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Genotyping-by-sequencing-based identification of Arabidopsis pattern recognition receptor RLP32 recognizing proteobacterial translation initiation factor IF1

Author

Listed:
  • Li Fan

    (University of Tübingen)

  • Katja Fröhlich

    (University of Tübingen)

  • Eric Melzer

    (University of Tübingen
    BioChem agrar, Labor für biologische und chemische Analytik GmbH)

  • Rory N. Pruitt

    (University of Tübingen)

  • Isabell Albert

    (University of Tübingen
    University of Erlangen-Nürnberg)

  • Lisha Zhang

    (University of Tübingen)

  • Anna Joe

    (University of Tübingen)

  • Chenlei Hua

    (University of Tübingen)

  • Yanyue Song

    (University of Tübingen)

  • Markus Albert

    (University of Tübingen
    University of Erlangen-Nürnberg)

  • Sang-Tae Kim

    (Max Planck Institute for Developmental Biology
    The Catholic University of Korea)

  • Detlef Weigel

    (Max Planck Institute for Developmental Biology)

  • Cyril Zipfel

    (University of Zürich)

  • Eunyoung Chae

    (Max Planck Institute for Developmental Biology
    National University of Singapore)

  • Andrea A. Gust

    (University of Tübingen)

  • Thorsten Nürnberger

    (University of Tübingen
    University of Johannesburg)

Abstract

Activation of plant pattern-triggered immunity (PTI) relies on the recognition of microbe-derived structures, termed patterns, through plant-encoded surface-resident pattern recognition receptors (PRRs). We show that proteobacterial translation initiation factor 1 (IF1) triggers PTI in Arabidopsis thaliana and related Brassicaceae species. Unlike for most other immunogenic patterns, IF1 elicitor activity cannot be assigned to a small peptide epitope, suggesting that tertiary fold features are required for IF1 receptor activation. We have deployed natural variation in IF1 sensitivity to identify Arabidopsis leucine-rich repeat (LRR) receptor-like protein 32 (RLP32) as IF1 receptor using a restriction site-associated DNA sequencing approach. RLP32 confers IF1 sensitivity to rlp32 mutants, IF1-insensitive Arabidopsis accessions and IF1-insensitive Nicotiana benthamiana, binds IF1 specifically and forms complexes with LRR receptor kinases SOBIR1 and BAK1 to mediate signaling. Similar to other PRRs, RLP32 confers resistance to Pseudomonas syringae, highlighting an unexpectedly complex array of bacterial pattern sensors within a single plant species.

Suggested Citation

  • 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.
    • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-28887-4
    DOI: 10.1038/s41467-022-28887-4
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    1. Yan Wang & Yuanpeng Xu & Yujing Sun & Huibin Wang & Jiaming Qi & Bowen Wan & Wenwu Ye & Yachun Lin & Yuanyuan Shao & Suomeng Dong & Brett M. Tyler & Yuanchao Wang, 2018. "Leucine-rich repeat receptor-like gene screen reveals that Nicotiana RXEG1 regulates glycoside hydrolase 12 MAMP detection," Nature Communications, Nature, vol. 9(1), pages 1-12, December.
    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. M. Salanoubat & S. Genin & F. Artiguenave & J. Gouzy & S. Mangenot & M. Arlat & A. Billault & P. Brottier & J. C. Camus & L. Cattolico & M. Chandler & N. Choisne & C. Claudel-Renard & S. Cunnac & N. D, 2002. "Genome sequence of the plant pathogen Ralstonia solanacearum," Nature, Nature, vol. 415(6871), pages 497-502, January.
    4. Volker Hegenauer & Peter Slaby & Max Körner & Julien-Alexander Bruckmüller & Ronja Burggraf & Isabell Albert & Bettina Kaiser & Birgit Löffelhardt & Irina Droste-Borel & Jan Sklenar & Frank L. H. Menk, 2020. "The tomato receptor CuRe1 senses a cell wall protein to identify Cuscuta as a pathogen," Nature Communications, Nature, vol. 11(1), pages 1-7, December.
    5. Bruno Pok Man Ngou & Hee-Kyung Ahn & Pingtao Ding & Jonathan D. G. Jones, 2021. "Mutual potentiation of plant immunity by cell-surface and intracellular receptors," Nature, Nature, vol. 592(7852), pages 110-115, April.
    6. Rory N. Pruitt & Federica Locci & Friederike Wanke & Lisha Zhang & Svenja C. Saile & Anna Joe & Darya Karelina & Chenlei Hua & Katja Fröhlich & Wei-Lin Wan & Meijuan Hu & Shaofei Rao & Sara C. Stolze , 2021. "The EDS1–PAD4–ADR1 node mediates Arabidopsis pattern-triggered immunity," Nature, Nature, vol. 598(7881), pages 495-499, October.
    7. Cyril Zipfel & Silke Robatzek & Lionel Navarro & Edward J. Oakeley & Jonathan D. G. Jones & Georg Felix & Thomas Boller, 2004. "Bacterial disease resistance in Arabidopsis through flagellin perception," Nature, Nature, vol. 428(6984), pages 764-767, April.
    8. Magnus Nordborg & Tina T Hu & Yoko Ishino & Jinal Jhaveri & Christopher Toomajian & Honggang Zheng & Erica Bakker & Peter Calabrese & Jean Gladstone & Rana Goyal & Mattias Jakobsson & Sung Kim & Yuri , 2005. "The Pattern of Polymorphism in Arabidopsis thaliana," PLOS Biology, Public Library of Science, vol. 3(7), pages 1-1, May.
    9. Minhang Yuan & Zeyu Jiang & Guozhi Bi & Kinya Nomura & Menghui Liu & Yiping Wang & Boying Cai & Jian-Min Zhou & Sheng Yang He & Xiu-Fang Xin, 2021. "Pattern-recognition receptors are required for NLR-mediated plant immunity," Nature, Nature, vol. 592(7852), pages 105-109, April.
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    1. Yuankun Yang & Christina E. Steidele & Clemens Rössner & Birgit Löffelhardt & Dagmar Kolb & Thomas Leisen & Weiguo Zhang & Christina Ludwig & Georg Felix & Michael F. Seidl & Annette Becker & Thorsten, 2023. "Convergent evolution of plant pattern recognition receptors sensing cysteine-rich patterns from three microbial kingdoms," Nature Communications, Nature, vol. 14(1), pages 1-12, December.

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