Potato mop-top virus co-opts the stress sensor HIPP26 for long-distance movement

Graham H. Cowan, Alison G. Roberts, Susan Jones, Pankaj Kumar, Pruthvi B. Kalyandurg, Jose F. Gil, Eugene I Savenkov, Piers Hemsley, Lesley Torrance (Lead / Corresponding author)

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Abstract

Virus entry to the vascular system is a vital process in the initiation of a systemic infection. Virus movement proteins (MP) are key to this and the potato mop-top virus (PMTV) MP, TGB1, is involved in long distance movement of both viral ribonucleoprotein complexes and virions. Analysis of TGB1 interactions with host Nicotiana benthamiana proteins revealed a novel interaction with a member of the heavy metal associated isoprenylated plant protein family, HIPP26, thought to act as a plasma membrane to nucleus abiotic stress signalling relay. NbHIPP26 promoter-reporter fusions revealed vascular tissue specific expression with NbHIPP26 gene expression being upregulated by drought and PMTV infection. In addition, PMTV infection protected plants from drought. Knock down of NbHIPP26 expression inhibited virus long distance movement but did not affect cell-to-cell movement. NbHIPP26 localised at the plasma membrane and plasmodesmata. Mutational and biochemical analysis indicated that this localisation was mediated by lipidation (S-acylation and prenylation), as non-lipidated NbHIPP26 was found predominantly in the nucleus. Co-expression of NbHIPP26 with TGB1 resulted in a similar nuclear accumulation of NbHIPP26. TGB1 interacted with the C terminal CVVM (prenyl) domain of NbHIPP26, and bimolecular fluorescence complementation revealed that the TGB1-HIPP26 complex decorated microtubules with strong accumulation in the nucleolus and little signal at the plasma membrane or plasmodesmata. The data support a mechanism where interaction with TGB1 negates or reverses NbHIPP26 lipidation, releasing membrane-associated NbHIPP26 and re-directing it via microtubules to the nucleus thereby activating the drought stress response and facilitating virus long distance movement.

Original languageEnglish
Pages (from-to)2052-2070
Number of pages19
JournalPlant Physiology
Volume176
Issue number2
Early online date26 Jan 2018
DOIs
Publication statusPublished - Mar 2018

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    Cowan, G. H., Roberts, A. G., Jones, S., Kumar, P., Kalyandurg, P. B., Gil, J. F., Savenkov, E. I., Hemsley, P., & Torrance, L. (2018). Potato mop-top virus co-opts the stress sensor HIPP26 for long-distance movement. Plant Physiology, 176(2), 2052-2070. https://doi.org/10.1104/pp.17.01698