Identifying plant genes shaping microbiota composition in the barley rhizosphere

Carmen Escudero-Martinez; Max Coulter; Rodrigo Alegria Terrazas; Alexandre Foito; Rumana Kapadia; Laura Pietrangelo; Mauro Maver; Rajiv Sharma; Alessio Aprile; Jenny A. Morris; Pete E. Hedley; Andreas Maurer; Klaus Pillen; Gino Naclerio; Tanja  Mimmo; Geoffrey J. Barton; Robbie Waugh; James Abbott; Davide Bulgarelli

doi:10.1038/s41467-022-31022-y

Identifying plant genes shaping microbiota composition in the barley rhizosphere

Carmen Escudero-Martinez, Max Coulter, Rodrigo Alegria Terrazas, Alexandre Foito, Rumana Kapadia, Laura Pietrangelo, Mauro Maver, Rajiv Sharma, Alessio Aprile, Jenny A. Morris, Pete E. Hedley, Andreas Maurer, Klaus Pillen, Gino Naclerio, Tanja Mimmo, Geoffrey J. Barton, Robbie Waugh, James Abbott, Davide Bulgarelli (Lead / Corresponding author)

Research output: Contribution to journal › Article › peer-review

54 Citations (Scopus)

117 Downloads (Pure)

Abstract

A prerequisite to exploiting soil microbes for sustainable crop production is the identification of the plant genes shaping microbiota composition in the rhizosphere, the interface between roots and soil. Here we use metagenomics information as an external quantitative phenotype to map the host genetic determinants of the rhizosphere microbiota in wild and domesticated genotypes of barley, the fourth most cultivated cereal globally. We identify a small number of loci with a major effect on the composition of rhizosphere communities. One of those, designated the QRMC-3HS, emerges as a major determinant of microbiota composition. We subject soil-grown sibling lines harbouring contrasting alleles at QRMC-3HS and hosting contrasting microbiotas to comparative root RNA-seq profiling. This allows us to identify three primary candidate genes, including a Nucleotide-Binding-Leucine-Rich-Repeat (NLR) gene in a region of structural variation of the barley genome. Our results provide insights into the footprint of crop improvement on the plants capacity of shaping rhizosphere microbes.

Original language	English
Article number	3443
Number of pages	14
Journal	Nature Communications
Volume	13
DOIs	https://doi.org/10.1038/s41467-022-31022-y
Publication status	Published - 16 Jun 2022

Keywords

Agricultural genetics
Microbiome
Plant domestication

ASJC Scopus subject areas

General Physics and Astronomy
General Chemistry
General Biochemistry,Genetics and Molecular Biology

Access to Document

10.1038/s41467-022-31022-yLicence: CC BY

Final Published VersionFinal published version, 1.84 MBLicence: CC BY

Cite this

Escudero-Martinez, C., Coulter, M., Alegria Terrazas, R., Foito, A., Kapadia, R., Pietrangelo, L., Maver, M., Sharma, R., Aprile, A., Morris, J. A., Hedley, P. E., Maurer, A., Pillen, K., Naclerio, G., Mimmo, T., Barton, G. J., Waugh, R., Abbott, J., & Bulgarelli, D. (2022). Identifying plant genes shaping microbiota composition in the barley rhizosphere. Nature Communications, 13, Article 3443 . https://doi.org/10.1038/s41467-022-31022-y

@article{2de454690006479484ad832e700aa084,

title = "Identifying plant genes shaping microbiota composition in the barley rhizosphere",

abstract = "A prerequisite to exploiting soil microbes for sustainable crop production is the identification of the plant genes shaping microbiota composition in the rhizosphere, the interface between roots and soil. Here we use metagenomics information as an external quantitative phenotype to map the host genetic determinants of the rhizosphere microbiota in wild and domesticated genotypes of barley, the fourth most cultivated cereal globally. We identify a small number of loci with a major effect on the composition of rhizosphere communities. One of those, designated the QRMC-3HS, emerges as a major determinant of microbiota composition. We subject soil-grown sibling lines harbouring contrasting alleles at QRMC-3HS and hosting contrasting microbiotas to comparative root RNA-seq profiling. This allows us to identify three primary candidate genes, including a Nucleotide-Binding-Leucine-Rich-Repeat (NLR) gene in a region of structural variation of the barley genome. Our results provide insights into the footprint of crop improvement on the plants capacity of shaping rhizosphere microbes.",

keywords = "Agricultural genetics, Microbiome, Plant domestication",

author = "Carmen Escudero-Martinez and Max Coulter and {Alegria Terrazas}, Rodrigo and Alexandre Foito and Rumana Kapadia and Laura Pietrangelo and Mauro Maver and Rajiv Sharma and Alessio Aprile and Morris, {Jenny A.} and Hedley, {Pete E.} and Andreas Maurer and Klaus Pillen and Gino Naclerio and Tanja Mimmo and Barton, {Geoffrey J.} and Robbie Waugh and James Abbott and Davide Bulgarelli",

note = "Funding Information: We thank Malcolm Macaulay and Jim Wilde (The James Hutton Institute, Invergowrie, UK) for the technical assistance during the execution of the experiments. We also thank Nils Stein and Mary Ziems (IPK, Gatersleben, Germany) who kindly provided us with seeds of the barley pan-genome collection. In addition, we thank Malcolm Macaulay and Luke Ramsay (The James Hutton Institute, Invergowrie, UK) who provided access to the diagnostic technology for Btr genes. This work was supported by a Royal Society of Edinburgh Personal Research Fellowship to D.B. and an UKRI grant (BB/S002871/1) to D.B., G.B. and R.W. Publisher Copyright: {\textcopyright} 2022, The Author(s).",

year = "2022",

month = jun,

day = "16",

doi = "10.1038/s41467-022-31022-y",

language = "English",

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Escudero-Martinez, C, Coulter, M, Alegria Terrazas, R, Foito, A, Kapadia, R, Pietrangelo, L, Maver, M, Sharma, R, Aprile, A, Morris, JA, Hedley, PE, Maurer, A, Pillen, K, Naclerio, G, Mimmo, T, Barton, GJ , Waugh, R , Abbott, J & Bulgarelli, D 2022, 'Identifying plant genes shaping microbiota composition in the barley rhizosphere', Nature Communications, vol. 13, 3443 . https://doi.org/10.1038/s41467-022-31022-y

TY - JOUR

T1 - Identifying plant genes shaping microbiota composition in the barley rhizosphere

AU - Escudero-Martinez, Carmen

AU - Coulter, Max

AU - Alegria Terrazas, Rodrigo

AU - Foito, Alexandre

AU - Kapadia, Rumana

AU - Pietrangelo, Laura

AU - Maver, Mauro

AU - Sharma, Rajiv

AU - Aprile, Alessio

AU - Morris, Jenny A.

AU - Hedley, Pete E.

AU - Maurer, Andreas

AU - Pillen, Klaus

AU - Naclerio, Gino

AU - Mimmo, Tanja

AU - Barton, Geoffrey J.

AU - Waugh, Robbie

AU - Abbott, James

AU - Bulgarelli, Davide

N1 - Funding Information: We thank Malcolm Macaulay and Jim Wilde (The James Hutton Institute, Invergowrie, UK) for the technical assistance during the execution of the experiments. We also thank Nils Stein and Mary Ziems (IPK, Gatersleben, Germany) who kindly provided us with seeds of the barley pan-genome collection. In addition, we thank Malcolm Macaulay and Luke Ramsay (The James Hutton Institute, Invergowrie, UK) who provided access to the diagnostic technology for Btr genes. This work was supported by a Royal Society of Edinburgh Personal Research Fellowship to D.B. and an UKRI grant (BB/S002871/1) to D.B., G.B. and R.W. Publisher Copyright: © 2022, The Author(s).

PY - 2022/6/16

Y1 - 2022/6/16

N2 - A prerequisite to exploiting soil microbes for sustainable crop production is the identification of the plant genes shaping microbiota composition in the rhizosphere, the interface between roots and soil. Here we use metagenomics information as an external quantitative phenotype to map the host genetic determinants of the rhizosphere microbiota in wild and domesticated genotypes of barley, the fourth most cultivated cereal globally. We identify a small number of loci with a major effect on the composition of rhizosphere communities. One of those, designated the QRMC-3HS, emerges as a major determinant of microbiota composition. We subject soil-grown sibling lines harbouring contrasting alleles at QRMC-3HS and hosting contrasting microbiotas to comparative root RNA-seq profiling. This allows us to identify three primary candidate genes, including a Nucleotide-Binding-Leucine-Rich-Repeat (NLR) gene in a region of structural variation of the barley genome. Our results provide insights into the footprint of crop improvement on the plants capacity of shaping rhizosphere microbes.

AB - A prerequisite to exploiting soil microbes for sustainable crop production is the identification of the plant genes shaping microbiota composition in the rhizosphere, the interface between roots and soil. Here we use metagenomics information as an external quantitative phenotype to map the host genetic determinants of the rhizosphere microbiota in wild and domesticated genotypes of barley, the fourth most cultivated cereal globally. We identify a small number of loci with a major effect on the composition of rhizosphere communities. One of those, designated the QRMC-3HS, emerges as a major determinant of microbiota composition. We subject soil-grown sibling lines harbouring contrasting alleles at QRMC-3HS and hosting contrasting microbiotas to comparative root RNA-seq profiling. This allows us to identify three primary candidate genes, including a Nucleotide-Binding-Leucine-Rich-Repeat (NLR) gene in a region of structural variation of the barley genome. Our results provide insights into the footprint of crop improvement on the plants capacity of shaping rhizosphere microbes.

KW - Agricultural genetics

KW - Microbiome

KW - Plant domestication

UR - https://www.biorxiv.org/content/10.1101/2021.12.20.472907v3

UR - http://www.scopus.com/inward/record.url?scp=85132069806&partnerID=8YFLogxK

U2 - 10.1038/s41467-022-31022-y

DO - 10.1038/s41467-022-31022-y

M3 - Article

C2 - 35710760

SN - 2041-1723

VL - 13

JO - Nature Communications

JF - Nature Communications

M1 - 3443

ER -

Identifying plant genes shaping microbiota composition in the barley rhizosphere

Abstract

Keywords

ASJC Scopus subject areas

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Unravelling the Barley Genetic Control of the Rhizosphere Microbiota

Barley root exudates collection and primary metabolite profiling

Cite this

Identifying plant genes shaping microbiota composition in the barley rhizosphere

Abstract

Keywords

ASJC Scopus subject areas

Access to Document

Other files and links

Fingerprint

Projects

Unravelling the Barley Genetic Control of the Rhizosphere Microbiota

Research output

Barley root exudates collection and primary metabolite profiling

Cite this