Selective Autophagy Limits Cauliflower Mosaic Virus Infection by NBR1-mediated Targeting of Viral Capsid Protein and Particles

Proc Natl Acad Sci U S A. 2017 Mar 7;114(10):E2026-E2035. doi: 10.1073/pnas.1610687114. Epub 2017 Feb 21.

Abstract

Autophagy plays a paramount role in mammalian antiviral immunity including direct targeting of viruses and their individual components, and many viruses have evolved measures to antagonize or even exploit autophagy mechanisms for the benefit of infection. In plants, however, the functions of autophagy in host immunity and viral pathogenesis are poorly understood. In this study, we have identified both anti- and proviral roles of autophagy in the compatible interaction of cauliflower mosaic virus (CaMV), a double-stranded DNA pararetrovirus, with the model plant Arabidopsis thaliana We show that the autophagy cargo receptor NEIGHBOR OF BRCA1 (NBR1) targets nonassembled and virus particle-forming capsid proteins to mediate their autophagy-dependent degradation, thereby restricting the establishment of CaMV infection. Intriguingly, the CaMV-induced virus factory inclusions seem to protect against autophagic destruction by sequestering capsid proteins and coordinating particle assembly and storage. In addition, we found that virus-triggered autophagy prevents extensive senescence and tissue death of infected plants in a largely NBR1-independent manner. This survival function significantly extends the timespan of virus production, thereby increasing the chances for virus particle acquisition by aphid vectors and CaMV transmission. Together, our results provide evidence for the integration of selective autophagy into plant immunity against viruses and reveal potential viral strategies to evade and adapt autophagic processes for successful pathogenesis.

Keywords: cauliflower mosaic virus; innate immunity; plant virus; selective autophagy; xenophagy.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Aphids / virology
  • Arabidopsis / genetics*
  • Arabidopsis / immunology
  • Arabidopsis / virology
  • Arabidopsis Proteins / genetics*
  • Arabidopsis Proteins / immunology
  • Autophagy / genetics
  • Autophagy / immunology*
  • Capsid / chemistry
  • Capsid / metabolism
  • Capsid Proteins / genetics
  • Capsid Proteins / metabolism
  • Carrier Proteins / genetics*
  • Carrier Proteins / immunology
  • Caulimovirus / genetics
  • Caulimovirus / growth & development
  • Gene Expression Regulation, Plant*
  • Host-Pathogen Interactions
  • Plant Diseases / genetics*
  • Plant Diseases / immunology
  • Plant Diseases / virology
  • Plant Immunity / genetics*
  • Proteolysis
  • Signal Transduction
  • Virion / genetics
  • Virion / growth & development

Substances

  • Arabidopsis Proteins
  • Capsid Proteins
  • Carrier Proteins
  • NBR1 protein, Arabidopsis