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Identifying plant genes shaping microbiota composition in the barley rhizosphere

Author

Listed:
  • Carmen Escudero-Martinez

    (University of Dundee, Plant Sciences, School of Life Sciences)

  • Max Coulter

    (University of Dundee, Plant Sciences, School of Life Sciences
    University of Dundee, Computational Biology, School of Life Sciences)

  • Rodrigo Alegria Terrazas

    (University of Dundee, Plant Sciences, School of Life Sciences
    Mohammed VI Polytechnic University, Agrobiosciences Program, Plant & Soil Microbiome Subprogram)

  • Alexandre Foito

    (The James Hutton Institute)

  • Rumana Kapadia

    (University of Dundee, Plant Sciences, School of Life Sciences)

  • Laura Pietrangelo

    (University of Dundee, Plant Sciences, School of Life Sciences
    University of Molise)

  • Mauro Maver

    (University of Dundee, Plant Sciences, School of Life Sciences
    Free University of Bozen-Bolzano
    Free University of Bozen-Bolzano)

  • Rajiv Sharma

    (Scotland’s Rural College)

  • Alessio Aprile

    (University of Dundee, Plant Sciences, School of Life Sciences
    University of Salento)

  • Jenny Morris

    (The James Hutton Institute)

  • Pete E. Hedley

    (The James Hutton Institute)

  • Andreas Maurer

    (Martin-Luther-University)

  • Klaus Pillen

    (Martin-Luther-University)

  • Gino Naclerio

    (University of Molise)

  • Tanja Mimmo

    (Free University of Bozen-Bolzano
    Free University of Bozen-Bolzano)

  • Geoffrey J. Barton

    (University of Dundee, Computational Biology, School of Life Sciences)

  • Robbie Waugh

    (University of Dundee, Plant Sciences, School of Life Sciences
    The James Hutton Institute)

  • James Abbott

    (University of Dundee, Computational Biology, School of Life Sciences)

  • Davide Bulgarelli

    (University of Dundee, Plant Sciences, School of Life Sciences)

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 plant’s capacity of shaping rhizosphere microbes.

Suggested Citation

  • Carmen Escudero-Martinez & Max Coulter & Rodrigo Alegria Terrazas & Alexandre Foito & Rumana Kapadia & Laura Pietrangelo & Mauro Maver & Rajiv Sharma & Alessio Aprile & Jenny Morris & Pete E. Hedley &, 2022. "Identifying plant genes shaping microbiota composition in the barley rhizosphere," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
  • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-31022-y
    DOI: 10.1038/s41467-022-31022-y
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    1. Martin Mascher & Heidrun Gundlach & Axel Himmelbach & Sebastian Beier & Sven O. Twardziok & Thomas Wicker & Volodymyr Radchuk & Christoph Dockter & Pete E. Hedley & Joanne Russell & Micha Bayer & Luke, 2017. "A chromosome conformation capture ordered sequence of the barley genome," Nature, Nature, vol. 544(7651), pages 427-433, April.
    2. Yang Bai & Daniel B. Müller & Girish Srinivas & Ruben Garrido-Oter & Eva Potthoff & Matthias Rott & Nina Dombrowski & Philipp C. Münch & Stijn Spaepen & Mitja Remus-Emsermann & Bruno Hüttel & Alice C., 2015. "Functional overlap of the Arabidopsis leaf and root microbiota," Nature, Nature, vol. 528(7582), pages 364-369, December.
    3. Matthew W. Horton & Natacha Bodenhausen & Kathleen Beilsmith & Dazhe Meng & Brian D. Muegge & Sathish Subramanian & M. Madlen Vetter & Bjarni J. Vilhjálmsson & Magnus Nordborg & Jeffrey I. Gordon & Jo, 2014. "Genome-wide association study of Arabidopsis thaliana leaf microbial community," Nature Communications, Nature, vol. 5(1), pages 1-7, December.
    4. Jonathan D. G. Jones & Jeffery L. Dangl, 2006. "The plant immune system," Nature, Nature, vol. 444(7117), pages 323-329, November.
    5. Murukarthick Jayakodi & Sudharsan Padmarasu & Georg Haberer & Venkata Suresh Bonthala & Heidrun Gundlach & Cécile Monat & Thomas Lux & Nadia Kamal & Daniel Lang & Axel Himmelbach & Jennifer Ens & Xiao, 2020. "The barley pan-genome reveals the hidden legacy of mutation breeding," Nature, Nature, vol. 588(7837), pages 284-289, December.
    6. Ben O. Oyserman & Stalin Sarango Flores & Thom Griffioen & Xinya Pan & Elmar Wijk & Lotte Pronk & Wouter Lokhorst & Azkia Nurfikari & Joseph N. Paulson & Mercedeh Movassagh & Nejc Stopnisek & Anne Kup, 2022. "Disentangling the genetic basis of rhizosphere microbiome assembly in tomato," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
    7. Huan Wang & Shenghao Zou & Yiwen Li & Fanyun Lin & Dingzhong Tang, 2020. "An ankyrin-repeat and WRKY-domain-containing immune receptor confers stripe rust resistance in wheat," Nature Communications, Nature, vol. 11(1), pages 1-11, December.
    8. Davide Bulgarelli & Matthias Rott & Klaus Schlaeppi & Emiel Ver Loren van Themaat & Nahal Ahmadinejad & Federica Assenza & Philipp Rauf & Bruno Huettel & Richard Reinhardt & Elmon Schmelzer & Joerg Pe, 2012. "Revealing structure and assembly cues for Arabidopsis root-inhabiting bacterial microbiota," Nature, Nature, vol. 488(7409), pages 91-95, August.
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    Cited by:

    1. Tomislav Cernava, 2024. "Coming of age for Microbiome gene breeding in plants," Nature Communications, Nature, vol. 15(1), pages 1-3, December.
    2. Pin Su & Houxiang Kang & Qianze Peng & Wisnu Adi Wicaksono & Gabriele Berg & Zhuoxin Liu & Jiejia Ma & Deyong Zhang & Tomislav Cernava & Yong Liu, 2024. "Microbiome homeostasis on rice leaves is regulated by a precursor molecule of lignin biosynthesis," Nature Communications, Nature, vol. 15(1), pages 1-16, December.

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