Identification of a transcription factor AoMsn2 of the Hog1 signaling pathway contributes to fungal growth, development and pathogenicity in Arthrobotrys oligospora

Introduction: Arthrobotrys oligospora has been utilized as a model strain to study the interaction between fungi and nematodes owing to its ability to capture nematodes by developing specialized traps. A previous study showed that high-osmolarity glycerol (Hog1) signaling regulates the osmoregulatio...

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Main Authors: Qianqian Liu, Kexin Jiang, Shipeng Duan, Na Zhao, Yanmei Shen, Lirong Zhu, Ke-Qin Zhang, Jinkui Yang
Format: Article
Language:English
Published: Elsevier 2025-02-01
Series:Journal of Advanced Research
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Online Access:http://www.sciencedirect.com/science/article/pii/S2090123224000523
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author Qianqian Liu
Kexin Jiang
Shipeng Duan
Na Zhao
Yanmei Shen
Lirong Zhu
Ke-Qin Zhang
Jinkui Yang
author_facet Qianqian Liu
Kexin Jiang
Shipeng Duan
Na Zhao
Yanmei Shen
Lirong Zhu
Ke-Qin Zhang
Jinkui Yang
author_sort Qianqian Liu
collection DOAJ
description Introduction: Arthrobotrys oligospora has been utilized as a model strain to study the interaction between fungi and nematodes owing to its ability to capture nematodes by developing specialized traps. A previous study showed that high-osmolarity glycerol (Hog1) signaling regulates the osmoregulation and nematocidal activity of A. oligospora. However, the function of downstream transcription factors of the Hog1 signaling in the nematode-trapping (NT) fungi remains unclear. Objective: This study aimed to investigate the functions and potential regulatory network of AoMsn2, a downstream transcription factor of the Hog1 signaling pathway in A. oligospora. Methods: The function of AoMsn2 was characterized using targeted gene deletion, phenotypic experiments, real-time quantitative PCR, RNA sequencing, untargeted metabolomics, and yeast two-hybrid analysis. Results: Loss of Aomsn2 significantly enlarged and swollen the hyphae, with an increase in septa and a significant decrease in nuclei. In particular, spore yield, spore germination rate, traps, and nematode predation efficiency were remarkably decreased in the mutants. Phenotypic and transcriptomic analyses revealed that AoMsn2 is essential for fatty acid metabolism and autophagic pathways. Additionally, untargeted metabolomic analysis identified an important function of AoMsn2 in the modulation of secondary metabolites. Furtherly, we analyzed the protein interaction network of AoMsn2 based on the Kyoto Encyclopedia of Genes and Genomes pathway map and the online website STRING. Finally, Hog1 and six putative targeted proteins of AoMsn2 were identified by Y2H analysis. Conclusion: Our study reveals that AoMsn2 plays crucial roles in the growth, conidiation, trap development, fatty acid metabolism, and secondary metabolism, as well as establishes a broad basis for understanding the regulatory mechanisms of trap morphogenesis and environmental adaptation in NT fungi.
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spelling doaj-art-bbe6ed5175b449a5b808775717f8e35b2025-01-18T05:04:16ZengElsevierJournal of Advanced Research2090-12322025-02-0168115Identification of a transcription factor AoMsn2 of the Hog1 signaling pathway contributes to fungal growth, development and pathogenicity in Arthrobotrys oligosporaQianqian Liu0Kexin Jiang1Shipeng Duan2Na Zhao3Yanmei Shen4Lirong Zhu5Ke-Qin Zhang6Jinkui Yang7State Key Laboratory for Conservation and Utilization of Bio-Resources in Yunnan, Key Laboratory for Southwest Microbial Diversity of the Ministry of Education, and School of Life Science, Yunnan University, Kunming 650032, ChinaState Key Laboratory for Conservation and Utilization of Bio-Resources in Yunnan, Key Laboratory for Southwest Microbial Diversity of the Ministry of Education, and School of Life Science, Yunnan University, Kunming 650032, ChinaState Key Laboratory for Conservation and Utilization of Bio-Resources in Yunnan, Key Laboratory for Southwest Microbial Diversity of the Ministry of Education, and School of Life Science, Yunnan University, Kunming 650032, ChinaState Key Laboratory for Conservation and Utilization of Bio-Resources in Yunnan, Key Laboratory for Southwest Microbial Diversity of the Ministry of Education, and School of Life Science, Yunnan University, Kunming 650032, ChinaState Key Laboratory for Conservation and Utilization of Bio-Resources in Yunnan, Key Laboratory for Southwest Microbial Diversity of the Ministry of Education, and School of Life Science, Yunnan University, Kunming 650032, ChinaState Key Laboratory for Conservation and Utilization of Bio-Resources in Yunnan, Key Laboratory for Southwest Microbial Diversity of the Ministry of Education, and School of Life Science, Yunnan University, Kunming 650032, ChinaState Key Laboratory for Conservation and Utilization of Bio-Resources in Yunnan, Key Laboratory for Southwest Microbial Diversity of the Ministry of Education, and School of Life Science, Yunnan University, Kunming 650032, ChinaCorresponding author.; State Key Laboratory for Conservation and Utilization of Bio-Resources in Yunnan, Key Laboratory for Southwest Microbial Diversity of the Ministry of Education, and School of Life Science, Yunnan University, Kunming 650032, ChinaIntroduction: Arthrobotrys oligospora has been utilized as a model strain to study the interaction between fungi and nematodes owing to its ability to capture nematodes by developing specialized traps. A previous study showed that high-osmolarity glycerol (Hog1) signaling regulates the osmoregulation and nematocidal activity of A. oligospora. However, the function of downstream transcription factors of the Hog1 signaling in the nematode-trapping (NT) fungi remains unclear. Objective: This study aimed to investigate the functions and potential regulatory network of AoMsn2, a downstream transcription factor of the Hog1 signaling pathway in A. oligospora. Methods: The function of AoMsn2 was characterized using targeted gene deletion, phenotypic experiments, real-time quantitative PCR, RNA sequencing, untargeted metabolomics, and yeast two-hybrid analysis. Results: Loss of Aomsn2 significantly enlarged and swollen the hyphae, with an increase in septa and a significant decrease in nuclei. In particular, spore yield, spore germination rate, traps, and nematode predation efficiency were remarkably decreased in the mutants. Phenotypic and transcriptomic analyses revealed that AoMsn2 is essential for fatty acid metabolism and autophagic pathways. Additionally, untargeted metabolomic analysis identified an important function of AoMsn2 in the modulation of secondary metabolites. Furtherly, we analyzed the protein interaction network of AoMsn2 based on the Kyoto Encyclopedia of Genes and Genomes pathway map and the online website STRING. Finally, Hog1 and six putative targeted proteins of AoMsn2 were identified by Y2H analysis. Conclusion: Our study reveals that AoMsn2 plays crucial roles in the growth, conidiation, trap development, fatty acid metabolism, and secondary metabolism, as well as establishes a broad basis for understanding the regulatory mechanisms of trap morphogenesis and environmental adaptation in NT fungi.http://www.sciencedirect.com/science/article/pii/S2090123224000523Arthrobotrys oligosporaHog1 signaling pathwayTranscription factor Msn2ConidiationTrap formationSecondary metabolism
spellingShingle Qianqian Liu
Kexin Jiang
Shipeng Duan
Na Zhao
Yanmei Shen
Lirong Zhu
Ke-Qin Zhang
Jinkui Yang
Identification of a transcription factor AoMsn2 of the Hog1 signaling pathway contributes to fungal growth, development and pathogenicity in Arthrobotrys oligospora
Journal of Advanced Research
Arthrobotrys oligospora
Hog1 signaling pathway
Transcription factor Msn2
Conidiation
Trap formation
Secondary metabolism
title Identification of a transcription factor AoMsn2 of the Hog1 signaling pathway contributes to fungal growth, development and pathogenicity in Arthrobotrys oligospora
title_full Identification of a transcription factor AoMsn2 of the Hog1 signaling pathway contributes to fungal growth, development and pathogenicity in Arthrobotrys oligospora
title_fullStr Identification of a transcription factor AoMsn2 of the Hog1 signaling pathway contributes to fungal growth, development and pathogenicity in Arthrobotrys oligospora
title_full_unstemmed Identification of a transcription factor AoMsn2 of the Hog1 signaling pathway contributes to fungal growth, development and pathogenicity in Arthrobotrys oligospora
title_short Identification of a transcription factor AoMsn2 of the Hog1 signaling pathway contributes to fungal growth, development and pathogenicity in Arthrobotrys oligospora
title_sort identification of a transcription factor aomsn2 of the hog1 signaling pathway contributes to fungal growth development and pathogenicity in arthrobotrys oligospora
topic Arthrobotrys oligospora
Hog1 signaling pathway
Transcription factor Msn2
Conidiation
Trap formation
Secondary metabolism
url http://www.sciencedirect.com/science/article/pii/S2090123224000523
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