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Root microbiota drive direct integration of phosphate stress and immunity

Author

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  • Gabriel Castrillo

    (University of North Carolina, Chapel Hill, North Carolina 27599-3280, USA
    Howard Hughes Medical Institute, University of North Carolina)

  • Paulo José Pereira Lima Teixeira

    (University of North Carolina, Chapel Hill, North Carolina 27599-3280, USA
    Howard Hughes Medical Institute, University of North Carolina)

  • Sur Herrera Paredes

    (University of North Carolina, Chapel Hill, North Carolina 27599-3280, USA
    Howard Hughes Medical Institute, University of North Carolina
    Curriculum in Bioinformatics and Computational Biology, University of North Carolina)

  • Theresa F. Law

    (University of North Carolina, Chapel Hill, North Carolina 27599-3280, USA
    Howard Hughes Medical Institute, University of North Carolina)

  • Laura de Lorenzo

    (Centro Nacional de Biotecnología, CNB-CSIC
    †Present addresses: NewLeaf Symbiotics, St. Louis, Missouri 63132, USA (N.W.B.); Department of Plant and Soil Sciences, University of Kentucky, Lexington, Kentucky 40546, USA (L.d.L.).)

  • Meghan E. Feltcher

    (University of North Carolina, Chapel Hill, North Carolina 27599-3280, USA
    Howard Hughes Medical Institute, University of North Carolina)

  • Omri M. Finkel

    (University of North Carolina, Chapel Hill, North Carolina 27599-3280, USA
    Howard Hughes Medical Institute, University of North Carolina)

  • Natalie W. Breakfield

    (University of North Carolina, Chapel Hill, North Carolina 27599-3280, USA
    Howard Hughes Medical Institute, University of North Carolina
    †Present addresses: NewLeaf Symbiotics, St. Louis, Missouri 63132, USA (N.W.B.); Department of Plant and Soil Sciences, University of Kentucky, Lexington, Kentucky 40546, USA (L.d.L.).)

  • Piotr Mieczkowski

    (University of North Carolina
    Lineberger Comprehensive Cancer Center, University of North Carolina
    Carolina Center for Genome Sciences, University of North Carolina)

  • Corbin D. Jones

    (University of North Carolina, Chapel Hill, North Carolina 27599-3280, USA
    Curriculum in Bioinformatics and Computational Biology, University of North Carolina
    University of North Carolina
    Lineberger Comprehensive Cancer Center, University of North Carolina)

  • Javier Paz-Ares

    (Centro Nacional de Biotecnología, CNB-CSIC)

  • Jeffery L. Dangl

    (University of North Carolina, Chapel Hill, North Carolina 27599-3280, USA
    Howard Hughes Medical Institute, University of North Carolina
    Curriculum in Bioinformatics and Computational Biology, University of North Carolina
    Carolina Center for Genome Sciences, University of North Carolina)

Abstract

Plants live in biogeochemically diverse soils with diverse microbiota. Plant organs associate intimately with a subset of these microbes, and the structure of the microbial community can be altered by soil nutrient content. Plant-associated microbes can compete with the plant and with each other for nutrients, but may also carry traits that increase the productivity of the plant. It is unknown how the plant immune system coordinates microbial recognition with nutritional cues during microbiome assembly. Here we establish that a genetic network controlling the phosphate stress response influences the structure of the root microbiome community, even under non-stress phosphate conditions. We define a molecular mechanism regulating coordination between nutrition and defence in the presence of a synthetic bacterial community. We further demonstrate that the master transcriptional regulators of phosphate stress response in Arabidopsis thaliana also directly repress defence, consistent with plant prioritization of nutritional stress over defence. Our work will further efforts to define and deploy useful microbes to enhance plant performance.

Suggested Citation

  • Gabriel Castrillo & Paulo José Pereira Lima Teixeira & Sur Herrera Paredes & Theresa F. Law & Laura de Lorenzo & Meghan E. Feltcher & Omri M. Finkel & Natalie W. Breakfield & Piotr Mieczkowski & Corbi, 2017. "Root microbiota drive direct integration of phosphate stress and immunity," Nature, Nature, vol. 543(7646), pages 513-518, March.
  • Handle: RePEc:nat:nature:v:543:y:2017:i:7646:d:10.1038_nature21417
    DOI: 10.1038/nature21417
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    Cited by:

    1. 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.
    2. Kei Hiruma & Seishiro Aoki & Junya Takino & Takeshi Higa & Yuniar Devi Utami & Akito Shiina & Masanori Okamoto & Masami Nakamura & Nanami Kawamura & Yoshihiro Ohmori & Ryohei Sugita & Keitaro Tanoi & , 2023. "A fungal sesquiterpene biosynthesis gene cluster critical for mutualist-pathogen transition in Colletotrichum tofieldiae," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    3. Beatriz Val-Torregrosa & Mireia Bundó & Blanca San Segundo, 2021. "Crosstalk between Nutrient Signalling Pathways and Immune Responses in Rice," Agriculture, MDPI, vol. 11(8), pages 1-21, August.
    4. Shikai La & Jiafan Li & Si Ma & Xingqun Liu & Lihong Gao & Yongqiang Tian, 2024. "Protective role of native root-associated bacterial consortium against root-knot nematode infection in susceptible plants," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
    5. Yukari Nagatoshi & Kenta Ikazaki & Yasufumi Kobayashi & Nobuyuki Mizuno & Ryohei Sugita & Yumiko Takebayashi & Mikiko Kojima & Hitoshi Sakakibara & Natsuko I. Kobayashi & Keitaro Tanoi & Kenichiro Fuj, 2023. "Phosphate starvation response precedes abscisic acid response under progressive mild drought in plants," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    6. 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.
    7. 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.
    8. Ang Liu & Yaqian Zhao & Yamei Cai & Peiying Kang & Yulong Huang & Min Li & Anran Yang, 2023. "Towards Effective, Sustainable Solution for Hospital Wastewater Treatment to Cope with the Post-Pandemic Era," IJERPH, MDPI, vol. 20(4), pages 1-21, February.
    9. Xin-Ran Li & Jongho Sun & Doris Albinsky & Darius Zarrabian & Raphaella Hull & Tak Lee & Edwin Jarratt-Barnham & Chai Hao Chiu & Amy Jacobsen & Eleni Soumpourou & Alessio Albanese & Wouter Kohlen & Le, 2022. "Nutrient regulation of lipochitooligosaccharide recognition in plants via NSP1 and NSP2," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    10. Yayu Wang & Xiaolin Wang & Shuai Sun & Canzhi Jin & Jianmu Su & Jinpu Wei & Xinyue Luo & Jiawen Wen & Tong Wei & Sunil Kumar Sahu & Hongfeng Zou & Hongyun Chen & Zhixin Mu & Gengyun Zhang & Xin Liu & , 2022. "GWAS, MWAS and mGWAS provide insights into precision agriculture based on genotype-dependent microbial effects in foxtail millet," Nature Communications, Nature, vol. 13(1), pages 1-17, December.
    11. Xuexia Chen & Shuai Zhang & Lijin Yi & Zhengwei Liu & Xiangyu Ye & Bo Yu & Shuai Shi & Xiaoxia Lu, 2022. "Evaluation of Biodegradation of BTEX in the Subsurface of a Petrochemical Site near the Yangtze River, China," IJERPH, MDPI, vol. 19(24), pages 1-12, December.
    12. 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.
    13. Xue Jin & Huiting Jia & Lingyi Ran & Fengzhi Wu & Junjie Liu & Klaus Schlaeppi & Francisco Dini-Andreote & Zhong Wei & Xingang Zhou, 2024. "Fusaric acid mediates the assembly of disease-suppressive rhizosphere microbiota via induced shifts in plant root exudates," Nature Communications, Nature, vol. 15(1), pages 1-15, December.

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