Root Hair Mutations Displace the Barley Rhizosphere Microbiota

Senga Robertson-Albertyn, Rodrigo Alegria Terrazas, Katharin Balbirnie, Manuel Blank, Agnieszka Janiak, Iwona Szarejko, Beata Chmielewska, Jagna Karcz, Jenny Morris, Peter E. Hedley, Timothy S. George, Davide Bulgarelli (Lead / Corresponding author)

Research output: Contribution to journalArticle

8 Citations (Scopus)
99 Downloads (Pure)

Abstract

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.
Original languageEnglish
Article number1094
Pages (from-to)1-15
Number of pages15
JournalFrontiers in Plant Science
Volume8
DOIs
Publication statusPublished - 26 Jun 2017

Fingerprint

root hairs
rhizosphere
barley
mutation
host plants
Sphingomonadales
soil
Xanthomonadales
Burkholderiales
microbiome
Rhizobiales
mutants
genetic traits
genotype
mutualism
Proteobacteria
Actinomycetales
stem elongation
agricultural soils
bacterial communities

Keywords

  • rhizosphere
  • microbiota
  • Plant-Microbe Interactions
  • root hairs
  • Barley (Hordeum vulgare L.)

Cite this

Robertson-Albertyn, Senga ; Alegria Terrazas, Rodrigo ; Balbirnie, Katharin ; Blank, Manuel ; Janiak, Agnieszka ; Szarejko, Iwona ; Chmielewska, Beata ; Karcz, Jagna ; Morris, Jenny ; Hedley, Peter E. ; George, Timothy S. ; Bulgarelli, Davide. / Root Hair Mutations Displace the Barley Rhizosphere Microbiota. In: Frontiers in Plant Science. 2017 ; Vol. 8. pp. 1-15.
@article{b135d9c74b4f4b77bf4509e458690fe4,
title = "Root Hair Mutations Displace the Barley Rhizosphere Microbiota",
abstract = "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.",
keywords = "rhizosphere, microbiota, Plant-Microbe Interactions, root hairs, Barley (Hordeum vulgare L.)",
author = "Senga Robertson-Albertyn and {Alegria Terrazas}, Rodrigo and Katharin Balbirnie and Manuel Blank and Agnieszka Janiak and Iwona Szarejko and Beata Chmielewska and Jagna Karcz and Jenny Morris and Hedley, {Peter E.} and George, {Timothy S.} and Davide Bulgarelli",
note = "This work was supported by a Royal Society of Edinburgh/Scottish Government Personal Research Fellowship co-funded by Marie Curie Actions awarded to DB. SRA is supported by a BBSRC iCASE studentship awarded to DB (BB/M016811/1) and partnered by the James Hutton Limited (Invergowrie, UK). RAT is supported by a Scottish Food Security Alliance-Crops studentship, provided by the University of Dundee, the University of Aberdeen, and the James Hutton Institute. James Hutton researchers receive financial support from the Rural and Environment Science and Analytical Service Division of the Scottish Government.",
year = "2017",
month = "6",
day = "26",
doi = "10.3389/fpls.2017.01094",
language = "English",
volume = "8",
pages = "1--15",
journal = "Frontiers in Plant Science",
issn = "1664-462X",
publisher = "Frontiers Media",

}

Robertson-Albertyn, S, Alegria Terrazas, R, Balbirnie, K, Blank, M, Janiak, A, Szarejko, I, Chmielewska, B, Karcz, J, Morris, J, Hedley, PE, George, TS & Bulgarelli, D 2017, 'Root Hair Mutations Displace the Barley Rhizosphere Microbiota', Frontiers in Plant Science, vol. 8, 1094, pp. 1-15. https://doi.org/10.3389/fpls.2017.01094

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, Peter E.; George, Timothy S.; Bulgarelli, Davide (Lead / Corresponding author).

In: Frontiers in Plant Science, Vol. 8, 1094, 26.06.2017, p. 1-15.

Research output: Contribution to journalArticle

TY - JOUR

T1 - Root Hair Mutations Displace the Barley Rhizosphere Microbiota

AU - Robertson-Albertyn, Senga

AU - Alegria Terrazas, Rodrigo

AU - Balbirnie, Katharin

AU - Blank, Manuel

AU - Janiak, Agnieszka

AU - Szarejko, Iwona

AU - Chmielewska, Beata

AU - Karcz, Jagna

AU - Morris, Jenny

AU - Hedley, Peter E.

AU - George, Timothy S.

AU - Bulgarelli, Davide

N1 - This work was supported by a Royal Society of Edinburgh/Scottish Government Personal Research Fellowship co-funded by Marie Curie Actions awarded to DB. SRA is supported by a BBSRC iCASE studentship awarded to DB (BB/M016811/1) and partnered by the James Hutton Limited (Invergowrie, UK). RAT is supported by a Scottish Food Security Alliance-Crops studentship, provided by the University of Dundee, the University of Aberdeen, and the James Hutton Institute. James Hutton researchers receive financial support from the Rural and Environment Science and Analytical Service Division of the Scottish Government.

PY - 2017/6/26

Y1 - 2017/6/26

N2 - 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.

AB - 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.

KW - rhizosphere

KW - microbiota

KW - Plant-Microbe Interactions

KW - root hairs

KW - Barley (Hordeum vulgare L.)

U2 - 10.3389/fpls.2017.01094

DO - 10.3389/fpls.2017.01094

M3 - Article

VL - 8

SP - 1

EP - 15

JO - Frontiers in Plant Science

JF - Frontiers in Plant Science

SN - 1664-462X

M1 - 1094

ER -

Robertson-Albertyn S, Alegria Terrazas R, Balbirnie K, Blank M, Janiak A, Szarejko I et al. Root Hair Mutations Displace the Barley Rhizosphere Microbiota. Frontiers in Plant Science. 2017 Jun 26;8:1-15. 1094. https://doi.org/10.3389/fpls.2017.01094