NIK1-mediated translation suppression functions as a plant antiviral immunity mechanism

Nature. 2015 Apr 30;520(7549):679-82. doi: 10.1038/nature14171. Epub 2015 Feb 23.

Abstract

Plants and plant pathogens are subject to continuous co-evolutionary pressure for dominance, and the outcomes of these interactions can substantially impact agriculture and food security. In virus-plant interactions, one of the major mechanisms for plant antiviral immunity relies on RNA silencing, which is often suppressed by co-evolving virus suppressors, thus enhancing viral pathogenicity in susceptible hosts. In addition, plants use the nucleotide-binding and leucine-rich repeat (NB-LRR) domain-containing resistance proteins, which recognize viral effectors to activate effector-triggered immunity in a defence mechanism similar to that employed in non-viral infections. Unlike most eukaryotic organisms, plants are not known to activate mechanisms of host global translation suppression to fight viruses. Here we demonstrate in Arabidopsis that the constitutive activation of NIK1, a leucine-rich repeat receptor-like kinase (LRR-RLK) identified as a virulence target of the begomovirus nuclear shuttle protein (NSP), leads to global translation suppression and translocation of the downstream component RPL10 to the nucleus, where it interacts with a newly identified MYB-like protein, L10-INTERACTING MYB DOMAIN-CONTAINING PROTEIN (LIMYB), to downregulate translational machinery genes fully. LIMYB overexpression represses ribosomal protein genes at the transcriptional level, resulting in protein synthesis inhibition, decreased viral messenger RNA association with polysome fractions and enhanced tolerance to begomovirus. By contrast, the loss of LIMYB function releases the repression of translation-related genes and increases susceptibility to virus infection. Therefore, LIMYB links immune receptor LRR-RLK activation to global translation suppression as an antiviral immunity strategy in plants.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Active Transport, Cell Nucleus
  • Arabidopsis / immunology*
  • Arabidopsis / virology*
  • Arabidopsis Proteins / metabolism*
  • Begomovirus / immunology*
  • Cell Nucleus / metabolism
  • Down-Regulation
  • Gene Expression Regulation, Plant
  • Immune Tolerance
  • Immunity, Innate*
  • Plant Immunity*
  • Protein Binding
  • Protein Biosynthesis / genetics
  • Protein Biosynthesis / immunology*
  • Protein-Serine-Threonine Kinases / metabolism*
  • Ribosomal Protein L10
  • Ribosomal Proteins / metabolism
  • Transcription Factors / metabolism

Substances

  • Arabidopsis Proteins
  • Ribosomal Proteins
  • Transcription Factors
  • ribosomal protein L10, Arabidopsis
  • NIK1 protein, Arabidopsis
  • Protein-Serine-Threonine Kinases

Associated data

  • GEO/GSE56922