EGY3 mediates chloroplastic ROS homeostasis and promotes retrograde signaling in response to salt stress in Arabidopsis

Yong Zhuang; Ming Wei; Chengcheng Ling; Yangxuan Liu; Abdul Karim Amin; Penghui Li; Pengwei Li; Xufan Hu; Huaxu Bao; Heqiang Huo; Jan Smalle; Songhu Wang

doi:10.1016/j.celrep.2021.109384

EGY3 mediates chloroplastic ROS homeostasis and promotes retrograde signaling in response to salt stress in Arabidopsis

Yong Zhuang, Ming Wei, Chengcheng Ling, Yangxuan Liu, Abdul Karim Amin, Penghui Li, Pengwei Li, Xufan Hu, Huaxu Bao, Heqiang Huo, Jan Smalle, Songhu Wang

Plant and Soil Sciences

Research output: Contribution to journal › Article › peer-review

32 Scopus citations

Abstract

The chloroplast is the main organelle for stress-induced production of reactive oxygen species (ROS). However, how chloroplastic ROS homeostasis is maintained under salt stress is largely unknown. We show that EGY3, a gene encoding a chloroplast-localized protein, is induced by salt and oxidative stresses. The loss of EGY3 function causes stress hypersensitivity while EGY3 overexpression increases the tolerance to both salt and chloroplastic oxidative stresses. EGY3 interacts with chloroplastic Cu/Zn-SOD2 (CSD2) and promotes CSD2 stability under stress conditions. In egy3-1 mutant plants, the stress-induced CSD2 degradation limits H₂O₂ production in chloroplasts and impairs H₂O₂-mediated retrograde signaling, as indicated by the decreased expression of retrograde-signal-responsive genes required for stress tolerance. Both exogenous application of H₂O₂ (or APX inhibitor) and CSD2 overexpression can rescue the salt-stress hypersensitivity of egy3-1 mutants. Our findings reveal that EGY3 enhances the tolerance to salt stress by promoting the CSD2 stability and H₂O₂-mediated chloroplastic retrograde signaling.

Original language	English
Article number	109384
Journal	Cell Reports
Volume	36
Issue number	2
DOIs	https://doi.org/10.1016/j.celrep.2021.109384
State	Published - Jul 13 2021

Bibliographical note

Publisher Copyright:
© 2021 The Author(s)

Funding

This work was supported by National Natural Science Foundation of China (grant 31871354 ), the Hundred Talents Program (Chinese Academy of Sciences), Startup Funding of Anhui Agricultural University , and the “Wanjiang Scholar” program .

Funders	Funder number
National Natural Science Foundation of China (NSFC)	31871354
National Natural Science Foundation of China (NSFC)
Chinese Academy of Sciences
Anhui Agriculture University

Keywords

Cu/Zn-SOD2
HO-mediated retrograde signal
chloroplastic ROS
salt stress

ASJC Scopus subject areas

General Biochemistry, Genetics and Molecular Biology

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10.1016/j.celrep.2021.109384

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title = "EGY3 mediates chloroplastic ROS homeostasis and promotes retrograde signaling in response to salt stress in Arabidopsis",

abstract = "The chloroplast is the main organelle for stress-induced production of reactive oxygen species (ROS). However, how chloroplastic ROS homeostasis is maintained under salt stress is largely unknown. We show that EGY3, a gene encoding a chloroplast-localized protein, is induced by salt and oxidative stresses. The loss of EGY3 function causes stress hypersensitivity while EGY3 overexpression increases the tolerance to both salt and chloroplastic oxidative stresses. EGY3 interacts with chloroplastic Cu/Zn-SOD2 (CSD2) and promotes CSD2 stability under stress conditions. In egy3-1 mutant plants, the stress-induced CSD2 degradation limits H2O2 production in chloroplasts and impairs H2O2-mediated retrograde signaling, as indicated by the decreased expression of retrograde-signal-responsive genes required for stress tolerance. Both exogenous application of H2O2 (or APX inhibitor) and CSD2 overexpression can rescue the salt-stress hypersensitivity of egy3-1 mutants. Our findings reveal that EGY3 enhances the tolerance to salt stress by promoting the CSD2 stability and H2O2-mediated chloroplastic retrograde signaling.",

keywords = "Cu/Zn-SOD2, HO-mediated retrograde signal, chloroplastic ROS, salt stress",

author = "Yong Zhuang and Ming Wei and Chengcheng Ling and Yangxuan Liu and Amin, {Abdul Karim} and Penghui Li and Pengwei Li and Xufan Hu and Huaxu Bao and Heqiang Huo and Jan Smalle and Songhu Wang",

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AU - Zhuang, Yong

AU - Wei, Ming

AU - Ling, Chengcheng

AU - Liu, Yangxuan

AU - Amin, Abdul Karim

AU - Li, Penghui

AU - Li, Pengwei

AU - Hu, Xufan

AU - Bao, Huaxu

AU - Huo, Heqiang

AU - Smalle, Jan

AU - Wang, Songhu

PY - 2021/7/13

Y1 - 2021/7/13

N2 - The chloroplast is the main organelle for stress-induced production of reactive oxygen species (ROS). However, how chloroplastic ROS homeostasis is maintained under salt stress is largely unknown. We show that EGY3, a gene encoding a chloroplast-localized protein, is induced by salt and oxidative stresses. The loss of EGY3 function causes stress hypersensitivity while EGY3 overexpression increases the tolerance to both salt and chloroplastic oxidative stresses. EGY3 interacts with chloroplastic Cu/Zn-SOD2 (CSD2) and promotes CSD2 stability under stress conditions. In egy3-1 mutant plants, the stress-induced CSD2 degradation limits H2O2 production in chloroplasts and impairs H2O2-mediated retrograde signaling, as indicated by the decreased expression of retrograde-signal-responsive genes required for stress tolerance. Both exogenous application of H2O2 (or APX inhibitor) and CSD2 overexpression can rescue the salt-stress hypersensitivity of egy3-1 mutants. Our findings reveal that EGY3 enhances the tolerance to salt stress by promoting the CSD2 stability and H2O2-mediated chloroplastic retrograde signaling.

AB - The chloroplast is the main organelle for stress-induced production of reactive oxygen species (ROS). However, how chloroplastic ROS homeostasis is maintained under salt stress is largely unknown. We show that EGY3, a gene encoding a chloroplast-localized protein, is induced by salt and oxidative stresses. The loss of EGY3 function causes stress hypersensitivity while EGY3 overexpression increases the tolerance to both salt and chloroplastic oxidative stresses. EGY3 interacts with chloroplastic Cu/Zn-SOD2 (CSD2) and promotes CSD2 stability under stress conditions. In egy3-1 mutant plants, the stress-induced CSD2 degradation limits H2O2 production in chloroplasts and impairs H2O2-mediated retrograde signaling, as indicated by the decreased expression of retrograde-signal-responsive genes required for stress tolerance. Both exogenous application of H2O2 (or APX inhibitor) and CSD2 overexpression can rescue the salt-stress hypersensitivity of egy3-1 mutants. Our findings reveal that EGY3 enhances the tolerance to salt stress by promoting the CSD2 stability and H2O2-mediated chloroplastic retrograde signaling.

KW - Cu/Zn-SOD2

KW - HO-mediated retrograde signal

KW - chloroplastic ROS

KW - salt stress

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EGY3 mediates chloroplastic ROS homeostasis and promotes retrograde signaling in response to salt stress in Arabidopsis

Abstract

Bibliographical note

Funding

Keywords

ASJC Scopus subject areas

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