Cargando…

The Elongator Subunit Elp3 Regulates Development, Stress Tolerance, Cell Cycle, and Virulence in the Entomopathogenic Fungus Beauveria bassiana

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...

Descripción completa

Detalles Bibliográficos
Autores principales: Cai, Qing, Wang, Juanjuan, Xie, Jiatao, Jiang, Daohong, Keyhani, Nemat O.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: MDPI 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9410351/
https://www.ncbi.nlm.nih.gov/pubmed/36012822
http://dx.doi.org/10.3390/jof8080834
_version_ 1784775072419938304
author Cai, Qing
Wang, Juanjuan
Xie, Jiatao
Jiang, Daohong
Keyhani, Nemat O.
author_facet Cai, Qing
Wang, Juanjuan
Xie, Jiatao
Jiang, Daohong
Keyhani, Nemat O.
author_sort Cai, Qing
collection PubMed
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, Beauveria bassiana. BbElp3 showed high localization levels to mitochondria, with some nuclear and cytoplasmic localization also apparent. Targeted gene knockout of BbElp3 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, Galleria mellonella. The ΔBbElp3 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 ΔBbElp3 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.
format Online
Article
Text
id pubmed-9410351
institution National Center for Biotechnology Information
language English
publishDate 2022
publisher MDPI
record_format MEDLINE/PubMed
spelling pubmed-94103512022-08-26 The Elongator Subunit Elp3 Regulates Development, Stress Tolerance, Cell Cycle, and Virulence in the Entomopathogenic Fungus Beauveria bassiana Cai, Qing Wang, Juanjuan Xie, Jiatao Jiang, Daohong Keyhani, Nemat O. J Fungi (Basel) Article 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, Beauveria bassiana. BbElp3 showed high localization levels to mitochondria, with some nuclear and cytoplasmic localization also apparent. Targeted gene knockout of BbElp3 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, Galleria mellonella. The ΔBbElp3 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 ΔBbElp3 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. MDPI 2022-08-10 /pmc/articles/PMC9410351/ /pubmed/36012822 http://dx.doi.org/10.3390/jof8080834 Text en © 2022 by the authors. https://creativecommons.org/licenses/by/4.0/Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
spellingShingle Article
Cai, Qing
Wang, Juanjuan
Xie, Jiatao
Jiang, Daohong
Keyhani, Nemat O.
The Elongator Subunit Elp3 Regulates Development, Stress Tolerance, Cell Cycle, and Virulence in the Entomopathogenic Fungus Beauveria bassiana
title The Elongator Subunit Elp3 Regulates Development, Stress Tolerance, Cell Cycle, and Virulence in the Entomopathogenic Fungus Beauveria bassiana
title_full The Elongator Subunit Elp3 Regulates Development, Stress Tolerance, Cell Cycle, and Virulence in the Entomopathogenic Fungus Beauveria bassiana
title_fullStr The Elongator Subunit Elp3 Regulates Development, Stress Tolerance, Cell Cycle, and Virulence in the Entomopathogenic Fungus Beauveria bassiana
title_full_unstemmed The Elongator Subunit Elp3 Regulates Development, Stress Tolerance, Cell Cycle, and Virulence in the Entomopathogenic Fungus Beauveria bassiana
title_short The Elongator Subunit Elp3 Regulates Development, Stress Tolerance, Cell Cycle, and Virulence in the Entomopathogenic Fungus Beauveria bassiana
title_sort elongator subunit elp3 regulates development, stress tolerance, cell cycle, and virulence in the entomopathogenic fungus beauveria bassiana
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9410351/
https://www.ncbi.nlm.nih.gov/pubmed/36012822
http://dx.doi.org/10.3390/jof8080834
work_keys_str_mv AT caiqing theelongatorsubunitelp3regulatesdevelopmentstresstolerancecellcycleandvirulenceintheentomopathogenicfungusbeauveriabassiana
AT wangjuanjuan theelongatorsubunitelp3regulatesdevelopmentstresstolerancecellcycleandvirulenceintheentomopathogenicfungusbeauveriabassiana
AT xiejiatao theelongatorsubunitelp3regulatesdevelopmentstresstolerancecellcycleandvirulenceintheentomopathogenicfungusbeauveriabassiana
AT jiangdaohong theelongatorsubunitelp3regulatesdevelopmentstresstolerancecellcycleandvirulenceintheentomopathogenicfungusbeauveriabassiana
AT keyhaninemato theelongatorsubunitelp3regulatesdevelopmentstresstolerancecellcycleandvirulenceintheentomopathogenicfungusbeauveriabassiana
AT caiqing elongatorsubunitelp3regulatesdevelopmentstresstolerancecellcycleandvirulenceintheentomopathogenicfungusbeauveriabassiana
AT wangjuanjuan elongatorsubunitelp3regulatesdevelopmentstresstolerancecellcycleandvirulenceintheentomopathogenicfungusbeauveriabassiana
AT xiejiatao elongatorsubunitelp3regulatesdevelopmentstresstolerancecellcycleandvirulenceintheentomopathogenicfungusbeauveriabassiana
AT jiangdaohong elongatorsubunitelp3regulatesdevelopmentstresstolerancecellcycleandvirulenceintheentomopathogenicfungusbeauveriabassiana
AT keyhaninemato elongatorsubunitelp3regulatesdevelopmentstresstolerancecellcycleandvirulenceintheentomopathogenicfungusbeauveriabassiana