A multilayered regulatory network mediated by protein phosphatase 4 controls carbon catabolite repression and de-repression in Magnaporthe oryzae
Abstract Carbon catabolite repression (CCR) and de-repression (CCDR) are critical for fungal development and pathogenicity, yet the underlying regulatory mechanisms remain poorly understood in pathogenic fungi. Here, we identify a serine/threonine protein phosphatase catalytic subunit, Pp4c, as esse...
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Nature Portfolio
2025-01-01
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| Series: | Communications Biology |
| Online Access: | https://doi.org/10.1038/s42003-025-07581-3 |
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| author | Zhicheng Huang Qing Wang Yan Li Pengyun Huang Jian Liao Jing Wang Hui Li Yingying Cai Jiaoyu Wang Xiaohong Liu Fu-Cheng Lin Jianping Lu |
| author_facet | Zhicheng Huang Qing Wang Yan Li Pengyun Huang Jian Liao Jing Wang Hui Li Yingying Cai Jiaoyu Wang Xiaohong Liu Fu-Cheng Lin Jianping Lu |
| author_sort | Zhicheng Huang |
| collection | DOAJ |
| description | Abstract Carbon catabolite repression (CCR) and de-repression (CCDR) are critical for fungal development and pathogenicity, yet the underlying regulatory mechanisms remain poorly understood in pathogenic fungi. Here, we identify a serine/threonine protein phosphatase catalytic subunit, Pp4c, as essential for growth, conidiation, virulence, and the utilization of carbohydrates and lipids in Magnaporthe oryzae. We demonstrate that the protein phosphatase 4 complex (Pp4c and Smek1 subunits), the AMP-activated protein kinase (AMPK) Snf1, and the transcriptional regulators CreA (repressor) and Crf1 (activator) collaboratively regulate the utilization of non-preferred carbon sources. Protein interaction and phosphorylation analyses reveal that under glucose-rich conditions, Snf1 and Smek1 directly regulate the phosphorylation status of CreA and Crf1. In contrast, under l-arabinose-rich conditions, Snf1 indirectly modulates the dephosphorylation of these transcription factors via Pp4c and Smek1. Phosphorylation-mediated activation or inactivation of CreA and Crf1 drives CCR and CCDR, thereby governing the metabolism of carbon sources derived from plant cell walls and contributing to fungal pathogenicity. These findings provide deep insights into the regulation of CCR and CCDR, emphasizing their significance in carbon metabolism and pathogenicity in phytopathogenic fungi. |
| format | Article |
| id | doaj-art-ec067ef67a8840248b679b6be44e3f5c |
| institution | Kabale University |
| issn | 2399-3642 |
| language | English |
| publishDate | 2025-01-01 |
| publisher | Nature Portfolio |
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| spelling | doaj-art-ec067ef67a8840248b679b6be44e3f5c2025-02-02T12:37:13ZengNature PortfolioCommunications Biology2399-36422025-01-018111610.1038/s42003-025-07581-3A multilayered regulatory network mediated by protein phosphatase 4 controls carbon catabolite repression and de-repression in Magnaporthe oryzaeZhicheng Huang0Qing Wang1Yan Li2Pengyun Huang3Jian Liao4Jing Wang5Hui Li6Yingying Cai7Jiaoyu Wang8Xiaohong Liu9Fu-Cheng Lin10Jianping Lu11Xianghu Laboratory, College of Life Sciences, Zhejiang UniversityXianghu Laboratory, College of Life Sciences, Zhejiang UniversityXianghu Laboratory, College of Life Sciences, Zhejiang UniversitySchool of Medicine, Linyi UniversityInstitute of Biotechnology, Zhejiang UniversityState Key Laboratory for Managing Biotic and Chemical Threats to the Quality and Safety of Agro-Products, Key Laboratory of Agricultural Microbiome of MARA and Zhejiang Province, Key Laboratory of Biotechnology in Plant Protection of MARA and Zhejiang Province, Institute of Plant Protection and Microbiology, Zhejiang Academy of Agricultural SciencesXianghu Laboratory, College of Life Sciences, Zhejiang UniversityState Key Laboratory for Managing Biotic and Chemical Threats to the Quality and Safety of Agro-Products, Key Laboratory of Agricultural Microbiome of MARA and Zhejiang Province, Key Laboratory of Biotechnology in Plant Protection of MARA and Zhejiang Province, Institute of Plant Protection and Microbiology, Zhejiang Academy of Agricultural SciencesState Key Laboratory for Managing Biotic and Chemical Threats to the Quality and Safety of Agro-Products, Key Laboratory of Agricultural Microbiome of MARA and Zhejiang Province, Key Laboratory of Biotechnology in Plant Protection of MARA and Zhejiang Province, Institute of Plant Protection and Microbiology, Zhejiang Academy of Agricultural SciencesInstitute of Biotechnology, Zhejiang UniversityXianghu Laboratory, College of Life Sciences, Zhejiang UniversityXianghu Laboratory, College of Life Sciences, Zhejiang UniversityAbstract Carbon catabolite repression (CCR) and de-repression (CCDR) are critical for fungal development and pathogenicity, yet the underlying regulatory mechanisms remain poorly understood in pathogenic fungi. Here, we identify a serine/threonine protein phosphatase catalytic subunit, Pp4c, as essential for growth, conidiation, virulence, and the utilization of carbohydrates and lipids in Magnaporthe oryzae. We demonstrate that the protein phosphatase 4 complex (Pp4c and Smek1 subunits), the AMP-activated protein kinase (AMPK) Snf1, and the transcriptional regulators CreA (repressor) and Crf1 (activator) collaboratively regulate the utilization of non-preferred carbon sources. Protein interaction and phosphorylation analyses reveal that under glucose-rich conditions, Snf1 and Smek1 directly regulate the phosphorylation status of CreA and Crf1. In contrast, under l-arabinose-rich conditions, Snf1 indirectly modulates the dephosphorylation of these transcription factors via Pp4c and Smek1. Phosphorylation-mediated activation or inactivation of CreA and Crf1 drives CCR and CCDR, thereby governing the metabolism of carbon sources derived from plant cell walls and contributing to fungal pathogenicity. These findings provide deep insights into the regulation of CCR and CCDR, emphasizing their significance in carbon metabolism and pathogenicity in phytopathogenic fungi.https://doi.org/10.1038/s42003-025-07581-3 |
| spellingShingle | Zhicheng Huang Qing Wang Yan Li Pengyun Huang Jian Liao Jing Wang Hui Li Yingying Cai Jiaoyu Wang Xiaohong Liu Fu-Cheng Lin Jianping Lu A multilayered regulatory network mediated by protein phosphatase 4 controls carbon catabolite repression and de-repression in Magnaporthe oryzae Communications Biology |
| title | A multilayered regulatory network mediated by protein phosphatase 4 controls carbon catabolite repression and de-repression in Magnaporthe oryzae |
| title_full | A multilayered regulatory network mediated by protein phosphatase 4 controls carbon catabolite repression and de-repression in Magnaporthe oryzae |
| title_fullStr | A multilayered regulatory network mediated by protein phosphatase 4 controls carbon catabolite repression and de-repression in Magnaporthe oryzae |
| title_full_unstemmed | A multilayered regulatory network mediated by protein phosphatase 4 controls carbon catabolite repression and de-repression in Magnaporthe oryzae |
| title_short | A multilayered regulatory network mediated by protein phosphatase 4 controls carbon catabolite repression and de-repression in Magnaporthe oryzae |
| title_sort | multilayered regulatory network mediated by protein phosphatase 4 controls carbon catabolite repression and de repression in magnaporthe oryzae |
| url | https://doi.org/10.1038/s42003-025-07581-3 |
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