Phylogenomics analysis of velvet regulators in the fungal kingdom
ABSTRACTAll life forms have evolved to respond appropriately to various environmental and internal cues. In the animal kingdom, the prototypical regulator class of such cellular responses is the Rel homology domain proteins including nuclear factor kappa-light-chain-enhancer of activated B cells (NF...
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| Format: | Article |
| Language: | English |
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American Society for Microbiology
2024-02-01
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| Series: | Microbiology Spectrum |
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| Online Access: | https://journals.asm.org/doi/10.1128/spectrum.03717-23 |
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| author | Wanping Chen Ye-Eun Son He-Jin Cho Dasol Choi Hee-Soo Park Jae-Hyuk Yu |
| author_facet | Wanping Chen Ye-Eun Son He-Jin Cho Dasol Choi Hee-Soo Park Jae-Hyuk Yu |
| author_sort | Wanping Chen |
| collection | DOAJ |
| description | ABSTRACTAll life forms have evolved to respond appropriately to various environmental and internal cues. In the animal kingdom, the prototypical regulator class of such cellular responses is the Rel homology domain proteins including nuclear factor kappa-light-chain-enhancer of activated B cells (NF-κB). Fungi, the close relatives of animals, have also evolved with their own NF-κB-like regulators called velvet family proteins to govern cellular and chemical development. Here, we conducted a detailed investigation of the taxonomic broad presence of velvet proteins. We observed that velvet proteins are widely distributed in the fungal kingdom. Moreover, we have identified and characterized 21 major velvet clades in fungi. We have further revealed that the highly conserved velvet domain is composed of three distinct motifs and acts as an evolutionarily independent domain, which can be shuffled with various functional domains. Such rearrangements of the velvet domain have resulted in the functional and type diversity of the present velvet regulators. Importantly, our in-deep analyses of the primary and 3D structures of the various velvet domains showed that the fungal velvet domains can be divided into two major clans: the VelB and the VosA clans. The 3D structure comparisons revealed a close similarity of the velvet domain with many other eukaryotic DNA-binding proteins, including those of the Rel, Runt, and signal transducer and activator of transcription families, sharing a common β-sandwich fold. Altogether, this study improves our understanding of velvet regulators in the fungal kingdom.IMPORTANCEFungi are the relatives of animals in Opisthokonta and closely associated with human life by interactive ways such as pathogenicity, food, and secondary metabolites including beneficial ones like penicillin and harmful ones like the carcinogenic aflatoxins. Similar to animals, fungi have also evolved with NF-κB-like velvet family regulators. The velvet proteins constitute a large protein family of fungal transcription factors sharing a common velvet domain and play a key role in coordinating fungal secondary metabolism, developmental and differentiation processes. Our current understanding on velvet regulators is mostly from Ascomycota fungi; however, they remain largely unknown outside Ascomycota. Therefore, this study performed a taxonomic broad investigation of velvet proteins across the fungal kingdom and conducted a detailed analysis on velvet distribution, structure, diversity, and evolution. The results provide a holistic view of velvet regulatory system in the fungal kingdom. |
| first_indexed | 2024-03-08T05:19:32Z |
| format | Article |
| id | doaj.art-f8cceec5aeef41d4b846b86f133cef42 |
| institution | Directory Open Access Journal |
| issn | 2165-0497 |
| language | English |
| last_indexed | 2024-03-08T05:19:32Z |
| publishDate | 2024-02-01 |
| publisher | American Society for Microbiology |
| record_format | Article |
| series | Microbiology Spectrum |
| spelling | doaj.art-f8cceec5aeef41d4b846b86f133cef422024-02-06T14:04:54ZengAmerican Society for MicrobiologyMicrobiology Spectrum2165-04972024-02-0112210.1128/spectrum.03717-23Phylogenomics analysis of velvet regulators in the fungal kingdomWanping Chen0Ye-Eun Son1He-Jin Cho2Dasol Choi3Hee-Soo Park4Jae-Hyuk Yu5School of Food Science and Biotechnology, Kyungpook National University, Daegu, South KoreaSchool of Food Science and Biotechnology, Kyungpook National University, Daegu, South KoreaSchool of Food Science and Biotechnology, Kyungpook National University, Daegu, South KoreaDepartment of Bacteriology, University of Wisconsin, Madison, Wisconsin, USASchool of Food Science and Biotechnology, Kyungpook National University, Daegu, South KoreaDepartment of Bacteriology, University of Wisconsin, Madison, Wisconsin, USAABSTRACTAll life forms have evolved to respond appropriately to various environmental and internal cues. In the animal kingdom, the prototypical regulator class of such cellular responses is the Rel homology domain proteins including nuclear factor kappa-light-chain-enhancer of activated B cells (NF-κB). Fungi, the close relatives of animals, have also evolved with their own NF-κB-like regulators called velvet family proteins to govern cellular and chemical development. Here, we conducted a detailed investigation of the taxonomic broad presence of velvet proteins. We observed that velvet proteins are widely distributed in the fungal kingdom. Moreover, we have identified and characterized 21 major velvet clades in fungi. We have further revealed that the highly conserved velvet domain is composed of three distinct motifs and acts as an evolutionarily independent domain, which can be shuffled with various functional domains. Such rearrangements of the velvet domain have resulted in the functional and type diversity of the present velvet regulators. Importantly, our in-deep analyses of the primary and 3D structures of the various velvet domains showed that the fungal velvet domains can be divided into two major clans: the VelB and the VosA clans. The 3D structure comparisons revealed a close similarity of the velvet domain with many other eukaryotic DNA-binding proteins, including those of the Rel, Runt, and signal transducer and activator of transcription families, sharing a common β-sandwich fold. Altogether, this study improves our understanding of velvet regulators in the fungal kingdom.IMPORTANCEFungi are the relatives of animals in Opisthokonta and closely associated with human life by interactive ways such as pathogenicity, food, and secondary metabolites including beneficial ones like penicillin and harmful ones like the carcinogenic aflatoxins. Similar to animals, fungi have also evolved with NF-κB-like velvet family regulators. The velvet proteins constitute a large protein family of fungal transcription factors sharing a common velvet domain and play a key role in coordinating fungal secondary metabolism, developmental and differentiation processes. Our current understanding on velvet regulators is mostly from Ascomycota fungi; however, they remain largely unknown outside Ascomycota. Therefore, this study performed a taxonomic broad investigation of velvet proteins across the fungal kingdom and conducted a detailed analysis on velvet distribution, structure, diversity, and evolution. The results provide a holistic view of velvet regulatory system in the fungal kingdom.https://journals.asm.org/doi/10.1128/spectrum.03717-23velvet regulatorsfungiDNA-bindingRel homology domainnuclear factor kappa-light-chain-enhancer of activated B cells (NF-κB)fungal development |
| spellingShingle | Wanping Chen Ye-Eun Son He-Jin Cho Dasol Choi Hee-Soo Park Jae-Hyuk Yu Phylogenomics analysis of velvet regulators in the fungal kingdom Microbiology Spectrum velvet regulators fungi DNA-binding Rel homology domain nuclear factor kappa-light-chain-enhancer of activated B cells (NF-κB) fungal development |
| title | Phylogenomics analysis of velvet regulators in the fungal kingdom |
| title_full | Phylogenomics analysis of velvet regulators in the fungal kingdom |
| title_fullStr | Phylogenomics analysis of velvet regulators in the fungal kingdom |
| title_full_unstemmed | Phylogenomics analysis of velvet regulators in the fungal kingdom |
| title_short | Phylogenomics analysis of velvet regulators in the fungal kingdom |
| title_sort | phylogenomics analysis of velvet regulators in the fungal kingdom |
| topic | velvet regulators fungi DNA-binding Rel homology domain nuclear factor kappa-light-chain-enhancer of activated B cells (NF-κB) fungal development |
| url | https://journals.asm.org/doi/10.1128/spectrum.03717-23 |
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