Cargando…

Interference with plastome gene expression and Clp protease activity in Arabidopsis triggers a chloroplast unfolded protein response to restore protein homeostasis

Disruption of protein homeostasis in chloroplasts impairs the correct functioning of essential metabolic pathways, including the methylerythritol 4-phosphate (MEP) pathway for the production of plastidial isoprenoids involved in photosynthesis and growth. We previously found that misfolded and aggre...

Descripción completa

Detalles Bibliográficos
Autores principales: Llamas, Ernesto, Pulido, Pablo, Rodriguez-Concepcion, Manuel
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2017
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5627961/
https://www.ncbi.nlm.nih.gov/pubmed/28937985
http://dx.doi.org/10.1371/journal.pgen.1007022
_version_ 1783268807100334080
author Llamas, Ernesto
Pulido, Pablo
Rodriguez-Concepcion, Manuel
author_facet Llamas, Ernesto
Pulido, Pablo
Rodriguez-Concepcion, Manuel
author_sort Llamas, Ernesto
collection PubMed
description Disruption of protein homeostasis in chloroplasts impairs the correct functioning of essential metabolic pathways, including the methylerythritol 4-phosphate (MEP) pathway for the production of plastidial isoprenoids involved in photosynthesis and growth. We previously found that misfolded and aggregated forms of the first enzyme of the MEP pathway are degraded by the Clp protease with the involvement of Hsp70 and Hsp100/ClpC1 chaperones in Arabidopsis thaliana. By contrast, the combined unfolding and disaggregating actions of Hsp70 and Hsp100/ClpB3 chaperones allow solubilization and hence reactivation of the enzyme. The repair pathway is promoted when the levels of ClpB3 proteins increase upon reduction of Clp protease activity in mutants or wild-type plants treated with the chloroplast protein synthesis inhibitor lincomycin (LIN). Here we show that LIN treatment rapidly increases the levels of aggregated proteins in the chloroplast, unleashing a specific retrograde signaling pathway that up-regulates expression of ClpB3 and other nuclear genes encoding plastidial chaperones. As a consequence, folding capacity is increased to restore protein homeostasis. This sort of chloroplast unfolded protein response (cpUPR) mechanism appears to be mediated by the heat shock transcription factor HsfA2. Expression of HsfA2 and cpUPR-related target genes is independent of GUN1, a central integrator of retrograde signaling pathways. However, double mutants defective in both GUN1 and plastome gene expression (or Clp protease activity) are seedling lethal, confirming that the GUN1 protein is essential for protein homeostasis in chloroplasts.
format Online
Article
Text
id pubmed-5627961
institution National Center for Biotechnology Information
language English
publishDate 2017
publisher Public Library of Science
record_format MEDLINE/PubMed
spelling pubmed-56279612017-10-20 Interference with plastome gene expression and Clp protease activity in Arabidopsis triggers a chloroplast unfolded protein response to restore protein homeostasis Llamas, Ernesto Pulido, Pablo Rodriguez-Concepcion, Manuel PLoS Genet Research Article Disruption of protein homeostasis in chloroplasts impairs the correct functioning of essential metabolic pathways, including the methylerythritol 4-phosphate (MEP) pathway for the production of plastidial isoprenoids involved in photosynthesis and growth. We previously found that misfolded and aggregated forms of the first enzyme of the MEP pathway are degraded by the Clp protease with the involvement of Hsp70 and Hsp100/ClpC1 chaperones in Arabidopsis thaliana. By contrast, the combined unfolding and disaggregating actions of Hsp70 and Hsp100/ClpB3 chaperones allow solubilization and hence reactivation of the enzyme. The repair pathway is promoted when the levels of ClpB3 proteins increase upon reduction of Clp protease activity in mutants or wild-type plants treated with the chloroplast protein synthesis inhibitor lincomycin (LIN). Here we show that LIN treatment rapidly increases the levels of aggregated proteins in the chloroplast, unleashing a specific retrograde signaling pathway that up-regulates expression of ClpB3 and other nuclear genes encoding plastidial chaperones. As a consequence, folding capacity is increased to restore protein homeostasis. This sort of chloroplast unfolded protein response (cpUPR) mechanism appears to be mediated by the heat shock transcription factor HsfA2. Expression of HsfA2 and cpUPR-related target genes is independent of GUN1, a central integrator of retrograde signaling pathways. However, double mutants defective in both GUN1 and plastome gene expression (or Clp protease activity) are seedling lethal, confirming that the GUN1 protein is essential for protein homeostasis in chloroplasts. Public Library of Science 2017-09-22 /pmc/articles/PMC5627961/ /pubmed/28937985 http://dx.doi.org/10.1371/journal.pgen.1007022 Text en © 2017 Llamas 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
Llamas, Ernesto
Pulido, Pablo
Rodriguez-Concepcion, Manuel
Interference with plastome gene expression and Clp protease activity in Arabidopsis triggers a chloroplast unfolded protein response to restore protein homeostasis
title Interference with plastome gene expression and Clp protease activity in Arabidopsis triggers a chloroplast unfolded protein response to restore protein homeostasis
title_full Interference with plastome gene expression and Clp protease activity in Arabidopsis triggers a chloroplast unfolded protein response to restore protein homeostasis
title_fullStr Interference with plastome gene expression and Clp protease activity in Arabidopsis triggers a chloroplast unfolded protein response to restore protein homeostasis
title_full_unstemmed Interference with plastome gene expression and Clp protease activity in Arabidopsis triggers a chloroplast unfolded protein response to restore protein homeostasis
title_short Interference with plastome gene expression and Clp protease activity in Arabidopsis triggers a chloroplast unfolded protein response to restore protein homeostasis
title_sort interference with plastome gene expression and clp protease activity in arabidopsis triggers a chloroplast unfolded protein response to restore protein homeostasis
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5627961/
https://www.ncbi.nlm.nih.gov/pubmed/28937985
http://dx.doi.org/10.1371/journal.pgen.1007022
work_keys_str_mv AT llamasernesto interferencewithplastomegeneexpressionandclpproteaseactivityinarabidopsistriggersachloroplastunfoldedproteinresponsetorestoreproteinhomeostasis
AT pulidopablo interferencewithplastomegeneexpressionandclpproteaseactivityinarabidopsistriggersachloroplastunfoldedproteinresponsetorestoreproteinhomeostasis
AT rodriguezconcepcionmanuel interferencewithplastomegeneexpressionandclpproteaseactivityinarabidopsistriggersachloroplastunfoldedproteinresponsetorestoreproteinhomeostasis