Csn5 inhibits autophagy by regulating the ubiquitination of Atg6 and Tor to mediate the pathogenicity of Magnaporthe oryzae
Abstract Csn5 is subunit 5 of the COP9 signalosome (CSN), but the mechanism by which it strictly controls the pathogenicity of pathogenic fungi through autophagy remains unclear. Here, we found that Csn5 deficiency attenuated pathogenicity and enhanced autophagy in Magnaporthe oryzae. MoCSN5 knockou...
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BMC
2024-04-01
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Series: | Cell Communication and Signaling |
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Online Access: | https://doi.org/10.1186/s12964-024-01598-7 |
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author | Zi-Fang Shen Lin Li Jing-Yi Wang Jian Liao Yun-Ran Zhang Xue-Ming Zhu Zi-He Wang Jian-Ping Lu Xiao-Hong Liu Fu-Cheng Lin |
author_facet | Zi-Fang Shen Lin Li Jing-Yi Wang Jian Liao Yun-Ran Zhang Xue-Ming Zhu Zi-He Wang Jian-Ping Lu Xiao-Hong Liu Fu-Cheng Lin |
author_sort | Zi-Fang Shen |
collection | DOAJ |
description | Abstract Csn5 is subunit 5 of the COP9 signalosome (CSN), but the mechanism by which it strictly controls the pathogenicity of pathogenic fungi through autophagy remains unclear. Here, we found that Csn5 deficiency attenuated pathogenicity and enhanced autophagy in Magnaporthe oryzae. MoCSN5 knockout led to overubiquitination and overdegradation of MoTor (the core protein of the TORC1 complex [target of rapamycin]) thereby promoted autophagy. In addition, we identified MoCsn5 as a new interactor of MoAtg6. Atg6 was found to be ubiquitinated through linkage with lysine 48 (K48) in cells, which is necessary for infection-associated autophagy in pathogenic fungi. K48-ubiquitination of Atg6 enhanced its degradation and thereby inhibited autophagic activity. Our experimental results indicated that MoCsn5 promoted K48-ubiquitination of MoAtg6, which reduced the MoAtg6 protein content and thus inhibited autophagy. Aberrant ubiquitination and autophagy in ΔMocsn5 led to pleiotropic defects in the growth, development, stress resistance, and pathogenicity of M. oryzae. In summary, our study revealed a novel mechanism by which Csn5 regulates autophagy and pathogenicity in rice blast fungus through ubiquitination. |
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language | English |
last_indexed | 2024-04-24T09:50:38Z |
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spelling | doaj.art-0ca4b32a1b9e43d38a8dcb27a1daf4962024-04-14T11:23:15ZengBMCCell Communication and Signaling1478-811X2024-04-0122111910.1186/s12964-024-01598-7Csn5 inhibits autophagy by regulating the ubiquitination of Atg6 and Tor to mediate the pathogenicity of Magnaporthe oryzaeZi-Fang Shen0Lin Li1Jing-Yi Wang2Jian Liao3Yun-Ran Zhang4Xue-Ming Zhu5Zi-He Wang6Jian-Ping Lu7Xiao-Hong Liu8Fu-Cheng Lin9State Key Laboratory for Managing Biotic and Chemical Treats to the Quality and Safety of Agro-Products, Zhejiang Provincial Key Laboratory of Agricultural Microbiomics, Key Laboratory of Agricultural Microbiome (MARA), Institute of Plant Protection and Microbiology, Zhejiang Academy of Agricultural SciencesState Key Laboratory for Managing Biotic and Chemical Treats to the Quality and Safety of Agro-Products, Zhejiang Provincial Key Laboratory of Agricultural Microbiomics, Key Laboratory of Agricultural Microbiome (MARA), Institute of Plant Protection and Microbiology, Zhejiang Academy of Agricultural SciencesState Key Laboratory for Managing Biotic and Chemical Treats to the Quality and Safety of Agro-Products, Zhejiang Provincial Key Laboratory of Agricultural Microbiomics, Key Laboratory of Agricultural Microbiome (MARA), Institute of Biotechnology, Zhejiang UniversityState Key Laboratory for Managing Biotic and Chemical Treats to the Quality and Safety of Agro-Products, Zhejiang Provincial Key Laboratory of Agricultural Microbiomics, Key Laboratory of Agricultural Microbiome (MARA), Institute of Biotechnology, Zhejiang UniversityState Key Laboratory for Managing Biotic and Chemical Treats to the Quality and Safety of Agro-Products, Zhejiang Provincial Key Laboratory of Agricultural Microbiomics, Key Laboratory of Agricultural Microbiome (MARA), Institute of Biotechnology, Zhejiang UniversityState Key Laboratory for Managing Biotic and Chemical Treats to the Quality and Safety of Agro-Products, Zhejiang Provincial Key Laboratory of Agricultural Microbiomics, Key Laboratory of Agricultural Microbiome (MARA), Institute of Plant Protection and Microbiology, Zhejiang Academy of Agricultural SciencesState Key Laboratory for Managing Biotic and Chemical Treats to the Quality and Safety of Agro-Products, Zhejiang Provincial Key Laboratory of Agricultural Microbiomics, Key Laboratory of Agricultural Microbiome (MARA), Institute of Biotechnology, Zhejiang UniversityCollege of Life Sciences, Zhejiang UniversityState Key Laboratory for Managing Biotic and Chemical Treats to the Quality and Safety of Agro-Products, Zhejiang Provincial Key Laboratory of Agricultural Microbiomics, Key Laboratory of Agricultural Microbiome (MARA), Institute of Biotechnology, Zhejiang UniversityState Key Laboratory for Managing Biotic and Chemical Treats to the Quality and Safety of Agro-Products, Zhejiang Provincial Key Laboratory of Agricultural Microbiomics, Key Laboratory of Agricultural Microbiome (MARA), Institute of Plant Protection and Microbiology, Zhejiang Academy of Agricultural SciencesAbstract Csn5 is subunit 5 of the COP9 signalosome (CSN), but the mechanism by which it strictly controls the pathogenicity of pathogenic fungi through autophagy remains unclear. Here, we found that Csn5 deficiency attenuated pathogenicity and enhanced autophagy in Magnaporthe oryzae. MoCSN5 knockout led to overubiquitination and overdegradation of MoTor (the core protein of the TORC1 complex [target of rapamycin]) thereby promoted autophagy. In addition, we identified MoCsn5 as a new interactor of MoAtg6. Atg6 was found to be ubiquitinated through linkage with lysine 48 (K48) in cells, which is necessary for infection-associated autophagy in pathogenic fungi. K48-ubiquitination of Atg6 enhanced its degradation and thereby inhibited autophagic activity. Our experimental results indicated that MoCsn5 promoted K48-ubiquitination of MoAtg6, which reduced the MoAtg6 protein content and thus inhibited autophagy. Aberrant ubiquitination and autophagy in ΔMocsn5 led to pleiotropic defects in the growth, development, stress resistance, and pathogenicity of M. oryzae. In summary, our study revealed a novel mechanism by which Csn5 regulates autophagy and pathogenicity in rice blast fungus through ubiquitination.https://doi.org/10.1186/s12964-024-01598-7COP9 signalosomeCsn5AutophagyUbiquitinationPathogenicityRice blast fungus |
spellingShingle | Zi-Fang Shen Lin Li Jing-Yi Wang Jian Liao Yun-Ran Zhang Xue-Ming Zhu Zi-He Wang Jian-Ping Lu Xiao-Hong Liu Fu-Cheng Lin Csn5 inhibits autophagy by regulating the ubiquitination of Atg6 and Tor to mediate the pathogenicity of Magnaporthe oryzae Cell Communication and Signaling COP9 signalosome Csn5 Autophagy Ubiquitination Pathogenicity Rice blast fungus |
title | Csn5 inhibits autophagy by regulating the ubiquitination of Atg6 and Tor to mediate the pathogenicity of Magnaporthe oryzae |
title_full | Csn5 inhibits autophagy by regulating the ubiquitination of Atg6 and Tor to mediate the pathogenicity of Magnaporthe oryzae |
title_fullStr | Csn5 inhibits autophagy by regulating the ubiquitination of Atg6 and Tor to mediate the pathogenicity of Magnaporthe oryzae |
title_full_unstemmed | Csn5 inhibits autophagy by regulating the ubiquitination of Atg6 and Tor to mediate the pathogenicity of Magnaporthe oryzae |
title_short | Csn5 inhibits autophagy by regulating the ubiquitination of Atg6 and Tor to mediate the pathogenicity of Magnaporthe oryzae |
title_sort | csn5 inhibits autophagy by regulating the ubiquitination of atg6 and tor to mediate the pathogenicity of magnaporthe oryzae |
topic | COP9 signalosome Csn5 Autophagy Ubiquitination Pathogenicity Rice blast fungus |
url | https://doi.org/10.1186/s12964-024-01598-7 |
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