Potato mop-top virus co-opts the stress sensor HIPP26 for long-distance movement
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.
Citation
Cowan , G H , Roberts , A G , Jones , S , Kumar , P , Kalyandurg , P B , Gil , J F , Savenkov , E I , Hemsley , P A & Torrance , L 2018 , ' Potato mop-top virus co-opts the stress sensor HIPP26 for long-distance movement ' , Plant Physiology , vol. 176 , no. 3 , pp. 2052-2070 . https://doi.org/10.1104/pp.17.01698
Publication
Plant Physiology
Status
Peer reviewed
ISSN
0032-0889Type
Journal article
Rights
Copyright © 2018, American Society of Plant Biologists. This work has been made available online in accordance with the publisher’s policies. This is the author created, accepted version manuscript following peer review and may differ slightly from the final published version. The final published version of this work is available at https://doi.org/10.1104/pp.17.01698
Description
The work of LT, GC, SJ and AR is funded by the Scottish Government’s Rural and Environmental Science and Analytical Services (RESAS) Division, PH by the BBSRC (grant BB/M024911/1) and The Royal Society and EIS by the Swedish Research Council Formas and the Carl Tryggers Foundation.Collections
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