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Functional overlap of the Arabidopsis leaf and root microbiota

Author

Listed:
  • Yang Bai

    (Max Planck Institute for Plant Breeding Research)

  • Daniel B. Müller

    (Institute of Microbiology, ETH Zurich)

  • Girish Srinivas

    (Max Planck Institute for Plant Breeding Research)

  • Ruben Garrido-Oter

    (Max Planck Institute for Plant Breeding Research
    Heinrich Heine University Düsseldorf
    Cluster of Excellence on Plant Sciences (CEPLAS), Max Planck Institute for Plant Breeding Research)

  • Eva Potthoff

    (Institute of Microbiology, ETH Zurich)

  • Matthias Rott

    (Max Planck Institute for Plant Breeding Research)

  • Nina Dombrowski

    (Max Planck Institute for Plant Breeding Research)

  • Philipp C. Münch

    (Computational Biology of Infection Research, Helmholtz Center for Infection Research
    Max-von-Pettenkofer Institute, Ludwig Maximilian University, German Center for Infection Research (DZIF), partner site LMU Munich
    German Center for Infection Research (DZIF), partner site Hannover-Braunschweig)

  • Stijn Spaepen

    (Max Planck Institute for Plant Breeding Research)

  • Mitja Remus-Emsermann

    (Institute of Microbiology, ETH Zurich)

  • Bruno Hüttel

    (Max Planck Genome Center, Max Planck Institute for Plant Breeding Research)

  • Alice C. McHardy

    (Cluster of Excellence on Plant Sciences (CEPLAS), Max Planck Institute for Plant Breeding Research
    Computational Biology of Infection Research, Helmholtz Center for Infection Research)

  • Julia A. Vorholt

    (Institute of Microbiology, ETH Zurich)

  • Paul Schulze-Lefert

    (Max Planck Institute for Plant Breeding Research
    Cluster of Excellence on Plant Sciences (CEPLAS), Max Planck Institute for Plant Breeding Research)

Abstract

Roots and leaves of healthy plants host taxonomically structured bacterial assemblies, and members of these communities contribute to plant growth and health. We established Arabidopsis leaf- and root-derived microbiota culture collections representing the majority of bacterial species that are reproducibly detectable by culture-independent community sequencing. We found an extensive taxonomic overlap between the leaf and root microbiota. Genome drafts of 400 isolates revealed a large overlap of genome-encoded functional capabilities between leaf- and root-derived bacteria with few significant differences at the level of individual functional categories. Using defined bacterial communities and a gnotobiotic Arabidopsis plant system we show that the isolates form assemblies resembling natural microbiota on their cognate host organs, but are also capable of ectopic leaf or root colonization. While this raises the possibility of reciprocal relocation between root and leaf microbiota members, genome information and recolonization experiments also provide evidence for microbiota specialization to their respective niche.

Suggested Citation

  • 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.
  • Handle: RePEc:nat:nature:v:528:y:2015:i:7582:d:10.1038_nature16192
    DOI: 10.1038/nature16192
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    Cited by:

    1. Lucas Hemmerle & Benjamin A. Maier & Miriam Bortfeld-Miller & Birgitta Ryback & Christoph G. Gäbelein & Martin Ackermann & Julia A. Vorholt, 2022. "Dynamic character displacement among a pair of bacterial phyllosphere commensals in situ," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    2. 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.
    3. Mingxing Wang & An-Hui Ge & Xingzhu Ma & Xiaolin Wang & Qiujin Xie & Like Wang & Xianwei Song & Mengchen Jiang & Weibing Yang & Jeremy D. Murray & Yayu Wang & Huan Liu & Xiaofeng Cao & Ertao Wang, 2024. "Dynamic root microbiome sustains soybean productivity under unbalanced fertilization," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    4. Barbara Emmenegger & Julien Massoni & Christine M. Pestalozzi & Miriam Bortfeld-Miller & Benjamin A. Maier & Julia A. Vorholt, 2023. "Identifying microbiota community patterns important for plant protection using synthetic communities and machine learning," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    5. Zhaohui Cao & Wenlong Zuo & Lanxiang Wang & Junyu Chen & Zepeng Qu & Fan Jin & Lei Dai, 2023. "Spatial profiling of microbial communities by sequential FISH with error-robust encoding," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    6. Frederickson Entila & Xiaowei Han & Akira Mine & Paul Schulze-Lefert & Kenichi Tsuda, 2024. "Commensal lifestyle regulated by a negative feedback loop between Arabidopsis ROS and the bacterial T2SS," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    7. Li Fan & Katja Fröhlich & Eric Melzer & Rory N. Pruitt & Isabell Albert & Lisha Zhang & Anna Joe & Chenlei Hua & Yanyue Song & Markus Albert & Sang-Tae Kim & Detlef Weigel & Cyril Zipfel & Eunyoung Ch, 2022. "Genotyping-by-sequencing-based identification of Arabidopsis pattern recognition receptor RLP32 recognizing proteobacterial translation initiation factor IF1," Nature Communications, Nature, vol. 13(1), pages 1-13, December.
    8. Nathan Vannier & Fantin Mesny & Felix Getzke & Guillaume Chesneau & Laura Dethier & Jana Ordon & Thorsten Thiergart & Stéphane Hacquard, 2023. "Genome-resolved metatranscriptomics reveals conserved root colonization determinants in a synthetic microbiota," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    9. Benjamin H. Good & Layton B. Rosenfeld, 2023. "Eco-evolutionary feedbacks in the human gut microbiome," Nature Communications, Nature, vol. 14(1), pages 1-9, December.
    10. Lige Ma & Yu Luo & Chen Chen & Huan Luo & Shuqi Wang & Yue Yuan & Wenhua Yang & Can Liu & Xulv Cao & Nannan Li, 2023. "Bacterial Strategies for Improving the Yield, Quality, and Adaptability of Oil Crops," Agriculture, MDPI, vol. 14(1), pages 1-29, December.
    11. Jing Liang & Jiafan Zhang & Zongmu Yao & Shouyang Luo & Lei Tian & Chunjie Tian & Yu Sun, 2022. "Preliminary Findings of Polypropylene Carbonate (PPC) Plastic Film Mulching Effects on the Soil Microbial Community," Agriculture, MDPI, vol. 12(3), pages 1-13, March.
    12. Carin J. Ragland & Kevin Y. Shih & José R. Dinneny, 2024. "Choreographing root architecture and rhizosphere interactions through synthetic biology," Nature Communications, Nature, vol. 15(1), pages 1-11, December.
    13. Guy Amit & Amir Bashan, 2023. "Top-down identification of keystone taxa in the microbiome," Nature Communications, Nature, vol. 14(1), pages 1-12, December.
    14. Xin Zhou & Jinting Wang & Fang Liu & Junmin Liang & Peng Zhao & Clement K. M. Tsui & Lei Cai, 2022. "Cross-kingdom synthetic microbiota supports tomato suppression of Fusarium wilt disease," Nature Communications, Nature, vol. 13(1), pages 1-17, December.
    15. Chengjia Tan & Mohammad Talib Kalhoro & Yahya Faqir & Jiahua Ma & Matthew Duah Osei & Ghulam Khaliq, 2022. "Climate-Resilient Microbial Biotechnology: A Perspective on Sustainable Agriculture," Sustainability, MDPI, vol. 14(9), pages 1-29, May.

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