A Phytophthora effector recruits a host cytoplasmic transacetylase into nuclear speckles to enhance plant susceptibility

Abstract

Oomycete pathogens secrete host cell-entering effector proteins to manipulate host immunity during infection. We previously showed that PsAvh52, an early-induced RxLR effector secreted from the soybean root rot pathogen, Phytophthora sojae, could suppress plant immunity. Here, we found that PsAvh52 is required for full virulence on soybean and binds to a novel soybean transacetylase, GmTAP1, in vivo and in vitro. PsAvh52 could cause GmTAP1 to relocate into the nucleus where GmTAP1 could acetylate histones H2A and H3 during early infection, thereby promoting susceptibility to P. sojae. In the absence of PsAvh52, GmTAP1 remained confined to the cytoplasm and did not modify plant susceptibility. These results demonstrate that GmTAP1 is a susceptibility factor that is hijacked by PsAvh52 in order to promote epigenetic modifications that enhance the susceptibility of soybean to P. sojae infection.

Data availability

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

Article and author information

Author details

  1. Haiyang Li

    Department of Plant Pathology, Nanjing Agriculture University, Nanjing, China
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-8205-4875
  2. Haonan Wang

    Department of Plant Pathology, Nanjing Agriculture University, Nanjing, China
    Competing interests
    The authors declare that no competing interests exist.
  3. Maofeng Jing

    Department of Plant Pathology, Nanjing Agriculture University, Nanjing, China
    Competing interests
    The authors declare that no competing interests exist.
  4. Jinyi Zhu

    Department of Plant Pathology, Nanjing Agriculture University, Nanjing, China
    Competing interests
    The authors declare that no competing interests exist.
  5. Baodian Guo

    Department of Plant Pathology, Nanjing Agriculture University, Nanjing, China
    Competing interests
    The authors declare that no competing interests exist.
  6. Yang Wang

    Department of Plant Pathology, Nanjing Agriculture University, Nanjing, China
    Competing interests
    The authors declare that no competing interests exist.
  7. Yachun Lin

    Department of Plant Pathology, Nanjing Agriculture University, Nanjing, China
    Competing interests
    The authors declare that no competing interests exist.
  8. Han Chen

    Department of Plant Pathology, Nanjing Agriculture University, Nanjing, China
    Competing interests
    The authors declare that no competing interests exist.
  9. Liang Kong

    Department of Plant Pathology, Nanjing Agriculture University, Nanjing, China
    Competing interests
    The authors declare that no competing interests exist.
  10. Zhenchuan Ma

    Department of Plant Pathology, Nanjing Agriculture University, Nanjing, China
    Competing interests
    The authors declare that no competing interests exist.
  11. Yan Wang

    Department of Plant Pathology, Nanjing Agriculture University, Nanjing, China
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-7465-5518
  12. Wenwu Ye

    Department of Plant Pathology, Nanjing Agriculture University, Nanjing, China
    Competing interests
    The authors declare that no competing interests exist.
  13. Suomeng Dong

    Department of Plant Pathology, Nanjing Agriculture University, Nanjing, China
    Competing interests
    The authors declare that no competing interests exist.
  14. Brett M Tyler

    Center for Genome Research and Biocomputing, Oregon State University, Corvallis, United States
    Competing interests
    The authors declare that no competing interests exist.
  15. Yuanchao Wang

    Department of Plant Pathology, Nanjing Agriculture University, Nanjing, China
    For correspondence
    wangyc@njau.edu.cn
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-5803-5343

Funding

Creative Research Groups of the National Natural Science Foundation of China (31721004)

  • Yuanchao Wang

The Special Fund for Agro-scientific Research in the Public Interest (201303018)

  • Yuanchao Wang

The China Agriculture Research System (CARS-004-PS14)

  • Yuanchao Wang

The Key Programme of the National Natural Science Foundation of China (31430073)

  • Yuanchao Wang

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

Copyright

© 2018, 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.

Metrics

  • 4,396
    views
  • 1,032
    downloads
  • 58
    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. Haiyang Li
  2. Haonan Wang
  3. Maofeng Jing
  4. Jinyi Zhu
  5. Baodian Guo
  6. Yang Wang
  7. Yachun Lin
  8. Han Chen
  9. Liang Kong
  10. Zhenchuan Ma
  11. Yan Wang
  12. Wenwu Ye
  13. Suomeng Dong
  14. Brett M Tyler
  15. Yuanchao Wang
(2018)
A Phytophthora effector recruits a host cytoplasmic transacetylase into nuclear speckles to enhance plant susceptibility
eLife 7:e40039.
https://doi.org/10.7554/eLife.40039

Share this article

https://doi.org/10.7554/eLife.40039

Further reading

    1. Ecology
    2. Microbiology and Infectious Disease
    Tom Clegg, Samraat Pawar
    Research Article Updated

    Predicting how species diversity changes along environmental gradients is an enduring problem in ecology. In microbes, current theories tend to invoke energy availability and enzyme kinetics as the main drivers of temperature-richness relationships. Here, we derive a general empirically-grounded theory that can explain this phenomenon by linking microbial species richness in competitive communities to variation in the temperature-dependence of their interaction and growth rates. Specifically, the shape of the microbial community temperature-richness relationship depends on how rapidly the strength of effective competition between species pairs changes with temperature relative to the variance of their growth rates. Furthermore, it predicts that a thermal specialist-generalist tradeoff in growth rates alters coexistence by shifting this balance, causing richness to peak at relatively higher temperatures. Finally, we show that the observed patterns of variation in thermal performance curves of metabolic traits across extant bacterial taxa is indeed sufficient to generate the variety of community-level temperature-richness responses observed in the real world. Our results provide a new and general mechanism that can help explain temperature-diversity gradients in microbial communities, and provide a quantitative framework for interlinking variation in the thermal physiology of microbial species to their community-level diversity.

    1. Cell Biology
    2. Microbiology and Infectious Disease
    Clément Mazeaud, Stefan Pfister ... Laurent Chatel-Chaix
    Research Article

    Zika virus (ZIKV) infection causes significant human disease that, with no approved treatment or vaccine, constitutes a major public health concern. Its life cycle entirely relies on the cytoplasmic fate of the viral RNA genome (vRNA) through a fine-tuned equilibrium between vRNA translation, replication, and packaging into new virions, all within virus-induced replication organelles (vROs). In this study, with an RNA interference (RNAi) mini-screening and subsequent functional characterization, we have identified insulin-like growth factor 2 mRNA-binding protein 2 (IGF2BP2) as a new host dependency factor that regulates vRNA synthesis. In infected cells, IGF2BP2 associates with viral NS5 polymerase and redistributes to the perinuclear viral replication compartment. Combined fluorescence in situ hybridization-based confocal imaging, in vitro binding assays, and immunoprecipitation coupled to RT-qPCR showed that IGF2BP2 directly interacts with ZIKV vRNA 3’ nontranslated region. Using ZIKV sub-genomic replicons and a replication-independent vRO induction system, we demonstrated that IGF2BP2 knockdown impairs de novo vRO biogenesis and, consistently, vRNA synthesis. Finally, the analysis of immunopurified IGF2BP2 complex using quantitative mass spectrometry and RT-qPCR revealed that ZIKV infection alters the protein and RNA interactomes of IGF2BP2. Altogether, our data support that ZIKV hijacks and remodels the IGF2BP2 ribonucleoprotein complex to regulate vRO biogenesis and vRNA neosynthesis.