Cargando…

The Tudor Domain-Containing Protein BbTdp1 Contributes to Fungal Cell Development, the Cell Cycle, Virulence, and Transcriptional Regulation in the Insect Pathogenic Fungus Beauveria bassiana

Beauveria bassiana is an insect pathogenic fungus that serves as a model system for exploring the mechanisms of fungal development and host-pathogen interactions. Clinical and experimental studies have indicated that SND1 is closely correlated with the progression and invasiveness of common cancers...

Descripción completa

Detalles Bibliográficos
Autores principales: Qiu, Lei, Li, Ze, Zhang, Li, Zhang, Tong-Sheng, Hu, Shun-Juan, Song, Ji-Zheng, Liu, Jia-Hua, Zhang, Jing, Wang, Juan-Juan, Cheng, Wen
Formato: Online Artículo Texto
Lenguaje:English
Publicado: American Society for Microbiology 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8552692/
https://www.ncbi.nlm.nih.gov/pubmed/34378960
http://dx.doi.org/10.1128/spectrum.00564-21
_version_ 1784591432306130944
author Qiu, Lei
Li, Ze
Zhang, Li
Zhang, Tong-Sheng
Hu, Shun-Juan
Song, Ji-Zheng
Liu, Jia-Hua
Zhang, Jing
Wang, Juan-Juan
Cheng, Wen
author_facet Qiu, Lei
Li, Ze
Zhang, Li
Zhang, Tong-Sheng
Hu, Shun-Juan
Song, Ji-Zheng
Liu, Jia-Hua
Zhang, Jing
Wang, Juan-Juan
Cheng, Wen
author_sort Qiu, Lei
collection PubMed
description Beauveria bassiana is an insect pathogenic fungus that serves as a model system for exploring the mechanisms of fungal development and host-pathogen interactions. Clinical and experimental studies have indicated that SND1 is closely correlated with the progression and invasiveness of common cancers as a potential oncogene, but this gene has rarely been studied in fungi. Here, we characterized the contributions of an SND1 ortholog (Tdp1) by constructing a BbTdp1 deletion strain and a complemented strain of B. bassiana. Compared with the wild-type (WT) strain, the ΔBbTdp1 mutant lost conidiation capacity (∼87.7%) and blastospore (∼96.3%) yields, increased sensitivity to chemical stress (4.4 to 54.3%) and heat shock (∼44.2%), and decreased virulence following topical application (∼24.7%) and hemocoel injection (∼40.0%). Flow cytometry readings showed smaller sizes of both conidia and blastospores for ΔBbTdp1 mutants. Transcriptomic data revealed 4,094 differentially expressed genes (|log(2) ratio| > 2 and a q value of <0.05) between ΔBbTdp1 mutants and the WT strain, which accounted for 41.6% of the total genes, indicating that extreme fluctuation in the global gene expression pattern had occurred. Moreover, deletion of BbTdp1 led to an abnormal cell cycle with a longer S phase and shorter G(2)/M and G(0)/G(1) phases of blastospores, and enzyme-linked immunosorbent assay confirmed that the level of phosphorylated cyclin-dependent kinase 1 (Cdk1) in the ΔBbTdp1 strain was ∼31.5% lower than in the WT strain. In summary, our study is the first to report that BbTdp1 plays a vital role in regulating conidia and blastospore yields, fungal morphological changes, and pathogenicity in entomopathogenic fungi. IMPORTANCE In this study, we used Beauveria bassiana as a biological model to report the role of BbTdp1 in entomopathogenic fungi. Our findings indicated that BbTdp1 contributed significantly to cell development, the cell cycle, and virulence in B. bassiana. In addition, deletion of BbTdp1 led to drastic fluctuations in the transcriptional profile. BbTdp1 can be developed as a novel target for B. bassiana development and pathogenicity, which also provides a framework for the study of Tdp1 in other fungi.
format Online
Article
Text
id pubmed-8552692
institution National Center for Biotechnology Information
language English
publishDate 2021
publisher American Society for Microbiology
record_format MEDLINE/PubMed
spelling pubmed-85526922021-11-08 The Tudor Domain-Containing Protein BbTdp1 Contributes to Fungal Cell Development, the Cell Cycle, Virulence, and Transcriptional Regulation in the Insect Pathogenic Fungus Beauveria bassiana Qiu, Lei Li, Ze Zhang, Li Zhang, Tong-Sheng Hu, Shun-Juan Song, Ji-Zheng Liu, Jia-Hua Zhang, Jing Wang, Juan-Juan Cheng, Wen Microbiol Spectr Research Article Beauveria bassiana is an insect pathogenic fungus that serves as a model system for exploring the mechanisms of fungal development and host-pathogen interactions. Clinical and experimental studies have indicated that SND1 is closely correlated with the progression and invasiveness of common cancers as a potential oncogene, but this gene has rarely been studied in fungi. Here, we characterized the contributions of an SND1 ortholog (Tdp1) by constructing a BbTdp1 deletion strain and a complemented strain of B. bassiana. Compared with the wild-type (WT) strain, the ΔBbTdp1 mutant lost conidiation capacity (∼87.7%) and blastospore (∼96.3%) yields, increased sensitivity to chemical stress (4.4 to 54.3%) and heat shock (∼44.2%), and decreased virulence following topical application (∼24.7%) and hemocoel injection (∼40.0%). Flow cytometry readings showed smaller sizes of both conidia and blastospores for ΔBbTdp1 mutants. Transcriptomic data revealed 4,094 differentially expressed genes (|log(2) ratio| > 2 and a q value of <0.05) between ΔBbTdp1 mutants and the WT strain, which accounted for 41.6% of the total genes, indicating that extreme fluctuation in the global gene expression pattern had occurred. Moreover, deletion of BbTdp1 led to an abnormal cell cycle with a longer S phase and shorter G(2)/M and G(0)/G(1) phases of blastospores, and enzyme-linked immunosorbent assay confirmed that the level of phosphorylated cyclin-dependent kinase 1 (Cdk1) in the ΔBbTdp1 strain was ∼31.5% lower than in the WT strain. In summary, our study is the first to report that BbTdp1 plays a vital role in regulating conidia and blastospore yields, fungal morphological changes, and pathogenicity in entomopathogenic fungi. IMPORTANCE In this study, we used Beauveria bassiana as a biological model to report the role of BbTdp1 in entomopathogenic fungi. Our findings indicated that BbTdp1 contributed significantly to cell development, the cell cycle, and virulence in B. bassiana. In addition, deletion of BbTdp1 led to drastic fluctuations in the transcriptional profile. BbTdp1 can be developed as a novel target for B. bassiana development and pathogenicity, which also provides a framework for the study of Tdp1 in other fungi. American Society for Microbiology 2021-08-11 /pmc/articles/PMC8552692/ /pubmed/34378960 http://dx.doi.org/10.1128/spectrum.00564-21 Text en Copyright © 2021 Qiu et al. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Research Article
Qiu, Lei
Li, Ze
Zhang, Li
Zhang, Tong-Sheng
Hu, Shun-Juan
Song, Ji-Zheng
Liu, Jia-Hua
Zhang, Jing
Wang, Juan-Juan
Cheng, Wen
The Tudor Domain-Containing Protein BbTdp1 Contributes to Fungal Cell Development, the Cell Cycle, Virulence, and Transcriptional Regulation in the Insect Pathogenic Fungus Beauveria bassiana
title The Tudor Domain-Containing Protein BbTdp1 Contributes to Fungal Cell Development, the Cell Cycle, Virulence, and Transcriptional Regulation in the Insect Pathogenic Fungus Beauveria bassiana
title_full The Tudor Domain-Containing Protein BbTdp1 Contributes to Fungal Cell Development, the Cell Cycle, Virulence, and Transcriptional Regulation in the Insect Pathogenic Fungus Beauveria bassiana
title_fullStr The Tudor Domain-Containing Protein BbTdp1 Contributes to Fungal Cell Development, the Cell Cycle, Virulence, and Transcriptional Regulation in the Insect Pathogenic Fungus Beauveria bassiana
title_full_unstemmed The Tudor Domain-Containing Protein BbTdp1 Contributes to Fungal Cell Development, the Cell Cycle, Virulence, and Transcriptional Regulation in the Insect Pathogenic Fungus Beauveria bassiana
title_short The Tudor Domain-Containing Protein BbTdp1 Contributes to Fungal Cell Development, the Cell Cycle, Virulence, and Transcriptional Regulation in the Insect Pathogenic Fungus Beauveria bassiana
title_sort tudor domain-containing protein bbtdp1 contributes to fungal cell development, the cell cycle, virulence, and transcriptional regulation in the insect pathogenic fungus beauveria bassiana
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8552692/
https://www.ncbi.nlm.nih.gov/pubmed/34378960
http://dx.doi.org/10.1128/spectrum.00564-21
work_keys_str_mv AT qiulei thetudordomaincontainingproteinbbtdp1contributestofungalcelldevelopmentthecellcyclevirulenceandtranscriptionalregulationintheinsectpathogenicfungusbeauveriabassiana
AT lize thetudordomaincontainingproteinbbtdp1contributestofungalcelldevelopmentthecellcyclevirulenceandtranscriptionalregulationintheinsectpathogenicfungusbeauveriabassiana
AT zhangli thetudordomaincontainingproteinbbtdp1contributestofungalcelldevelopmentthecellcyclevirulenceandtranscriptionalregulationintheinsectpathogenicfungusbeauveriabassiana
AT zhangtongsheng thetudordomaincontainingproteinbbtdp1contributestofungalcelldevelopmentthecellcyclevirulenceandtranscriptionalregulationintheinsectpathogenicfungusbeauveriabassiana
AT hushunjuan thetudordomaincontainingproteinbbtdp1contributestofungalcelldevelopmentthecellcyclevirulenceandtranscriptionalregulationintheinsectpathogenicfungusbeauveriabassiana
AT songjizheng thetudordomaincontainingproteinbbtdp1contributestofungalcelldevelopmentthecellcyclevirulenceandtranscriptionalregulationintheinsectpathogenicfungusbeauveriabassiana
AT liujiahua thetudordomaincontainingproteinbbtdp1contributestofungalcelldevelopmentthecellcyclevirulenceandtranscriptionalregulationintheinsectpathogenicfungusbeauveriabassiana
AT zhangjing thetudordomaincontainingproteinbbtdp1contributestofungalcelldevelopmentthecellcyclevirulenceandtranscriptionalregulationintheinsectpathogenicfungusbeauveriabassiana
AT wangjuanjuan thetudordomaincontainingproteinbbtdp1contributestofungalcelldevelopmentthecellcyclevirulenceandtranscriptionalregulationintheinsectpathogenicfungusbeauveriabassiana
AT chengwen thetudordomaincontainingproteinbbtdp1contributestofungalcelldevelopmentthecellcyclevirulenceandtranscriptionalregulationintheinsectpathogenicfungusbeauveriabassiana
AT qiulei tudordomaincontainingproteinbbtdp1contributestofungalcelldevelopmentthecellcyclevirulenceandtranscriptionalregulationintheinsectpathogenicfungusbeauveriabassiana
AT lize tudordomaincontainingproteinbbtdp1contributestofungalcelldevelopmentthecellcyclevirulenceandtranscriptionalregulationintheinsectpathogenicfungusbeauveriabassiana
AT zhangli tudordomaincontainingproteinbbtdp1contributestofungalcelldevelopmentthecellcyclevirulenceandtranscriptionalregulationintheinsectpathogenicfungusbeauveriabassiana
AT zhangtongsheng tudordomaincontainingproteinbbtdp1contributestofungalcelldevelopmentthecellcyclevirulenceandtranscriptionalregulationintheinsectpathogenicfungusbeauveriabassiana
AT hushunjuan tudordomaincontainingproteinbbtdp1contributestofungalcelldevelopmentthecellcyclevirulenceandtranscriptionalregulationintheinsectpathogenicfungusbeauveriabassiana
AT songjizheng tudordomaincontainingproteinbbtdp1contributestofungalcelldevelopmentthecellcyclevirulenceandtranscriptionalregulationintheinsectpathogenicfungusbeauveriabassiana
AT liujiahua tudordomaincontainingproteinbbtdp1contributestofungalcelldevelopmentthecellcyclevirulenceandtranscriptionalregulationintheinsectpathogenicfungusbeauveriabassiana
AT zhangjing tudordomaincontainingproteinbbtdp1contributestofungalcelldevelopmentthecellcyclevirulenceandtranscriptionalregulationintheinsectpathogenicfungusbeauveriabassiana
AT wangjuanjuan tudordomaincontainingproteinbbtdp1contributestofungalcelldevelopmentthecellcyclevirulenceandtranscriptionalregulationintheinsectpathogenicfungusbeauveriabassiana
AT chengwen tudordomaincontainingproteinbbtdp1contributestofungalcelldevelopmentthecellcyclevirulenceandtranscriptionalregulationintheinsectpathogenicfungusbeauveriabassiana