Geminiviruses subvert ubiquitination by altering CSN-mediated derubylation of SCF E3 ligase complexes and inhibit jasmonate signaling in Arabidopsis thaliana

Plant Cell. 2011 Mar;23(3):1014-32. doi: 10.1105/tpc.110.080267. Epub 2011 Mar 25.

Abstract

Viruses must create a suitable cell environment and elude defense mechanisms, which likely involves interactions with host proteins and subsequent interference with or usurpation of cellular machinery. Here, we describe a novel strategy used by plant DNA viruses (Geminiviruses) to redirect ubiquitination by interfering with the activity of the CSN (COP9 signalosome) complex. We show that geminiviral C2 protein interacts with CSN5, and its expression in transgenic plants compromises CSN activity on CUL1. Several responses regulated by the CUL1-based SCF ubiquitin E3 ligases (including responses to jasmonates, auxins, gibberellins, ethylene, and abscisic acid) are altered in these plants. Impairment of SCF function is confirmed by stabilization of yellow fluorescent protein-GAI, a substrate of the SCF(SLY1). Transcriptomic analysis of these transgenic plants highlights the response to jasmonates as the main SCF-dependent process affected by C2. Exogenous jasmonate treatment of Arabidopsis thaliana plants disrupts geminivirus infection, suggesting that the suppression of the jasmonate response might be crucial for infection. Our findings suggest that C2 affects the activity of SCFs, most likely through interference with the CSN. As SCFs are key regulators of many cellular processes, the capability of viruses to selectively interfere with or hijack the activity of these complexes might define a novel and powerful strategy in viral infections.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Acetates / pharmacology*
  • Amino Acids, Cyclic / pharmacology
  • Arabidopsis / drug effects
  • Arabidopsis / genetics
  • Arabidopsis / virology*
  • Arabidopsis Proteins / drug effects
  • Arabidopsis Proteins / metabolism
  • COP9 Signalosome Complex
  • Cullin Proteins / genetics*
  • Cyclopentanes / pharmacology*
  • DNA-Binding Proteins / genetics
  • DNA-Binding Proteins / metabolism
  • Geminiviridae / pathogenicity*
  • Gene Expression Profiling
  • Gene Expression Regulation, Plant
  • Gibberellins / pharmacology
  • Mutation
  • Oxylipins / pharmacology*
  • Phenotype
  • Plant Growth Regulators / pharmacology
  • Plant Roots / growth & development
  • Plants, Genetically Modified / drug effects
  • Plants, Genetically Modified / genetics
  • Plants, Genetically Modified / metabolism
  • Recombinant Fusion Proteins / genetics
  • Ubiquitin-Protein Ligases / drug effects
  • Ubiquitin-Protein Ligases / metabolism
  • Ubiquitination
  • Ubiquitins / metabolism
  • Viral Proteins / genetics
  • Viral Proteins / metabolism

Substances

  • AC2 protein, geminivirus
  • Acetates
  • Amino Acids, Cyclic
  • Arabidopsis Proteins
  • COP9 signalosome subunit 5, Arabidopsis
  • Cullin 1
  • Cullin Proteins
  • Cyclopentanes
  • DNA-Binding Proteins
  • Gibberellins
  • Oxylipins
  • Plant Growth Regulators
  • Recombinant Fusion Proteins
  • Ubiquitins
  • Viral Proteins
  • 1-aminocyclopropane-1-carboxylic acid
  • jasmonic acid
  • methyl jasmonate
  • gibberellic acid
  • Ubiquitin-Protein Ligases
  • COP9 Signalosome Complex

Associated data

  • GEO/GSE24475