Potato Mop-Top Virus Co-Opts the Stress Sensor HIPP26 for Long-Distance Movement1[OPEN]

• Published in: Plant physiology (Bethesda) 2018-01, Vol.176 (3), p.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: Article
• Language: English
• Subjects: Cell Biology
• ISSN: 0032-0889; 1532-2548
• DOI: 10.1104/pp.17.01698

After a virus movement protein interacts with the HIPP26 stress sensor, the complex relocalizes to the nucleus, activating the drought stress response and thereby facilitating virus long-distance movement. 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.