Geminivirus Activates ASYMMETRIC LEAVES 2 to Accelerate Cytoplasmic DCP2-Mediated mRNA Turnover and Weakens RNA Silencing in Arabidopsis

PLoS Pathog. 2015 Oct 2;11(10):e1005196. doi: 10.1371/journal.ppat.1005196. eCollection 2015 Oct.

Abstract

Aberrant viral RNAs produced in infected plant cells serve as templates for the synthesis of dsRNAs. The derived virus-related small interfering RNAs (siRNA) mediate cleavage of viral RNAs by post-transcriptional gene silencing (PTGS), thus blocking virus multiplication. Here, we identified ASYMMETRIC LEAVES2 (AS2) as a new component of plant P body complex which mediates mRNA decapping and degradation. We found that AS2 promotes DCP2 decapping activity, accelerates mRNA turnover rate, inhibits siRNA accumulation and functions as an endogenous suppressor of PTGS. Consistent with these findings, as2 mutant plants are resistant to virus infection whereas AS2 over-expression plants are hypersensitive. The geminivirus nuclear shuttle protein BV1 protein, which shuttles between nuclei and cytoplasm, induces AS2 expression, causes nuclear exit of AS2 to activate DCP2 decapping activity and renders infected plants more sensitive to viruses. These principles of gene induction and shuttling of induced proteins to promote mRNA decapping in the cytosol may be used by viral pathogens to weaken antiviral defenses in host plants.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Arabidopsis
  • Arabidopsis Proteins / genetics
  • Arabidopsis Proteins / metabolism*
  • Chromatin Immunoprecipitation
  • Cytoplasm / metabolism
  • Endoribonucleases / genetics
  • Endoribonucleases / metabolism*
  • Geminiviridae
  • Gene Expression Regulation, Plant / physiology*
  • Host-Parasite Interactions / physiology*
  • Immunoblotting
  • Plant Diseases / genetics*
  • Plant Diseases / immunology
  • Plant Immunity / physiology*
  • Plants, Genetically Modified
  • Polymerase Chain Reaction
  • RNA, Messenger
  • RNA, Small Interfering / genetics
  • Real-Time Polymerase Chain Reaction
  • Transcription Factors / genetics
  • Transcription Factors / metabolism*

Substances

  • AS2 protein, Arabidopsis
  • Arabidopsis Proteins
  • RNA, Messenger
  • RNA, Small Interfering
  • Transcription Factors
  • Endoribonucleases
  • Dcp2 protein, Arabidopsis

Grant support

The study was supported by the Chinese Academy of Sciences (Strategic Priority Research Program Grant NO. XDB11040300), Natural Science Foundation of China, NSFC31522046 and the Singapore National Research Foundation (CRP Award No. NRF-CRP8-2011-02) to JYe, and by grants from Singapore Millennium Foundation, the Cooperative Research Program for Agricultural Science and Technology Development (PJ906910), Rural Development Administration, Republic of Korea, and funding from Temasek Life Sciences Laboratory to NHC. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.