Heat Shock Factor HSFA6b Mediates Mitochondrial Unfolded Protein Response in <i>Arabidopsis thaliana</i>

Mitochondria are important organelles in eukaryotes and are involved in various metabolic processes. Mitochondrial proteotoxic stress triggers the mitochondrial unfolded protein response (UPR<sup>mt</sup>) to restore mitochondrial protein homeostasis and maintain normal life activities....

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Main Authors: Guolong Yu, Zhuoran Huang, Chaocheng Guo, Jiahao Li, Xinyuan Wang, Yudong Wang, Xu Wang
Format: Article
Language:English
Published: MDPI AG 2024-11-01
Series:Plants
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Online Access:https://www.mdpi.com/2223-7747/13/22/3116
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author Guolong Yu
Zhuoran Huang
Chaocheng Guo
Jiahao Li
Xinyuan Wang
Yudong Wang
Xu Wang
author_facet Guolong Yu
Zhuoran Huang
Chaocheng Guo
Jiahao Li
Xinyuan Wang
Yudong Wang
Xu Wang
author_sort Guolong Yu
collection DOAJ
description Mitochondria are important organelles in eukaryotes and are involved in various metabolic processes. Mitochondrial proteotoxic stress triggers the mitochondrial unfolded protein response (UPR<sup>mt</sup>) to restore mitochondrial protein homeostasis and maintain normal life activities. However, the regulatory mechanism of plant UPR<sup>mt</sup> remains to be revealed in Arabidopsis. Based on the fact that UPR<sup>mt</sup> activates heat shock protein (<i>HSP</i>) genes, we identified the heat shock transcription factor <i>HSFA6b</i> as a key regulator mediating UPR<sup>mt</sup> through reverse genetics. <i>HSFA6b</i> responded to mitochondrial proteotoxic stress and regulated mitochondrial heat shock proteins’ genes’ (<i>mtHSPs</i>) expression. HSFA6b translocated to the nuclear after treatment with doxycycline (Dox)—a mitochondrial ribosome translation inhibitor. HSFA6b binds to the <i>mtHSPs</i> promoters and activates <i>mtHSPs</i> expression. The <i>HSFA6b</i> mutation blocked the UPR<sup>mt</sup> signals to promote root growth under mitochondrial proteotoxic stress and accelerated leaf senescence during development. Our study reveals a novel signal-regulating mechanism in the UPR<sup>mt</sup> pathways and provides new insights regarding the regulation of plant growth and development and stress resistance by the UPR<sup>mt</sup> pathways.
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spelling doaj-art-e038e1ae06d54d74b7c9ece05654d59d2025-08-20T02:27:36ZengMDPI AGPlants2223-77472024-11-011322311610.3390/plants13223116Heat Shock Factor HSFA6b Mediates Mitochondrial Unfolded Protein Response in <i>Arabidopsis thaliana</i>Guolong Yu0Zhuoran Huang1Chaocheng Guo2Jiahao Li3Xinyuan Wang4Yudong Wang5Xu Wang6Shanghai Collaborative Innovation Center of Agri-Seeds, Joint Center for Single Cell Biology, School of Agriculture and Biology, Shanghai Jiao Tong University, Shanghai 200240, ChinaShanghai Collaborative Innovation Center of Agri-Seeds, Joint Center for Single Cell Biology, School of Agriculture and Biology, Shanghai Jiao Tong University, Shanghai 200240, ChinaShanghai Collaborative Innovation Center of Agri-Seeds, Joint Center for Single Cell Biology, School of Agriculture and Biology, Shanghai Jiao Tong University, Shanghai 200240, ChinaShanghai Collaborative Innovation Center of Agri-Seeds, Joint Center for Single Cell Biology, School of Agriculture and Biology, Shanghai Jiao Tong University, Shanghai 200240, ChinaShanghai Collaborative Innovation Center of Agri-Seeds, Joint Center for Single Cell Biology, School of Agriculture and Biology, Shanghai Jiao Tong University, Shanghai 200240, ChinaShanghai Collaborative Innovation Center of Agri-Seeds, Joint Center for Single Cell Biology, School of Agriculture and Biology, Shanghai Jiao Tong University, Shanghai 200240, ChinaShanghai Collaborative Innovation Center of Agri-Seeds, Joint Center for Single Cell Biology, School of Agriculture and Biology, Shanghai Jiao Tong University, Shanghai 200240, ChinaMitochondria are important organelles in eukaryotes and are involved in various metabolic processes. Mitochondrial proteotoxic stress triggers the mitochondrial unfolded protein response (UPR<sup>mt</sup>) to restore mitochondrial protein homeostasis and maintain normal life activities. However, the regulatory mechanism of plant UPR<sup>mt</sup> remains to be revealed in Arabidopsis. Based on the fact that UPR<sup>mt</sup> activates heat shock protein (<i>HSP</i>) genes, we identified the heat shock transcription factor <i>HSFA6b</i> as a key regulator mediating UPR<sup>mt</sup> through reverse genetics. <i>HSFA6b</i> responded to mitochondrial proteotoxic stress and regulated mitochondrial heat shock proteins’ genes’ (<i>mtHSPs</i>) expression. HSFA6b translocated to the nuclear after treatment with doxycycline (Dox)—a mitochondrial ribosome translation inhibitor. HSFA6b binds to the <i>mtHSPs</i> promoters and activates <i>mtHSPs</i> expression. The <i>HSFA6b</i> mutation blocked the UPR<sup>mt</sup> signals to promote root growth under mitochondrial proteotoxic stress and accelerated leaf senescence during development. Our study reveals a novel signal-regulating mechanism in the UPR<sup>mt</sup> pathways and provides new insights regarding the regulation of plant growth and development and stress resistance by the UPR<sup>mt</sup> pathways.https://www.mdpi.com/2223-7747/13/22/3116mitochondriamitochondrial proteotoxic stressmitochondrial unfolded protein response UPR<sup>mt</sup>heat shock factorheat shock protein
spellingShingle Guolong Yu
Zhuoran Huang
Chaocheng Guo
Jiahao Li
Xinyuan Wang
Yudong Wang
Xu Wang
Heat Shock Factor HSFA6b Mediates Mitochondrial Unfolded Protein Response in <i>Arabidopsis thaliana</i>
Plants
mitochondria
mitochondrial proteotoxic stress
mitochondrial unfolded protein response UPR<sup>mt</sup>
heat shock factor
heat shock protein
title Heat Shock Factor HSFA6b Mediates Mitochondrial Unfolded Protein Response in <i>Arabidopsis thaliana</i>
title_full Heat Shock Factor HSFA6b Mediates Mitochondrial Unfolded Protein Response in <i>Arabidopsis thaliana</i>
title_fullStr Heat Shock Factor HSFA6b Mediates Mitochondrial Unfolded Protein Response in <i>Arabidopsis thaliana</i>
title_full_unstemmed Heat Shock Factor HSFA6b Mediates Mitochondrial Unfolded Protein Response in <i>Arabidopsis thaliana</i>
title_short Heat Shock Factor HSFA6b Mediates Mitochondrial Unfolded Protein Response in <i>Arabidopsis thaliana</i>
title_sort heat shock factor hsfa6b mediates mitochondrial unfolded protein response in i arabidopsis thaliana i
topic mitochondria
mitochondrial proteotoxic stress
mitochondrial unfolded protein response UPR<sup>mt</sup>
heat shock factor
heat shock protein
url https://www.mdpi.com/2223-7747/13/22/3116
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