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Convergent evolution of plant pattern recognition receptors sensing cysteine-rich patterns from three microbial kingdoms

Author

Listed:
  • Yuankun Yang

    (Eberhard-Karls-University of Tübingen)

  • Christina E. Steidele

    (Eberhard-Karls-University of Tübingen
    Technische Universität München)

  • Clemens Rössner

    (Justus-Liebig-University Gießen)

  • Birgit Löffelhardt

    (Eberhard-Karls-University of Tübingen)

  • Dagmar Kolb

    (Eberhard-Karls-University of Tübingen)

  • Thomas Leisen

    (Technical University of Kaiserslautern)

  • Weiguo Zhang

    (Eberhard-Karls-University of Tübingen
    Northwest University)

  • Christina Ludwig

    (Technische Universität München)

  • Georg Felix

    (Eberhard-Karls-University of Tübingen)

  • Michael F. Seidl

    (Utrecht University
    Wageningen University & Research)

  • Annette Becker

    (Justus-Liebig-University Gießen)

  • Thorsten Nürnberger

    (Eberhard-Karls-University of Tübingen)

  • Matthias Hahn

    (Technical University of Kaiserslautern)

  • Bertolt Gust

    (Eberhard-Karls-University of Tübingen)

  • Harald Gross

    (Eberhard-Karls-University of Tübingen)

  • Ralph Hückelhoven

    (Technische Universität München)

  • Andrea A. Gust

    (Eberhard-Karls-University of Tübingen)

Abstract

The Arabidopsis thaliana Receptor-Like Protein RLP30 contributes to immunity against the fungal pathogen Sclerotinia sclerotiorum. Here we identify the RLP30-ligand as a small cysteine-rich protein (SCP) that occurs in many fungi and oomycetes and is also recognized by the Nicotiana benthamiana RLP RE02. However, RLP30 and RE02 share little sequence similarity and respond to different parts of the native/folded protein. Moreover, some Brassicaceae other than Arabidopsis also respond to a linear SCP peptide instead of the folded protein, suggesting that SCP is an eminent immune target that led to the convergent evolution of distinct immune receptors in plants. Surprisingly, RLP30 shows a second ligand specificity for a SCP-nonhomologous protein secreted by bacterial Pseudomonads. RLP30 expression in N. tabacum results in quantitatively lower susceptibility to bacterial, fungal and oomycete pathogens, thus demonstrating that detection of immunogenic patterns by Arabidopsis RLP30 is involved in defense against pathogens from three microbial kingdoms.

Suggested Citation

  • 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.
    • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-39208-8
    DOI: 10.1038/s41467-023-39208-8
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    1. 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.
    2. Jonathan D. G. Jones & Jeffery L. Dangl, 2006. "The plant immune system," Nature, Nature, vol. 444(7117), pages 323-329, November.
    3. Björn Schwanhäusser & Dorothea Busse & Na Li & Gunnar Dittmar & Johannes Schuchhardt & Jana Wolf & Wei Chen & Matthias Selbach, 2011. "Global quantification of mammalian gene expression control," Nature, Nature, vol. 473(7347), pages 337-342, May.
    4. 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.
    5. 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.
    6. Jizong Wang & Hongju Li & Zhifu Han & Heqiao Zhang & Tong Wang & Guangzhong Lin & Junbiao Chang & Weicai Yang & Jijie Chai, 2015. "Allosteric receptor activation by the plant peptide hormone phytosulfokine," Nature, Nature, vol. 525(7568), pages 265-268, September.
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