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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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 |
work_keys_str_mv |
AT michaeljskelly dynamicubiquitinationdeterminestranscriptionalactivityoftheplantimmunecoactivatornpr1 AT jamesjfurniss dynamicubiquitinationdeterminestranscriptionalactivityoftheplantimmunecoactivatornpr1 AT heathergrey dynamicubiquitinationdeterminestranscriptionalactivityoftheplantimmunecoactivatornpr1 AT kawingwong dynamicubiquitinationdeterminestranscriptionalactivityoftheplantimmunecoactivatornpr1 AT stevenhspoel dynamicubiquitinationdeterminestranscriptionalactivityoftheplantimmunecoactivatornpr1 |
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