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Peroxin Pex14/17 Is Required for Trap Formation, and Plays Pleiotropic Roles in Mycelial Development, Stress Response, and Secondary Metabolism in Arthrobotrys oligospora

The peroxins encoded by PEX genes involved in peroxisome biogenesis play a crucial role in cellular metabolism and pathogenicity in fungi. Herein, we characterized a filamentous fungus-specific peroxin Pex14/17 in the Arthrobotrys oligospora, a representative species of nematode-trapping fungi. The...

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Autores principales: Liu, Qianqian, Li, Dongni, Bai, Na, Zhu, Yingmei, Yang, Jinkui
Formato: Online Artículo Texto
Lenguaje:English
Publicado: American Society for Microbiology 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10117088/
https://www.ncbi.nlm.nih.gov/pubmed/36786584
http://dx.doi.org/10.1128/msphere.00012-23
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author Liu, Qianqian
Li, Dongni
Bai, Na
Zhu, Yingmei
Yang, Jinkui
author_facet Liu, Qianqian
Li, Dongni
Bai, Na
Zhu, Yingmei
Yang, Jinkui
author_sort Liu, Qianqian
collection PubMed
description The peroxins encoded by PEX genes involved in peroxisome biogenesis play a crucial role in cellular metabolism and pathogenicity in fungi. Herein, we characterized a filamentous fungus-specific peroxin Pex14/17 in the Arthrobotrys oligospora, a representative species of nematode-trapping fungi. The deletion of AoPEX14/17 resulted in a remarkable reduction in mycelial growth, conidia yield, trap formation, and pathogenicity. Compared with the wild-type strain, the ΔAopex14/17 mutant exhibited more lipid droplet and reactive oxygen species accumulation accompanied with a significant decrease in fatty acid utilization and tolerance to oxidative stress. Transcriptomic analysis indicated that AoPEX14/17 was involved in the regulation of metabolism, genetic information processing, environmental information processing, and cellular processes. In subcellular morphology, the deletion of AoPEX14/17 resulted in a decrease in the number of cell nuclei, autophagosomes, and Woronin bodies. Metabolic profile analysis showed that AoPex14/17 affects the biosynthesis of secondary metabolites. Yeast two-hybrid assay revealed that AoPex14/17 interacted with AoPex14 but not with AoPex13. Taken together, our results suggest that Pex14/17 is the main factor for modulating growth, development, and pathogenicity in A. oligospora. IMPORTANCE Peroxisome biogenesis genes (PEX) play an important role in growth, development, and pathogenicity in pathogenic fungi. However, the roles of PEX genes remain largely unknown in nematode-trapping (NT) fungi. Here, we provide direct evidence that AoPex14/17 regulates mycelial growth, conidiation, trap formation, autophagy, endocytosis, catalase activity, stress response to oxidants, lipid metabolism, and reactive oxygen species production. Transcriptome analysis and metabolic profile suggested that AoPex14/17 is involved in multiple cellular processes and the regulation of secondary metabolism. Therefore, our study extends the functions of PEX genes, which helps to elucidate the mechanism of organelle development and trap formation in NT fungi and lays the foundation for the development of efficient nematode biocontrol agents.
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spelling pubmed-101170882023-04-21 Peroxin Pex14/17 Is Required for Trap Formation, and Plays Pleiotropic Roles in Mycelial Development, Stress Response, and Secondary Metabolism in Arthrobotrys oligospora Liu, Qianqian Li, Dongni Bai, Na Zhu, Yingmei Yang, Jinkui mSphere Research Article The peroxins encoded by PEX genes involved in peroxisome biogenesis play a crucial role in cellular metabolism and pathogenicity in fungi. Herein, we characterized a filamentous fungus-specific peroxin Pex14/17 in the Arthrobotrys oligospora, a representative species of nematode-trapping fungi. The deletion of AoPEX14/17 resulted in a remarkable reduction in mycelial growth, conidia yield, trap formation, and pathogenicity. Compared with the wild-type strain, the ΔAopex14/17 mutant exhibited more lipid droplet and reactive oxygen species accumulation accompanied with a significant decrease in fatty acid utilization and tolerance to oxidative stress. Transcriptomic analysis indicated that AoPEX14/17 was involved in the regulation of metabolism, genetic information processing, environmental information processing, and cellular processes. In subcellular morphology, the deletion of AoPEX14/17 resulted in a decrease in the number of cell nuclei, autophagosomes, and Woronin bodies. Metabolic profile analysis showed that AoPex14/17 affects the biosynthesis of secondary metabolites. Yeast two-hybrid assay revealed that AoPex14/17 interacted with AoPex14 but not with AoPex13. Taken together, our results suggest that Pex14/17 is the main factor for modulating growth, development, and pathogenicity in A. oligospora. IMPORTANCE Peroxisome biogenesis genes (PEX) play an important role in growth, development, and pathogenicity in pathogenic fungi. However, the roles of PEX genes remain largely unknown in nematode-trapping (NT) fungi. Here, we provide direct evidence that AoPex14/17 regulates mycelial growth, conidiation, trap formation, autophagy, endocytosis, catalase activity, stress response to oxidants, lipid metabolism, and reactive oxygen species production. Transcriptome analysis and metabolic profile suggested that AoPex14/17 is involved in multiple cellular processes and the regulation of secondary metabolism. Therefore, our study extends the functions of PEX genes, which helps to elucidate the mechanism of organelle development and trap formation in NT fungi and lays the foundation for the development of efficient nematode biocontrol agents. American Society for Microbiology 2023-02-14 /pmc/articles/PMC10117088/ /pubmed/36786584 http://dx.doi.org/10.1128/msphere.00012-23 Text en Copyright © 2023 Liu 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
Liu, Qianqian
Li, Dongni
Bai, Na
Zhu, Yingmei
Yang, Jinkui
Peroxin Pex14/17 Is Required for Trap Formation, and Plays Pleiotropic Roles in Mycelial Development, Stress Response, and Secondary Metabolism in Arthrobotrys oligospora
title Peroxin Pex14/17 Is Required for Trap Formation, and Plays Pleiotropic Roles in Mycelial Development, Stress Response, and Secondary Metabolism in Arthrobotrys oligospora
title_full Peroxin Pex14/17 Is Required for Trap Formation, and Plays Pleiotropic Roles in Mycelial Development, Stress Response, and Secondary Metabolism in Arthrobotrys oligospora
title_fullStr Peroxin Pex14/17 Is Required for Trap Formation, and Plays Pleiotropic Roles in Mycelial Development, Stress Response, and Secondary Metabolism in Arthrobotrys oligospora
title_full_unstemmed Peroxin Pex14/17 Is Required for Trap Formation, and Plays Pleiotropic Roles in Mycelial Development, Stress Response, and Secondary Metabolism in Arthrobotrys oligospora
title_short Peroxin Pex14/17 Is Required for Trap Formation, and Plays Pleiotropic Roles in Mycelial Development, Stress Response, and Secondary Metabolism in Arthrobotrys oligospora
title_sort peroxin pex14/17 is required for trap formation, and plays pleiotropic roles in mycelial development, stress response, and secondary metabolism in arthrobotrys oligospora
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10117088/
https://www.ncbi.nlm.nih.gov/pubmed/36786584
http://dx.doi.org/10.1128/msphere.00012-23
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