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

Elife. 2018 Jun 22;7:e37476. doi: 10.7554/eLife.37476.

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 et al., 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.

Keywords: RXLR Effector; autophagosome; cell biology; defense-related autophagy; effector biology; haustoria; nicotiana benthamiana; phytophthora infestans; plant biology; plant immunity; selective autophagy.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • ATPases Associated with Diverse Cellular Activities / genetics
  • ATPases Associated with Diverse Cellular Activities / immunology
  • Autophagosomes / immunology
  • Autophagosomes / parasitology
  • Autophagy / genetics*
  • Autophagy / immunology
  • Autophagy-Related Protein 8 Family / genetics
  • Autophagy-Related Protein 8 Family / immunology
  • Carrier Proteins / genetics
  • Carrier Proteins / immunology
  • Gene Expression Regulation
  • Host-Pathogen Interactions*
  • Membrane Proteins / genetics
  • Membrane Proteins / immunology
  • Phytophthora infestans / genetics*
  • Phytophthora infestans / growth & development
  • Phytophthora infestans / pathogenicity
  • Plant Cells / immunology
  • Plant Cells / parasitology
  • Plant Diseases / genetics*
  • Plant Diseases / immunology
  • Plant Diseases / parasitology
  • Plant Immunity / genetics
  • Plant Proteins / genetics*
  • Plant Proteins / immunology
  • Protein Binding
  • Signal Transduction
  • Solanum tuberosum / genetics*
  • Solanum tuberosum / immunology
  • Solanum tuberosum / parasitology

Substances

  • Autophagy-Related Protein 8 Family
  • Carrier Proteins
  • Membrane Proteins
  • Plant Proteins
  • ATPases Associated with Diverse Cellular Activities