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.

Metrics

  • 4,251
    views
  • 1,037
    downloads
  • 88
    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. 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

Share this article

https://doi.org/10.7554/eLife.06671

Further reading

    1. Chromosomes and Gene Expression
    2. Immunology and Inflammation
    Rajan M Thomas, Matthew C Pahl ... Andrew D Wells
    Research Article

    Ikaros is a transcriptional factor required for conventional T cell development, differentiation, and anergy. While the related factors Helios and Eos have defined roles in regulatory T cells (Treg), a role for Ikaros has not been established. To determine the function of Ikaros in the Treg lineage, we generated mice with Treg-specific deletion of the Ikaros gene (Ikzf1). We find that Ikaros cooperates with Foxp3 to establish a major portion of the Treg epigenome and transcriptome. Ikaros-deficient Treg exhibit Th1-like gene expression with abnormal production of IL-2, IFNg, TNFa, and factors involved in Wnt and Notch signaling. While Ikzf1-Treg-cko mice do not develop spontaneous autoimmunity, Ikaros-deficient Treg are unable to control conventional T cell-mediated immune pathology in response to TCR and inflammatory stimuli in models of IBD and organ transplantation. These studies establish Ikaros as a core factor required in Treg for tolerance and the control of inflammatory immune responses.

    1. Cell Biology
    2. Chromosomes and Gene Expression
    Lucie Crhak Khaitova, Pavlina Mikulkova ... Karel Riha
    Research Article

    Heat stress is a major threat to global crop production, and understanding its impact on plant fertility is crucial for developing climate-resilient crops. Despite the known negative effects of heat stress on plant reproduction, the underlying molecular mechanisms remain poorly understood. Here, we investigated the impact of elevated temperature on centromere structure and chromosome segregation during meiosis in Arabidopsis thaliana. Consistent with previous studies, heat stress leads to a decline in fertility and micronuclei formation in pollen mother cells. Our results reveal that elevated temperature causes a decrease in the amount of centromeric histone and the kinetochore protein BMF1 at meiotic centromeres with increasing temperature. Furthermore, we show that heat stress increases the duration of meiotic divisions and prolongs the activity of the spindle assembly checkpoint during meiosis I, indicating an impaired efficiency of the kinetochore attachments to spindle microtubules. Our analysis of mutants with reduced levels of centromeric histone suggests that weakened centromeres sensitize plants to elevated temperature, resulting in meiotic defects and reduced fertility even at moderate temperatures. These results indicate that the structure and functionality of meiotic centromeres in Arabidopsis are highly sensitive to heat stress, and suggest that centromeres and kinetochores may represent a critical bottleneck in plant adaptation to increasing temperatures.