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A Subunit of the COP9 Signalosome, MoCsn6, Is Involved in Fungal Development, Pathogenicity, and Autophagy in Rice Blast Fungus

The COP9 signalosome (CSN) is a highly conserved protein complex in eukaryotes, affecting various development and signaling processes. To date, the biological functions of the COP9 signalosome and its subunits have not been determined in Magnaporthe oryzae. In this study, we characterized the CSN in...

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Autores principales: Shen, Zi-Fang, Li, Lin, Wang, Jing-Yi, Zhang, Yun-Ran, Wang, Zi-He, Liang, Shuang, Zhu, Xue-Ming, Lu, Jian-Ping, Lin, Fu-Cheng, Liu, Xiao-Hong
Formato: Online Artículo Texto
Lenguaje:English
Publicado: American Society for Microbiology 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9769505/
https://www.ncbi.nlm.nih.gov/pubmed/36445131
http://dx.doi.org/10.1128/spectrum.02020-22
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author Shen, Zi-Fang
Li, Lin
Wang, Jing-Yi
Zhang, Yun-Ran
Wang, Zi-He
Liang, Shuang
Zhu, Xue-Ming
Lu, Jian-Ping
Lin, Fu-Cheng
Liu, Xiao-Hong
author_facet Shen, Zi-Fang
Li, Lin
Wang, Jing-Yi
Zhang, Yun-Ran
Wang, Zi-He
Liang, Shuang
Zhu, Xue-Ming
Lu, Jian-Ping
Lin, Fu-Cheng
Liu, Xiao-Hong
author_sort Shen, Zi-Fang
collection PubMed
description The COP9 signalosome (CSN) is a highly conserved protein complex in eukaryotes, affecting various development and signaling processes. To date, the biological functions of the COP9 signalosome and its subunits have not been determined in Magnaporthe oryzae. In this study, we characterized the CSN in M. oryzae (which we named MoCsn6) and analyzed its biological functions. MoCsn6 is involved in fungal development, autophagy, and plant pathogenicity. Compared with the wild-type strain 70-15, ΔMocsn6 mutants showed a significantly reduced growth rate, sporulation rate, and germ tube germination rate. Pathogenicity assays showed that the ΔMocsn6 mutants did not cause or significantly reduced the number of disease spots on isolated barley leaves. After the MoCSN6 gene was complemented into the ΔMocsn6 mutant, vegetative growth, sporulation, and pathogenicity were restored. The Osm1 and Pmk1 phosphorylation pathways were also disrupted in the ΔMocsn6 mutants. Furthermore, we found that MoCsn6 participates in the autophagy pathway by interacting with the autophagy core protein MoAtg6 and regulating its ubiquitination level. Deletion of MoCSN6 resulted in rapid lipidation of MoAtg8 and degradation of the autophagic marker protein green fluorescent protein-tagged MoAtg8 under nutrient and starvation conditions, suggesting that MoCsn6 negatively regulates autophagic activity. Taken together, our results demonstrate that MoCsn6 plays a crucial role in regulating fungal development, pathogenicity, and autophagy in M. oryzae. IMPORTANCE Magnaporthe oryzae, a filamentous fungus, is the cause of many cereal diseases. Autophagy is involved in fungal development and pathogenicity. The COP9 signalosome (CSN) has been extensively studied in ubiquitin pathways, but its regulation of autophagy has rarely been reported in plant-pathogenic fungi. Investigations on the relationship between CSN and autophagy will deepen our understanding of the pathogenic mechanism of M. oryzae and provide new insights into the development of new drug targets to control fungal diseases. In this study, the important function of Csn6 in the autophagy regulation pathway and its impact on the pathogenicity of M. oryzae were determined. We showed that Csn6 manages autophagy by interacting with the autophagy core protein Atg6 and regulating its ubiquitination level. Furthermore, future investigations that explore the function of CSN will deepen our understanding of autophagy mechanisms in rice blast fungus.
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spelling pubmed-97695052022-12-22 A Subunit of the COP9 Signalosome, MoCsn6, Is Involved in Fungal Development, Pathogenicity, and Autophagy in Rice Blast Fungus Shen, Zi-Fang Li, Lin Wang, Jing-Yi Zhang, Yun-Ran Wang, Zi-He Liang, Shuang Zhu, Xue-Ming Lu, Jian-Ping Lin, Fu-Cheng Liu, Xiao-Hong Microbiol Spectr Research Article The COP9 signalosome (CSN) is a highly conserved protein complex in eukaryotes, affecting various development and signaling processes. To date, the biological functions of the COP9 signalosome and its subunits have not been determined in Magnaporthe oryzae. In this study, we characterized the CSN in M. oryzae (which we named MoCsn6) and analyzed its biological functions. MoCsn6 is involved in fungal development, autophagy, and plant pathogenicity. Compared with the wild-type strain 70-15, ΔMocsn6 mutants showed a significantly reduced growth rate, sporulation rate, and germ tube germination rate. Pathogenicity assays showed that the ΔMocsn6 mutants did not cause or significantly reduced the number of disease spots on isolated barley leaves. After the MoCSN6 gene was complemented into the ΔMocsn6 mutant, vegetative growth, sporulation, and pathogenicity were restored. The Osm1 and Pmk1 phosphorylation pathways were also disrupted in the ΔMocsn6 mutants. Furthermore, we found that MoCsn6 participates in the autophagy pathway by interacting with the autophagy core protein MoAtg6 and regulating its ubiquitination level. Deletion of MoCSN6 resulted in rapid lipidation of MoAtg8 and degradation of the autophagic marker protein green fluorescent protein-tagged MoAtg8 under nutrient and starvation conditions, suggesting that MoCsn6 negatively regulates autophagic activity. Taken together, our results demonstrate that MoCsn6 plays a crucial role in regulating fungal development, pathogenicity, and autophagy in M. oryzae. IMPORTANCE Magnaporthe oryzae, a filamentous fungus, is the cause of many cereal diseases. Autophagy is involved in fungal development and pathogenicity. The COP9 signalosome (CSN) has been extensively studied in ubiquitin pathways, but its regulation of autophagy has rarely been reported in plant-pathogenic fungi. Investigations on the relationship between CSN and autophagy will deepen our understanding of the pathogenic mechanism of M. oryzae and provide new insights into the development of new drug targets to control fungal diseases. In this study, the important function of Csn6 in the autophagy regulation pathway and its impact on the pathogenicity of M. oryzae were determined. We showed that Csn6 manages autophagy by interacting with the autophagy core protein Atg6 and regulating its ubiquitination level. Furthermore, future investigations that explore the function of CSN will deepen our understanding of autophagy mechanisms in rice blast fungus. American Society for Microbiology 2022-11-29 /pmc/articles/PMC9769505/ /pubmed/36445131 http://dx.doi.org/10.1128/spectrum.02020-22 Text en Copyright © 2022 Shen et al. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Research Article
Shen, Zi-Fang
Li, Lin
Wang, Jing-Yi
Zhang, Yun-Ran
Wang, Zi-He
Liang, Shuang
Zhu, Xue-Ming
Lu, Jian-Ping
Lin, Fu-Cheng
Liu, Xiao-Hong
A Subunit of the COP9 Signalosome, MoCsn6, Is Involved in Fungal Development, Pathogenicity, and Autophagy in Rice Blast Fungus
title A Subunit of the COP9 Signalosome, MoCsn6, Is Involved in Fungal Development, Pathogenicity, and Autophagy in Rice Blast Fungus
title_full A Subunit of the COP9 Signalosome, MoCsn6, Is Involved in Fungal Development, Pathogenicity, and Autophagy in Rice Blast Fungus
title_fullStr A Subunit of the COP9 Signalosome, MoCsn6, Is Involved in Fungal Development, Pathogenicity, and Autophagy in Rice Blast Fungus
title_full_unstemmed A Subunit of the COP9 Signalosome, MoCsn6, Is Involved in Fungal Development, Pathogenicity, and Autophagy in Rice Blast Fungus
title_short A Subunit of the COP9 Signalosome, MoCsn6, Is Involved in Fungal Development, Pathogenicity, and Autophagy in Rice Blast Fungus
title_sort subunit of the cop9 signalosome, mocsn6, is involved in fungal development, pathogenicity, and autophagy in rice blast fungus
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9769505/
https://www.ncbi.nlm.nih.gov/pubmed/36445131
http://dx.doi.org/10.1128/spectrum.02020-22
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