The oomycete-specific BAG subfamily maintains protein homeostasis and promotes pathogenicity in an atypical HSP70-independent manner

Summary: Protein homeostasis is vital for organisms and requires chaperones like the conserved Bcl-2-associated athanogene (BAG) co-chaperones that bind to the heat shock protein 70 (HSP70) through their C-terminal BAG domain (BD). Here, we show an unconventional BAG subfamily exclusively found in o...

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Main Authors: Gan Ai, Jierui Si, Yang Cheng, Rui Meng, Zishan Wu, Ruofei Xu, Xiaodan Wang, Ying Zhai, Hao Peng, Yurong Li, Daolong Dou, Maofeng Jing
Format: Article
Language:English
Published: Elsevier 2023-11-01
Series:Cell Reports
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S2211124723014031
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author Gan Ai
Jierui Si
Yang Cheng
Rui Meng
Zishan Wu
Ruofei Xu
Xiaodan Wang
Ying Zhai
Hao Peng
Yurong Li
Daolong Dou
Maofeng Jing
author_facet Gan Ai
Jierui Si
Yang Cheng
Rui Meng
Zishan Wu
Ruofei Xu
Xiaodan Wang
Ying Zhai
Hao Peng
Yurong Li
Daolong Dou
Maofeng Jing
author_sort Gan Ai
collection DOAJ
description Summary: Protein homeostasis is vital for organisms and requires chaperones like the conserved Bcl-2-associated athanogene (BAG) co-chaperones that bind to the heat shock protein 70 (HSP70) through their C-terminal BAG domain (BD). Here, we show an unconventional BAG subfamily exclusively found in oomycetes. Oomycete BAGs feature an atypical N-terminal BD with a short and oomycete-specific α1 helix (α1′), plus a C-terminal small heat shock protein (sHSP) domain. In oomycete pathogen Phytophthora sojae, both BD-α1′ and sHSP domains are required for P. sojae BAG (PsBAG) function in cyst germination, pathogenicity, and unfolded protein response assisting in 26S proteasome-mediated degradation of misfolded proteins. PsBAGs form homo- and heterodimers through their unique BD-α1′ to function properly, with no recruitment of HSP70s to form the common BAG-HSP70 complex found in other eukaryotes. Our study highlights an oomycete-exclusive protein homeostasis mechanism mediated by atypical BAGs, which provides a potential target for oomycete disease control.
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spelling doaj.art-8ce36a4a3dc34cd0be33a69bcf5af7a12023-11-30T05:07:02ZengElsevierCell Reports2211-12472023-11-014211113391The oomycete-specific BAG subfamily maintains protein homeostasis and promotes pathogenicity in an atypical HSP70-independent mannerGan Ai0Jierui Si1Yang Cheng2Rui Meng3Zishan Wu4Ruofei Xu5Xiaodan Wang6Ying Zhai7Hao Peng8Yurong Li9Daolong Dou10Maofeng Jing11Department of Plant Pathology, Key Laboratory of Soybean Disease and Pest Control (Ministry of Agriculture and Rural Affairs), Nanjing Agricultural University, Nanjing 210095, ChinaDepartment of Plant Pathology, Key Laboratory of Soybean Disease and Pest Control (Ministry of Agriculture and Rural Affairs), Nanjing Agricultural University, Nanjing 210095, ChinaDepartment of Plant Pathology, Key Laboratory of Soybean Disease and Pest Control (Ministry of Agriculture and Rural Affairs), Nanjing Agricultural University, Nanjing 210095, ChinaDepartment of Plant Pathology, Key Laboratory of Soybean Disease and Pest Control (Ministry of Agriculture and Rural Affairs), Nanjing Agricultural University, Nanjing 210095, ChinaDepartment of Plant Pathology, Key Laboratory of Soybean Disease and Pest Control (Ministry of Agriculture and Rural Affairs), Nanjing Agricultural University, Nanjing 210095, ChinaDepartment of Plant Pathology, Key Laboratory of Soybean Disease and Pest Control (Ministry of Agriculture and Rural Affairs), Nanjing Agricultural University, Nanjing 210095, ChinaDepartment of Plant Pathology, China Agricultural University, Beijing 100091, ChinaUSDA-ARS, Crop Diseases, Pests and Genetics Research Unit, Parlier, CA 93648, USAUSDA-ARS, Crop Diseases, Pests and Genetics Research Unit, Parlier, CA 93648, USACorteva Agriscience, Johnston, IA 50131, USADepartment of Plant Pathology, Key Laboratory of Soybean Disease and Pest Control (Ministry of Agriculture and Rural Affairs), Nanjing Agricultural University, Nanjing 210095, ChinaDepartment of Plant Pathology, Key Laboratory of Soybean Disease and Pest Control (Ministry of Agriculture and Rural Affairs), Nanjing Agricultural University, Nanjing 210095, China; Corresponding authorSummary: Protein homeostasis is vital for organisms and requires chaperones like the conserved Bcl-2-associated athanogene (BAG) co-chaperones that bind to the heat shock protein 70 (HSP70) through their C-terminal BAG domain (BD). Here, we show an unconventional BAG subfamily exclusively found in oomycetes. Oomycete BAGs feature an atypical N-terminal BD with a short and oomycete-specific α1 helix (α1′), plus a C-terminal small heat shock protein (sHSP) domain. In oomycete pathogen Phytophthora sojae, both BD-α1′ and sHSP domains are required for P. sojae BAG (PsBAG) function in cyst germination, pathogenicity, and unfolded protein response assisting in 26S proteasome-mediated degradation of misfolded proteins. PsBAGs form homo- and heterodimers through their unique BD-α1′ to function properly, with no recruitment of HSP70s to form the common BAG-HSP70 complex found in other eukaryotes. Our study highlights an oomycete-exclusive protein homeostasis mechanism mediated by atypical BAGs, which provides a potential target for oomycete disease control.http://www.sciencedirect.com/science/article/pii/S2211124723014031CP: PlantsCP: Microbiology
spellingShingle Gan Ai
Jierui Si
Yang Cheng
Rui Meng
Zishan Wu
Ruofei Xu
Xiaodan Wang
Ying Zhai
Hao Peng
Yurong Li
Daolong Dou
Maofeng Jing
The oomycete-specific BAG subfamily maintains protein homeostasis and promotes pathogenicity in an atypical HSP70-independent manner
Cell Reports
CP: Plants
CP: Microbiology
title The oomycete-specific BAG subfamily maintains protein homeostasis and promotes pathogenicity in an atypical HSP70-independent manner
title_full The oomycete-specific BAG subfamily maintains protein homeostasis and promotes pathogenicity in an atypical HSP70-independent manner
title_fullStr The oomycete-specific BAG subfamily maintains protein homeostasis and promotes pathogenicity in an atypical HSP70-independent manner
title_full_unstemmed The oomycete-specific BAG subfamily maintains protein homeostasis and promotes pathogenicity in an atypical HSP70-independent manner
title_short The oomycete-specific BAG subfamily maintains protein homeostasis and promotes pathogenicity in an atypical HSP70-independent manner
title_sort oomycete specific bag subfamily maintains protein homeostasis and promotes pathogenicity in an atypical hsp70 independent manner
topic CP: Plants
CP: Microbiology
url http://www.sciencedirect.com/science/article/pii/S2211124723014031
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