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Proteasome-associated HECT-type ubiquitin ligase activity is required for plant immunity

Regulated degradation of proteins by the 26S proteasome plays important roles in maintenance and signalling in eukaryotic cells. Proteins are marked for degradation by the action of E3 ligases that site-specifically modify their substrates by adding chains of ubiquitin. Innate immune signalling in p...

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Autores principales: Furniss, James J., Grey, Heather, Wang, Zhishuo, Nomoto, Mika, Jackson, Lorna, Tada, Yasuomi, Spoel, Steven H.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2018
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6286022/
https://www.ncbi.nlm.nih.gov/pubmed/30458055
http://dx.doi.org/10.1371/journal.ppat.1007447
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author Furniss, James J.
Grey, Heather
Wang, Zhishuo
Nomoto, Mika
Jackson, Lorna
Tada, Yasuomi
Spoel, Steven H.
author_facet Furniss, James J.
Grey, Heather
Wang, Zhishuo
Nomoto, Mika
Jackson, Lorna
Tada, Yasuomi
Spoel, Steven H.
author_sort Furniss, James J.
collection PubMed
description Regulated degradation of proteins by the 26S proteasome plays important roles in maintenance and signalling in eukaryotic cells. Proteins are marked for degradation by the action of E3 ligases that site-specifically modify their substrates by adding chains of ubiquitin. Innate immune signalling in plants is deeply reliant on the ubiquitin-26S proteasome system. While progress has been made in understanding substrate ubiquitination during plant immunity, how these substrates are processed upon arrival at the proteasome remains unclear. Here we show that specific members of the HECT domain-containing family of ubiquitin protein ligases (UPL) play important roles in proteasomal substrate processing during plant immunity. Mutations in UPL1, UPL3 and UPL5 significantly diminished immune responses activated by the immune hormone salicylic acid (SA). In depth analyses of upl3 mutants indicated that these plants were impaired in reprogramming of nearly the entire SA-induced transcriptome and failed to establish immunity against a hemi-biotrophic pathogen. UPL3 was found to physically interact with the regulatory particle of the proteasome and with other ubiquitin-26S proteasome pathway components. In agreement, we demonstrate that UPL3 enabled proteasomes to form polyubiquitin chains, thereby regulating total cellular polyubiquitination levels. Taken together, our findings suggest that proteasome-associated ubiquitin ligase activity of UPL3 promotes proteasomal processivity and is indispensable for development of plant immunity.
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spelling pubmed-62860222018-12-28 Proteasome-associated HECT-type ubiquitin ligase activity is required for plant immunity Furniss, James J. Grey, Heather Wang, Zhishuo Nomoto, Mika Jackson, Lorna Tada, Yasuomi Spoel, Steven H. PLoS Pathog Research Article Regulated degradation of proteins by the 26S proteasome plays important roles in maintenance and signalling in eukaryotic cells. Proteins are marked for degradation by the action of E3 ligases that site-specifically modify their substrates by adding chains of ubiquitin. Innate immune signalling in plants is deeply reliant on the ubiquitin-26S proteasome system. While progress has been made in understanding substrate ubiquitination during plant immunity, how these substrates are processed upon arrival at the proteasome remains unclear. Here we show that specific members of the HECT domain-containing family of ubiquitin protein ligases (UPL) play important roles in proteasomal substrate processing during plant immunity. Mutations in UPL1, UPL3 and UPL5 significantly diminished immune responses activated by the immune hormone salicylic acid (SA). In depth analyses of upl3 mutants indicated that these plants were impaired in reprogramming of nearly the entire SA-induced transcriptome and failed to establish immunity against a hemi-biotrophic pathogen. UPL3 was found to physically interact with the regulatory particle of the proteasome and with other ubiquitin-26S proteasome pathway components. In agreement, we demonstrate that UPL3 enabled proteasomes to form polyubiquitin chains, thereby regulating total cellular polyubiquitination levels. Taken together, our findings suggest that proteasome-associated ubiquitin ligase activity of UPL3 promotes proteasomal processivity and is indispensable for development of plant immunity. Public Library of Science 2018-11-20 /pmc/articles/PMC6286022/ /pubmed/30458055 http://dx.doi.org/10.1371/journal.ppat.1007447 Text en © 2018 Furniss et al http://creativecommons.org/licenses/by/4.0/ This is an open access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
Furniss, James J.
Grey, Heather
Wang, Zhishuo
Nomoto, Mika
Jackson, Lorna
Tada, Yasuomi
Spoel, Steven H.
Proteasome-associated HECT-type ubiquitin ligase activity is required for plant immunity
title Proteasome-associated HECT-type ubiquitin ligase activity is required for plant immunity
title_full Proteasome-associated HECT-type ubiquitin ligase activity is required for plant immunity
title_fullStr Proteasome-associated HECT-type ubiquitin ligase activity is required for plant immunity
title_full_unstemmed Proteasome-associated HECT-type ubiquitin ligase activity is required for plant immunity
title_short Proteasome-associated HECT-type ubiquitin ligase activity is required for plant immunity
title_sort proteasome-associated hect-type ubiquitin ligase activity is required for plant immunity
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6286022/
https://www.ncbi.nlm.nih.gov/pubmed/30458055
http://dx.doi.org/10.1371/journal.ppat.1007447
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