Acetylation of a fungal effector that translocates host PR1 facilitates virulence

  1. Jingtao Li
  2. Xiaoying Ma
  3. Chenyang Wang
  4. Sihui Liu
  5. Gang Yu
  6. Mingming Gao
  7. Hengwei Qian
  8. Mengjie Liu
  9. Ben F Luisi
  10. Dean W Gabriel
  11. Wenxing Liang  Is a corresponding author
  1. Qingdao Agricultural University, China
  2. Shanghai Jiao Tong University, China
  3. University of Cambridge, United Kingdom
  4. University of Florida, United States

Abstract

Pathogens utilize a panoply of effectors to manipulate plant defense. However, despite their importance, relatively little is actually known about regulation of these virulence factors. Here, we show that the effector FolSvp1, secreted from fungal pathogen Fusarium oxysporum f. sp. lycopersici (Fol) directly binds and translocates the tomato pathogenesis-related protein1, SlPR1, from the apoplast outside the plasma membrane to the host nucleus via its nuclear localization signal. Relocation of SlPR1 abolishes generation of the defense signaling peptide, CAPE1, from its C-terminus, and as a consequence, facilitates pathogen invasion of plants. The action of FolSvp1 requires covalent modification by acetylation for full virulence in host tomato tissues. The modification is catalyzed by the Fol FolArd1 lysine acetyltransferase prior to secretion. Addition of an acetyl group to one residue, K167, prevents ubiquitination-dependent degradation of FolSvp1 in both Fol and plant cells with different mechanisms, allowing it to function normally in fungal invasion. Either inactivation of FolSvp1 or removal of the acetyl group on K167 leads to impaired pathogenicity of Fol. These findings indicate that acetylation can regulate the stability of effectors of fungal plant pathogens with impact on virulence.

Data availability

All data generated or analysed during this study are included in the manuscript and supporting file.

Article and author information

Author details

  1. Jingtao Li

    Shandong Province Key Laboratory of Applied Mycology, Qingdao Agricultural University, Qingdao, China
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-2702-1736
  2. Xiaoying Ma

    Shandong Province Key Laboratory of Applied Mycology, Qingdao Agricultural University, Qingdao, China
    Competing interests
    The authors declare that no competing interests exist.
  3. Chenyang Wang

    Shandong Province Key Laboratory of Applied Mycology, Qingdao Agricultural University, Qingdao, China
    Competing interests
    The authors declare that no competing interests exist.
  4. Sihui Liu

    College of Science and Information, Qingdao Agricultural University, Qingdao, China
    Competing interests
    The authors declare that no competing interests exist.
  5. Gang Yu

    School of Agriculture and Biology, Shanghai Jiao Tong University, Shanghai, China
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-6720-7490
  6. Mingming Gao

    Shandong Province Key Laboratory of Applied Mycology, Qingdao Agricultural University, Qingdao, China
    Competing interests
    The authors declare that no competing interests exist.
  7. Hengwei Qian

    Shandong Province Key Laboratory of Applied Mycology, Qingdao Agricultural University, Qingdao, China
    Competing interests
    The authors declare that no competing interests exist.
  8. Mengjie Liu

    Shandong Province Key Laboratory of Applied Mycology, Qingdao Agricultural University, Qingdao, China
    Competing interests
    The authors declare that no competing interests exist.
  9. Ben F Luisi

    Department of Biochemistry, University of Cambridge, Cambridge, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-1144-9877
  10. Dean W Gabriel

    Department of Plant Pathology, University of Florida, Gainesville, United States
    Competing interests
    The authors declare that no competing interests exist.
  11. Wenxing Liang

    Shandong Province Key Laboratory of Applied Mycology, Qingdao Agricultural University, Qingdao, China
    For correspondence
    wliang1@qau.edu.cn
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-3791-4901

Funding

National Natural Science Foundation of China (31901830)

  • Jingtao Li

Wellcome Trust Investigator (222451/Z/21/Z)

  • Ben F Luisi

National Natural Science Foundation of China (31972213)

  • Wenxing Liang

Natural Science Foundation of Shandong Province (ZR2019BC032)

  • Jingtao Li

Natural Science Foundation of Shandong Province (ZR2020KC003)

  • Wenxing Liang

Ministry of Agriculture of China (2016ZX08009003-001)

  • Wenxing Liang

Key Research and Development Program of Shandong Province (2019YQ017)

  • Wenxing Liang

Shandong Province Double-Hundred Talent Plan"" (WST2018008)

  • Wenxing Liang

Taishan Scholar Project of Shandong Province (tshw20130963)

  • Wenxing Liang

Wellcome Trust Investigator (200873/Z/16/Z)

  • Ben F Luisi

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Reviewing Editor

  1. Jian-Min Zhou, Chinese Academy of Sciences, China

Publication history

  1. Received: August 11, 2022
  2. Preprint posted: September 10, 2022 (view preprint)
  3. Accepted: November 11, 2022
  4. Accepted Manuscript published: November 14, 2022 (version 1)
  5. Version of Record published: November 22, 2022 (version 2)

Copyright

© 2022, Li et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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  1. Jingtao Li
  2. Xiaoying Ma
  3. Chenyang Wang
  4. Sihui Liu
  5. Gang Yu
  6. Mingming Gao
  7. Hengwei Qian
  8. Mengjie Liu
  9. Ben F Luisi
  10. Dean W Gabriel
  11. Wenxing Liang
(2022)
Acetylation of a fungal effector that translocates host PR1 facilitates virulence
eLife 11:e82628.
https://doi.org/10.7554/eLife.82628
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