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Dynamic ubiquitination determines transcriptional activity of the plant immune coactivator NPR1

Activation of systemic acquired resistance in plants is associated with transcriptome reprogramming induced by the unstable coactivator NPR1. Immune-induced ubiquitination and proteasomal degradation of NPR1 are thought to facilitate continuous delivery of active NPR1 to target promoters, thereby ma...

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Autores principales: Skelly, Michael J, Furniss, James J, Grey, Heather, Wong, Ka-Wing, Spoel, Steven H
Formato: Online Artículo Texto
Lenguaje:English
Publicado: eLife Sciences Publications, Ltd 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6850887/
https://www.ncbi.nlm.nih.gov/pubmed/31589140
http://dx.doi.org/10.7554/eLife.47005
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author Skelly, Michael J
Furniss, James J
Grey, Heather
Wong, Ka-Wing
Spoel, Steven H
author_facet Skelly, Michael J
Furniss, James J
Grey, Heather
Wong, Ka-Wing
Spoel, Steven H
author_sort Skelly, Michael J
collection PubMed
description Activation of systemic acquired resistance in plants is associated with transcriptome reprogramming induced by the unstable coactivator NPR1. Immune-induced ubiquitination and proteasomal degradation of NPR1 are thought to facilitate continuous delivery of active NPR1 to target promoters, thereby maximising gene expression. Because of this potentially costly sacrificial process, we investigated if ubiquitination of NPR1 plays transcriptional roles prior to its proteasomal turnover. Here we show ubiquitination of NPR1 is a progressive event in which initial modification by a Cullin-RING E3 ligase promotes its chromatin association and expression of target genes. Only when polyubiquitination of NPR1 is enhanced by the E4 ligase, UBE4, it is targeted for proteasomal degradation. Conversely, ubiquitin ligase activities are opposed by UBP6/7, two proteasome-associated deubiquitinases that enhance NPR1 longevity. Thus, immune-induced transcriptome reprogramming requires sequential actions of E3 and E4 ligases balanced by opposing deubiquitinases that fine-tune activity of NPR1 without strict requirement for its sacrificial turnover.
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spelling pubmed-68508872019-11-14 Dynamic ubiquitination determines transcriptional activity of the plant immune coactivator NPR1 Skelly, Michael J Furniss, James J Grey, Heather Wong, Ka-Wing Spoel, Steven H eLife Plant Biology Activation of systemic acquired resistance in plants is associated with transcriptome reprogramming induced by the unstable coactivator NPR1. Immune-induced ubiquitination and proteasomal degradation of NPR1 are thought to facilitate continuous delivery of active NPR1 to target promoters, thereby maximising gene expression. Because of this potentially costly sacrificial process, we investigated if ubiquitination of NPR1 plays transcriptional roles prior to its proteasomal turnover. Here we show ubiquitination of NPR1 is a progressive event in which initial modification by a Cullin-RING E3 ligase promotes its chromatin association and expression of target genes. Only when polyubiquitination of NPR1 is enhanced by the E4 ligase, UBE4, it is targeted for proteasomal degradation. Conversely, ubiquitin ligase activities are opposed by UBP6/7, two proteasome-associated deubiquitinases that enhance NPR1 longevity. Thus, immune-induced transcriptome reprogramming requires sequential actions of E3 and E4 ligases balanced by opposing deubiquitinases that fine-tune activity of NPR1 without strict requirement for its sacrificial turnover. eLife Sciences Publications, Ltd 2019-10-07 /pmc/articles/PMC6850887/ /pubmed/31589140 http://dx.doi.org/10.7554/eLife.47005 Text en © 2019, Skelly et al http://creativecommons.org/licenses/by/4.0/ http://creativecommons.org/licenses/by/4.0/This article is distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use and redistribution provided that the original author and source are credited.
spellingShingle Plant Biology
Skelly, Michael J
Furniss, James J
Grey, Heather
Wong, Ka-Wing
Spoel, Steven H
Dynamic ubiquitination determines transcriptional activity of the plant immune coactivator NPR1
title Dynamic ubiquitination determines transcriptional activity of the plant immune coactivator NPR1
title_full Dynamic ubiquitination determines transcriptional activity of the plant immune coactivator NPR1
title_fullStr Dynamic ubiquitination determines transcriptional activity of the plant immune coactivator NPR1
title_full_unstemmed Dynamic ubiquitination determines transcriptional activity of the plant immune coactivator NPR1
title_short Dynamic ubiquitination determines transcriptional activity of the plant immune coactivator NPR1
title_sort dynamic ubiquitination determines transcriptional activity of the plant immune coactivator npr1
topic Plant Biology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6850887/
https://www.ncbi.nlm.nih.gov/pubmed/31589140
http://dx.doi.org/10.7554/eLife.47005
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