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Disentangling the genetic basis of rhizosphere microbiome assembly in tomato

Author

Listed:
  • Ben O. Oyserman

    (Netherlands Institute of Ecology
    Wageningen University)

  • Stalin Sarango Flores

    (Netherlands Institute of Ecology
    Leiden University)

  • Thom Griffioen

    (Netherlands Institute of Ecology)

  • Xinya Pan

    (Netherlands Institute of Ecology)

  • Elmar Wijk

    (Wageningen University)

  • Lotte Pronk

    (Wageningen University)

  • Wouter Lokhorst

    (Netherlands Institute of Ecology)

  • Azkia Nurfikari

    (Netherlands Institute of Ecology)

  • Joseph N. Paulson

    (Genentech, Inc. South San Francisco)

  • Mercedeh Movassagh

    (Harvard T.H. Chan School of Public Health
    Harvard T.H. Chan School of Public Health)

  • Nejc Stopnisek

    (Netherlands Institute of Ecology)

  • Anne Kupczok

    (Wageningen University)

  • Viviane Cordovez

    (Netherlands Institute of Ecology)

  • Víctor J. Carrión

    (Netherlands Institute of Ecology
    Leiden University)

  • Wilco Ligterink

    (Wageningen University)

  • Basten L. Snoek

    (Utrecht University)

  • Marnix H. Medema

    (Wageningen University
    Leiden University)

  • Jos M. Raaijmakers

    (Netherlands Institute of Ecology
    Leiden University)

Abstract

Microbiomes play a pivotal role in plant growth and health, but the genetic factors involved in microbiome assembly remain largely elusive. Here, we map the molecular features of the rhizosphere microbiome as quantitative traits of a diverse hybrid population of wild and domesticated tomato. Gene content analysis of prioritized tomato quantitative trait loci suggests a genetic basis for differential recruitment of various rhizobacterial lineages, including a Streptomyces-associated 6.31 Mbp region harboring tomato domestication sweeps and encoding, among others, the iron regulator FIT and the water channel aquaporin SlTIP2.3. Within metagenome-assembled genomes of root-associated Streptomyces and Cellvibrio, we identify bacterial genes involved in metabolism of plant polysaccharides, iron, sulfur, trehalose, and vitamins, whose genetic variation associates with specific tomato QTLs. By integrating ‘microbiomics’ and quantitative plant genetics, we pinpoint putative plant and reciprocal rhizobacterial traits underlying microbiome assembly, thereby providing a first step towards plant-microbiome breeding programs.

Suggested Citation

  • 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.
  • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-30849-9
    DOI: 10.1038/s41467-022-30849-9
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    Cited by:

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    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. 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.
    4. 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.
    5. 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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