Geminivirus-encoded TrAP suppressor inhibits the histone methyltransferase SUVH4/KYP to counter host defense

  1. Claudia Castillo-González
  2. Xiuying Liu
  3. Changjun Huang
  4. Changjiang Zhao
  5. Zeyang Ma
  6. Tao Hu
  7. Feng Sun
  8. Yijun Zhou
  9. Xiu-Jie Wang
  10. Xueping Zhou
  11. Xiuren Zhang  Is a corresponding author
  1. Texas A&M University, United States
  2. Jiangsu Academy of Agricultural Sciences, China
  3. Chinese Academy of Sciences, China
  4. Zhejiang University, China

Abstract

Transcriptional gene silencing (TGS) can serve as an innate immunity against invading DNA viruses throughout Eukaryotes. Geminivirus code for TrAP protein to suppress the TGS pathway. Here we identified an Arabidopsis H3K9me2 histone methyltransferase, Su(var)3-9 homolog 4 (SUVH4/KYP), as a bona fide cellular target of TrAP. TrAP interacts with the catalytic domain of KYP and inhibits its activity in vitro. TrAP elicits developmental anomalies phenocopying several TGS mutants, reduces the repressive H3K9me2 mark and CHH DNA methylation, and reactivates numerous endogenous KYP-repressed loci in vivo. Moreover, KYP binds to the viral chromatin, and controls its methylation to combat virus infection. Notably, kyp mutants support systemic infection of TrAP-deficient Geminivirus. We conclude that TrAP attenuates the TGS of the viral chromatin by inhibiting KYP activity to evade host surveillance. These findings provide new insight on the molecular arms race between host antiviral defense and virus counter defense at an epigenetic level.

Article and author information

Author details

  1. Claudia Castillo-González

    Department of Biochemistry and Biophysics, Texas A&M University, College Station, United States
    Competing interests
    The authors declare that no competing interests exist.
  2. Xiuying Liu

    Department of Biochemistry and Biophysics, Texas A&M University, College Station, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Changjun Huang

    Department of Biochemistry and Biophysics, Texas A&M University, College Station, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Changjiang Zhao

    Department of Biochemistry and Biophysics, Texas A&M University, College Station, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. Zeyang Ma

    Department of Biochemistry and Biophysics, Texas A&M University, College Station, United States
    Competing interests
    The authors declare that no competing interests exist.
  6. Tao Hu

    Department of Biochemistry and Biophysics, Texas A&M University, College Station, United States
    Competing interests
    The authors declare that no competing interests exist.
  7. Feng Sun

    Department of Biochemistry and Biophysics, Texas A&M University, College Station, United States
    Competing interests
    The authors declare that no competing interests exist.
  8. Yijun Zhou

    Institute of Plant Protection, Jiangsu Academy of Agricultural Sciences, Nanjing, China
    Competing interests
    The authors declare that no competing interests exist.
  9. Xiu-Jie Wang

    State Key Laboratory of Plant Genomics, Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing, China
    Competing interests
    The authors declare that no competing interests exist.
  10. Xueping Zhou

    Biotechnology Institute, College of Agriculture & Biotechnology, Zhejiang University, Zhejiang, China
    Competing interests
    The authors declare that no competing interests exist.
  11. Xiuren Zhang

    Department of Biochemistry and Biophysics, Texas A&M University, College Station, United States
    For correspondence
    xiuren.zhang@tamu.edu
    Competing interests
    The authors declare that no competing interests exist.

Reviewing Editor

  1. Detlef Weigel, Max Planck Institute for Developmental Biology, Germany

Version history

  1. Received: January 25, 2015
  2. Accepted: September 5, 2015
  3. Accepted Manuscript published: September 7, 2015 (version 1)
  4. Version of Record published: October 16, 2015 (version 2)

Copyright

© 2015, Castillo-González 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. Claudia Castillo-González
  2. Xiuying Liu
  3. Changjun Huang
  4. Changjiang Zhao
  5. Zeyang Ma
  6. Tao Hu
  7. Feng Sun
  8. Yijun Zhou
  9. Xiu-Jie Wang
  10. Xueping Zhou
  11. Xiuren Zhang
(2015)
Geminivirus-encoded TrAP suppressor inhibits the histone methyltransferase SUVH4/KYP to counter host defense
eLife 4:e06671.
https://doi.org/10.7554/eLife.06671

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