The plant specific transcription factors CBP60g and SARD1 are targeted by a Verticillium secretory protein VdSCP41 to modulate immunity

  1. Jun Qin
  2. Kailun Wang
  3. Lifan Sun
  4. Haiying Xing
  5. Sheng Wang
  6. Lin Li
  7. She Chen
  8. Hui-Shan Guo  Is a corresponding author
  9. Jie Zhang  Is a corresponding author
  1. Chinese Academy of Sciences, China
  2. National Institute of Biological Sciences, China

Abstract

The vascular pathogen Verticillium dahliae infects the roots of plants to cause Verticillium wilt. The molecular mechanisms underlying V. dahliae virulence and host resistance remain elusive. Here, we demonstrate that a secretory protein, VdSCP41, functions as an intracellular effector that promotes V. dahliae virulence. The Arabidopsis master immune regulators CBP60g and SARD1 and cotton GhCBP60b are targeted by VdSCP41. VdSCP41 binds the C-terminal portion of CBP60g to inhibit its transcription factor activity. Further analyses reveal a transcription activation domain within CBP60g that is required for VdSCP41 targeting. Mutations in both CBP60g and SARD1 compromise Arabidopsis resistance against V. dahliae and partially impair VdSCP41-mediated virulence. Moreover, Virus-induced silencing of GhCBP60b compromises cotton resistance to V. dahliae. This work uncovers a virulence strategy in which the V. dahliae secretory protein, VdSCP41, directly targets plant transcription factors to inhibit immunity, and reveals CBP60g, SARD1 and GhCBP60b as crucial components governing V. dahliae resistance.

Data availability

All data generated or analysed during this study are included in the manuscript and supporting files. Source data files have been provided.

Article and author information

Author details

  1. Jun Qin

    State Key Laboratory of Plant Genomics, Institute of Microbiology, Chinese Academy of Sciences, Beijing, China
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-1306-3433
  2. Kailun Wang

    State Key Laboratory of Plant Genomics, Institute of Microbiology, Chinese Academy of Sciences, Beijing, China
    Competing interests
    The authors declare that no competing interests exist.
  3. Lifan Sun

    State Key Laboratory of Plant Genomics, Institute of Microbiology, Chinese Academy of Sciences, Beijing, China
    Competing interests
    The authors declare that no competing interests exist.
  4. Haiying Xing

    State Key Laboratory of Plant Genomics, Institute of Microbiology, Chinese Academy of Sciences, Beijing, China
    Competing interests
    The authors declare that no competing interests exist.
  5. Sheng Wang

    State Key Laboratory of Plant Genomics, Institute of Microbiology, Chinese Academy of Sciences, Beijing, China
    Competing interests
    The authors declare that no competing interests exist.
  6. Lin Li

    National Institute of Biological Sciences, Beijing, China
    Competing interests
    The authors declare that no competing interests exist.
  7. She Chen

    National Institute of Biological Sciences, Beijing, China
    Competing interests
    The authors declare that no competing interests exist.
  8. Hui-Shan Guo

    State Key Laboratory of Plant Genomics, Institute of Microbiology, Chinese Academy of Sciences, Beijing, China
    For correspondence
    guohs@im.ac.cn
    Competing interests
    The authors declare that no competing interests exist.
  9. Jie Zhang

    State Key Laboratory of Plant Genomics, Institute of Microbiology, Chinese Academy of Sciences, Beijing, China
    For correspondence
    zhangjie@im.ac.cn
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-2781-8956

Funding

The Strategic Priority Research Program of the Chinese Academy of Sciences (XDB11020600)

  • Hui-Shan Guo
  • Jie Zhang

National Natural Science Foundation of China (31730078)

  • Jun Qin
  • Hui-Shan Guo
  • Jie Zhang

The Youth Innovation Promotion Association of Chinese Academy of Sciences

  • Jie Zhang

The Strategic Priority Research Program of the Chinese Academy of Sciences (XDB11040500)

  • Hui-Shan Guo
  • Jie Zhang

National Natural Science Foundation of China (31571968)

  • Jun Qin
  • Hui-Shan Guo
  • Jie Zhang

National Natural Science Foundation of China (31501593)

  • Jun Qin
  • Hui-Shan Guo
  • Jie Zhang

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

Reviewing Editor

  1. Gary Stacey, University of Missouri, United States

Version history

  1. Received: January 11, 2018
  2. Accepted: May 11, 2018
  3. Accepted Manuscript published: May 14, 2018 (version 1)
  4. Version of Record published: June 8, 2018 (version 2)

Copyright

© 2018, Qin 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.

Metrics

  • 4,222
    views
  • 1,113
    downloads
  • 101
    citations

Views, downloads and citations are aggregated across all versions of this paper published by eLife.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Open citations (links to open the citations from this article in various online reference manager services)

Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)

  1. Jun Qin
  2. Kailun Wang
  3. Lifan Sun
  4. Haiying Xing
  5. Sheng Wang
  6. Lin Li
  7. She Chen
  8. Hui-Shan Guo
  9. Jie Zhang
(2018)
The plant specific transcription factors CBP60g and SARD1 are targeted by a Verticillium secretory protein VdSCP41 to modulate immunity
eLife 7:e34902.
https://doi.org/10.7554/eLife.34902

Share this article

https://doi.org/10.7554/eLife.34902

Further reading

    1. Microbiology and Infectious Disease
    2. Structural Biology and Molecular Biophysics
    Thomas Kuhlman
    Insight

    A new study reveals how naturally occurring mutations affect the biophysical properties of nucleocapsid proteins in SARS-CoV-2.

    1. Microbiology and Infectious Disease
    Gretchen Diffendall, Aurelie Claes ... Artur Scherf
    Research Article

    While often undetected and untreated, persistent seasonal asymptomatic malaria infections remain a global public health problem. Despite the presence of parasites in the peripheral blood, no symptoms develop. Disease severity is correlated with the levels of infected red blood cells (iRBCs) adhering within blood vessels. Changes in iRBC adhesion capacity have been linked to seasonal asymptomatic malaria infections, however how this is occurring is still unknown. Here, we present evidence that RNA polymerase III (RNA Pol III) transcription in Plasmodium falciparum is downregulated in field isolates obtained from asymptomatic individuals during the dry season. Through experiments with in vitro cultured parasites, we have uncovered an RNA Pol III-dependent mechanism that controls pathogen proliferation and expression of a major virulence factor in response to external stimuli. Our findings establish a connection between P. falciparum cytoadhesion and a non-coding RNA family transcribed by Pol III. Additionally, we have identified P. falciparum Maf1 as a pivotal regulator of Pol III transcription, both for maintaining cellular homeostasis and for responding adaptively to external signals. These results introduce a novel perspective that contributes to our understanding of P. falciparum virulence. Furthermore, they establish a connection between this regulatory process and the occurrence of seasonal asymptomatic malaria infections.