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

• Published in: Plant physiology (Bethesda) Vol. 176; no. 3; pp. 2052 - 2070
• Main Authors: Cowan, Graham H., Roberts, Alison G., Jones, Susan, Kumar, Pankaj, Kalyandurg, Pruthvi B., Gil, Jose F., Savenkov, Eugene I., Hemsley, Piers A., Torrance, Lesley
• Format: Journal Article
• Language: English
• Published: United States American Society of Plant Biologists 01.03.2018
• Subjects: Acylation; Amino Acid Sequence; Botanik; Botany; CELL BIOLOGY; Cell Nucleolus - metabolism; Droughts; Gene Expression Regulation, Plant; Glucuronidase - metabolism; Green Fluorescent Proteins - metabolism; Lipids - chemistry; Models, Biological; Nicotiana - genetics; Nicotiana - metabolism; Nicotiana - virology; 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; Two-Hybrid System Techniques
• ISSN: 0032-0889; 1532-2548; 1532-2548
• DOI: 10.1104/pp.17.01698

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.