Host autophagy machinery is diverted to the pathogen interface to mediate focal defense responses against the Irish potato famine pathogen

  1. Yasin F Dagdas
  2. Pooja Pandey
  3. Yasin Tumtas
  4. Nattapong Sanguankiattichai
  5. Khaoula Belhaj
  6. Cian Duggan
  7. Alexandre Y Leary
  8. Maria Segretin
  9. Mauricio Contreras
  10. Zachary Savage
  11. Virendrasinh S Khandare
  12. Sophien Kamoun  Is a corresponding author
  13. Tolga O Bozkurt  Is a corresponding author
  1. The Sainsbury Laboratory, United Kingdom
  2. Imperial College London, United Kingdom
  3. INGEBI-CONICET, Argentina

Abstract

During plant cell invasion, the oomycete Phytophthora infestans remains enveloped by host-derived membranes whose functional properties are poorly understood. P. infestans secretes a myriad of effector proteins through these interfaces for plant colonization. Recently we showed that the effector protein PexRD54 reprograms host-selective autophagy by antagonising antimicrobial-autophagy receptor Joka2/NBR1 for ATG8CL binding (Dagdas, 2016). Here, we show that during infection, ATG8CL/Joka2 labelled defense-related autophagosomes are diverted toward the perimicrobial host membrane to restrict pathogen growth. PexRD54 also localizes to autophagosomes across the perimicrobial membrane, consistent with the view that the pathogen remodels host-microbe interface by co-opting the host autophagy machinery. Furthermore, we show that the host-pathogen interface is a hotspot for autophagosome biogenesis. Notably, overexpression of the early autophagosome biogenesis protein ATG9 enhances plant immunity. Our results implicate selective autophagy in polarized immune responses of plants and point to more complex functions for autophagy than the widely known degradative roles.

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. Yasin F Dagdas

    The Sainsbury Laboratory, Norwich, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-9502-355X
  2. Pooja Pandey

    Department of Life Sciences, Imperial College London, London, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-3145-7794
  3. Yasin Tumtas

    Department of Life Sciences, Imperial College London, London, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  4. Nattapong Sanguankiattichai

    Department of Life Sciences, Imperial College London, London, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  5. Khaoula Belhaj

    The Sainsbury Laboratory, Norwich, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  6. Cian Duggan

    Department of Life Sciences, Imperial College London, London, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  7. Alexandre Y Leary

    Department of Life Sciences, Imperial College London, London, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-7223-3557
  8. Maria Segretin

    INGEBI-CONICET, Buenos Aires, Argentina
    Competing interests
    The authors declare that no competing interests exist.
  9. Mauricio Contreras

    INGEBI-CONICET, Buenos Aires, Argentina
    Competing interests
    The authors declare that no competing interests exist.
  10. Zachary Savage

    Department of Life Sciences, Imperial College London, London, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  11. Virendrasinh S Khandare

    Department of Life Sciences, Imperial College London, London, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  12. Sophien Kamoun

    The Sainsbury Laboratory, Norwich, United Kingdom
    For correspondence
    sophien.kamoun@tsl.ac.uk
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-0290-0315
  13. Tolga O Bozkurt

    Department of Life Sciences, Imperial College London, London, United Kingdom
    For correspondence
    o.bozkurt@imperial.ac.uk
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-0507-6875

Funding

Gatsby Charitable Foundation

  • Yasin F Dagdas
  • Khaoula Belhaj
  • Sophien Kamoun
  • Tolga O Bozkurt

Biotechnology and Biological Sciences Research Council (BB/M002462/1)

  • Pooja Pandey
  • Yasin Tumtas
  • Nattapong Sanguankiattichai
  • Cian Duggan
  • Alexandre Y Leary
  • Maria Segretin
  • Mauricio Contreras
  • Zachary Savage
  • Tolga O Bozkurt

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: April 16, 2018
  2. Accepted: June 21, 2018
  3. Accepted Manuscript published: June 22, 2018 (version 1)
  4. Version of Record published: July 3, 2018 (version 2)

Copyright

© 2018, Dagdas 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. Yasin F Dagdas
  2. Pooja Pandey
  3. Yasin Tumtas
  4. Nattapong Sanguankiattichai
  5. Khaoula Belhaj
  6. Cian Duggan
  7. Alexandre Y Leary
  8. Maria Segretin
  9. Mauricio Contreras
  10. Zachary Savage
  11. Virendrasinh S Khandare
  12. Sophien Kamoun
  13. Tolga O Bozkurt
(2018)
Host autophagy machinery is diverted to the pathogen interface to mediate focal defense responses against the Irish potato famine pathogen
eLife 7:e37476.
https://doi.org/10.7554/eLife.37476

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