dx.doi.org/10.3389/fpls.2017.01094
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