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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Main Authors: Michael J Skelly, James J Furniss, Heather Grey, Ka-Wing Wong, Steven H Spoel
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2019-10-01
Series:eLife
Subjects:
Online Access:https://elifesciences.org/articles/47005
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spelling doaj-a4510a21d3f24b12b0e722ffaacc863b2021-05-05T17:58:55ZengeLife Sciences Publications LtdeLife2050-084X2019-10-01810.7554/eLife.47005Dynamic ubiquitination determines transcriptional activity of the plant immune coactivator NPR1Michael J Skelly0https://orcid.org/0000-0002-9024-0037James J Furniss1Heather Grey2Ka-Wing Wong3Steven H Spoel4https://orcid.org/0000-0003-4340-7591Institute of Molecular Plant Sciences, School of Biological Sciences, University of Edinburgh, Edinburgh, United KingdomInstitute of Molecular Plant Sciences, School of Biological Sciences, University of Edinburgh, Edinburgh, United KingdomInstitute of Molecular Plant Sciences, School of Biological Sciences, University of Edinburgh, Edinburgh, United KingdomInstitute of Molecular Plant Sciences, School of Biological Sciences, University of Edinburgh, Edinburgh, United KingdomInstitute of Molecular Plant Sciences, School of Biological Sciences, University of Edinburgh, Edinburgh, United KingdomActivation 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.https://elifesciences.org/articles/47005NPR1salicylic acidsystemic acquired resistanceplant immunityubiquitin
collection DOAJ
language English
format Article
sources DOAJ
author Michael J Skelly
James J Furniss
Heather Grey
Ka-Wing Wong
Steven H Spoel
spellingShingle Michael J Skelly
James J Furniss
Heather Grey
Ka-Wing Wong
Steven H Spoel
Dynamic ubiquitination determines transcriptional activity of the plant immune coactivator NPR1
eLife
NPR1
salicylic acid
systemic acquired resistance
plant immunity
ubiquitin
author_facet Michael J Skelly
James J Furniss
Heather Grey
Ka-Wing Wong
Steven H Spoel
author_sort Michael J Skelly
title 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_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_sort dynamic ubiquitination determines transcriptional activity of the plant immune coactivator npr1
publisher eLife Sciences Publications Ltd
series eLife
issn 2050-084X
publishDate 2019-10-01
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.
topic NPR1
salicylic acid
systemic acquired resistance
plant immunity
ubiquitin
url https://elifesciences.org/articles/47005
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