Potato Mop-Top Virus Co-Opts the Stress Sensor HIPP26 for Long-Distance Movement

Plant Physiol. 2018 Mar;176(3):2052-2070. doi: 10.1104/pp.17.01698. Epub 2018 Jan 26.

Abstract

Virus movement proteins facilitate virus entry into the vascular system to initiate systemic infection. The potato mop-top virus (PMTV) movement protein, TGB1, is involved in long-distance movement of both viral ribonucleoprotein complexes and virions. Here, our analysis of TGB1 interactions with host Nicotiana benthamiana proteins revealed an interaction with a member of the heavy metal-associated isoprenylated plant protein family, HIPP26, which acts as a plasma membrane-to-nucleus signal during abiotic stress. We found that knockdown of NbHIPP26 expression inhibited virus long-distance movement but did not affect cell-to-cell movement. Drought and PMTV infection up-regulated NbHIPP26 gene expression, and PMTV infection protected plants from drought. In addition, NbHIPP26 promoter-reporter fusions revealed vascular tissue-specific expression. Mutational and biochemical analyses indicated that NbHIPP26 subcellular localization at the plasma membrane and plasmodesmata was mediated by lipidation (S-acylation and prenylation), as nonlipidated NbHIPP26 was predominantly in the nucleus. Notably, coexpression of NbHIPP26 with TGB1 resulted in a similar nuclear accumulation of NbHIPP26. TGB1 interacted with the carboxyl-terminal CVVM (prenyl) domain of NbHIPP26, and bimolecular fluorescence complementation revealed that the TGB1-HIPP26 complex localized to microtubules and accumulated in the nucleolus, with little signal at the plasma membrane or plasmodesmata. These data support a mechanism where interaction with TGB1 negates or reverses NbHIPP26 lipidation, thus releasing membrane-associated NbHIPP26 and redirecting it via microtubules to the nucleus, thereby activating the drought stress response and facilitating virus long-distance movement.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Acylation
  • Amino Acid Sequence
  • Cell Nucleolus / metabolism
  • Droughts
  • Gene Expression Regulation, Plant
  • Glucuronidase / metabolism
  • Green Fluorescent Proteins / metabolism
  • Lipids / chemistry
  • Models, Biological
  • Phylogeny
  • Plant Diseases / virology
  • Plant Leaves / metabolism
  • Plant Proteins / chemistry
  • Plant Proteins / metabolism*
  • Plant Viral Movement Proteins / metabolism*
  • Plant Viruses / metabolism*
  • Plants, Genetically Modified
  • Protein Binding
  • Stress, Physiological*
  • Subcellular Fractions / metabolism
  • Tobacco / genetics
  • Tobacco / metabolism*
  • Tobacco / virology*
  • Two-Hybrid System Techniques

Substances

  • Lipids
  • Plant Proteins
  • Plant Viral Movement Proteins
  • Green Fluorescent Proteins
  • Glucuronidase

Supplementary concepts

  • Potato mop-top virus