The Elongator Subunit Elp3 Regulates Development, Stress Tolerance, Cell Cycle, and Virulence in the Entomopathogenic Fungus <i>Beauveria bassiana</i>
Transcriptional activity is mediated by chromatin remodeling, which in turn is affected by post-translational modifications, including histone acetylation. Histone acetyltransferases (HATs) are capable of promoting euchromatin formation and then activating gene transcription. Here, we characterize t...
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MDPI AG
2022-08-01
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| Series: | Journal of Fungi |
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| Online Access: | https://www.mdpi.com/2309-608X/8/8/834 |
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| author | Qing Cai Juanjuan Wang Jiatao Xie Daohong Jiang Nemat O. Keyhani |
| author_facet | Qing Cai Juanjuan Wang Jiatao Xie Daohong Jiang Nemat O. Keyhani |
| author_sort | Qing Cai |
| collection | DOAJ |
| description | Transcriptional activity is mediated by chromatin remodeling, which in turn is affected by post-translational modifications, including histone acetylation. Histone acetyltransferases (HATs) are capable of promoting euchromatin formation and then activating gene transcription. Here, we characterize the Elp3 GNAT family HAT, which is also a subunit of Elongator complex, in the environmentally and economically important fungal insect pathogen, <i>Beauveria bassiana.</i> BbElp3 showed high localization levels to mitochondria, with some nuclear and cytoplasmic localization also apparent. Targeted gene knockout of <i>BbElp3</i> resulted in impaired asexual development and morphogenesis, reduced tolerances to multiple stress conditions, reduced the ability of the fungus to utilize various carbon/nitrogen sources, increased susceptibility to rapamycin, and attenuated virulence in bioassays using the greater wax moth, <i>Galleria mellonella</i>. The Δ<i>BbElp3</i> mutant also showed disrupted cell cycle, abnormal hyphal septation patterns, and enlarged autophagosomes in vegetative hyphae. Transcriptome analyses revealed differential expression of 775 genes (DEGs), including 336 downregulated and 438 upregulated genes in the Δ<i>BbElp3</i> strain as compared to the wild type. Downregulated genes were mainly enriched in pathways involved in DNA processing and transcription, cell cycle control, cellular transportation, cell defense, and virulence, including hydrophobins, cellular transporters (ABC and MFS multidrug transporters), and insect cuticular degrading enzymes, while upregulated genes were mainly enriched in carbohydrate metabolism and amino acid metabolism. These data indicate pleiotropic effects of BbElp3 in impacting specific cellular processes related to asexual development, cell cycle, autophagy, and virulence. |
| first_indexed | 2024-03-09T04:15:17Z |
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| language | English |
| last_indexed | 2024-03-09T04:15:17Z |
| publishDate | 2022-08-01 |
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| series | Journal of Fungi |
| spelling | doaj.art-a83c8b5cb1264c9fbd2802e761cad2e72023-12-03T13:55:17ZengMDPI AGJournal of Fungi2309-608X2022-08-018883410.3390/jof8080834The Elongator Subunit Elp3 Regulates Development, Stress Tolerance, Cell Cycle, and Virulence in the Entomopathogenic Fungus <i>Beauveria bassiana</i>Qing Cai0Juanjuan Wang1Jiatao Xie2Daohong Jiang3Nemat O. Keyhani4College of Plant Science and Technology, Huazhong Agricultural University, Wuhan 430070, ChinaDepartment of Biotechnology, School of Biological Science and Biotechnology, University of Jinan, Jinan 250022, ChinaCollege of Plant Science and Technology, Huazhong Agricultural University, Wuhan 430070, ChinaCollege of Plant Science and Technology, Huazhong Agricultural University, Wuhan 430070, ChinaDepartment of Microbiology and Cell Science, University of Florida, Gainesville, FL 32611, USATranscriptional activity is mediated by chromatin remodeling, which in turn is affected by post-translational modifications, including histone acetylation. Histone acetyltransferases (HATs) are capable of promoting euchromatin formation and then activating gene transcription. Here, we characterize the Elp3 GNAT family HAT, which is also a subunit of Elongator complex, in the environmentally and economically important fungal insect pathogen, <i>Beauveria bassiana.</i> BbElp3 showed high localization levels to mitochondria, with some nuclear and cytoplasmic localization also apparent. Targeted gene knockout of <i>BbElp3</i> resulted in impaired asexual development and morphogenesis, reduced tolerances to multiple stress conditions, reduced the ability of the fungus to utilize various carbon/nitrogen sources, increased susceptibility to rapamycin, and attenuated virulence in bioassays using the greater wax moth, <i>Galleria mellonella</i>. The Δ<i>BbElp3</i> mutant also showed disrupted cell cycle, abnormal hyphal septation patterns, and enlarged autophagosomes in vegetative hyphae. Transcriptome analyses revealed differential expression of 775 genes (DEGs), including 336 downregulated and 438 upregulated genes in the Δ<i>BbElp3</i> strain as compared to the wild type. Downregulated genes were mainly enriched in pathways involved in DNA processing and transcription, cell cycle control, cellular transportation, cell defense, and virulence, including hydrophobins, cellular transporters (ABC and MFS multidrug transporters), and insect cuticular degrading enzymes, while upregulated genes were mainly enriched in carbohydrate metabolism and amino acid metabolism. These data indicate pleiotropic effects of BbElp3 in impacting specific cellular processes related to asexual development, cell cycle, autophagy, and virulence.https://www.mdpi.com/2309-608X/8/8/834histone acetyltransferasegene transcriptioncell cycleasexual developmentautophagymultidrug transporter |
| spellingShingle | Qing Cai Juanjuan Wang Jiatao Xie Daohong Jiang Nemat O. Keyhani The Elongator Subunit Elp3 Regulates Development, Stress Tolerance, Cell Cycle, and Virulence in the Entomopathogenic Fungus <i>Beauveria bassiana</i> Journal of Fungi histone acetyltransferase gene transcription cell cycle asexual development autophagy multidrug transporter |
| title | The Elongator Subunit Elp3 Regulates Development, Stress Tolerance, Cell Cycle, and Virulence in the Entomopathogenic Fungus <i>Beauveria bassiana</i> |
| title_full | The Elongator Subunit Elp3 Regulates Development, Stress Tolerance, Cell Cycle, and Virulence in the Entomopathogenic Fungus <i>Beauveria bassiana</i> |
| title_fullStr | The Elongator Subunit Elp3 Regulates Development, Stress Tolerance, Cell Cycle, and Virulence in the Entomopathogenic Fungus <i>Beauveria bassiana</i> |
| title_full_unstemmed | The Elongator Subunit Elp3 Regulates Development, Stress Tolerance, Cell Cycle, and Virulence in the Entomopathogenic Fungus <i>Beauveria bassiana</i> |
| title_short | The Elongator Subunit Elp3 Regulates Development, Stress Tolerance, Cell Cycle, and Virulence in the Entomopathogenic Fungus <i>Beauveria bassiana</i> |
| title_sort | elongator subunit elp3 regulates development stress tolerance cell cycle and virulence in the entomopathogenic fungus i beauveria bassiana i |
| topic | histone acetyltransferase gene transcription cell cycle asexual development autophagy multidrug transporter |
| url | https://www.mdpi.com/2309-608X/8/8/834 |
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