A Novel Cys2His2 Zinc Finger Homolog of AZF1 Modulates Holocellulase Expression in <italic toggle="yes">Trichoderma reesei</italic>
ABSTRACT Filamentous fungi are remarkable producers of enzymes dedicated to the degradation of sugar polymers found in the plant cell wall. Here, we integrated transcriptomic data to identify novel transcription factors (TFs) related to the control of gene expression of lignocellulosic hydrolases in...
| Main Authors: | , , , , , , , , , , , , |
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| Format: | Article |
| Language: | English |
| Published: |
American Society for Microbiology
2019-08-01
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| Series: | mSystems |
| Subjects: | |
| Online Access: | https://journals.asm.org/doi/10.1128/mSystems.00161-19 |
| _version_ | 1818461167519006720 |
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| author | Amanda Cristina Campos Antonieto Karoline Maria Vieira Nogueira Renato Graciano de Paula Luísa Czamanski Nora Murilo Henrique Anzolini Cassiano Maria-Eugenia Guazzaroni Fausto Almeida Thiago Aparecido da Silva Laure Nicolas Annick Ries Leandro Jose de Assis Gustavo Henrique Goldman Roberto Nascimento Silva Rafael Silva-Rocha |
| author_facet | Amanda Cristina Campos Antonieto Karoline Maria Vieira Nogueira Renato Graciano de Paula Luísa Czamanski Nora Murilo Henrique Anzolini Cassiano Maria-Eugenia Guazzaroni Fausto Almeida Thiago Aparecido da Silva Laure Nicolas Annick Ries Leandro Jose de Assis Gustavo Henrique Goldman Roberto Nascimento Silva Rafael Silva-Rocha |
| author_sort | Amanda Cristina Campos Antonieto |
| collection | DOAJ |
| description | ABSTRACT Filamentous fungi are remarkable producers of enzymes dedicated to the degradation of sugar polymers found in the plant cell wall. Here, we integrated transcriptomic data to identify novel transcription factors (TFs) related to the control of gene expression of lignocellulosic hydrolases in Trichoderma reesei and Aspergillus nidulans. Using various sets of differentially expressed genes, we identified some putative cis-regulatory elements that were related to known binding sites for Saccharomyces cerevisiae TFs. Comparative genomics allowed the identification of six transcriptional factors in filamentous fungi that have corresponding S. cerevisiae homologs. Additionally, a knockout strain of T. reesei lacking one of these TFs (S. cerevisiae AZF1 homolog) displayed strong reductions in the levels of expression of several cellulase-encoding genes in response to both Avicel and sugarcane bagasse, revealing a new player in the complex regulatory network operating in filamentous fungi during plant biomass degradation. Finally, RNA sequencing (RNA-seq) analysis showed the scope of the AZF1 homologue in regulating a number of processes in T. reesei, and chromatin immunoprecipitation-quantitative PCR (ChIP-qPCR) provided evidence for the direct interaction of this TF in the promoter regions of cel7a, cel45a, and swo. Therefore, we identified here a novel TF which plays a positive effect in the expression of cellulase-encoding genes in T. reesei. IMPORTANCE In this work, we used a systems biology approach to map new regulatory interactions in Trichoderma reesei controlling the expression of genes encoding cellulase and hemicellulase. By integrating transcriptomics related to complex biomass degradation, we were able to identify a novel transcriptional regulator which is able to activate the expression of these genes in response to two different cellulose sources. In vivo experimental validation confirmed the role of this new regulator in several other processes related to carbon source utilization and nutrient transport. Therefore, this work revealed novel forms of regulatory interaction in this model system for plant biomass deconstruction and also represented a new approach that could be easy applied to other organisms. |
| first_indexed | 2024-12-14T23:41:50Z |
| format | Article |
| id | doaj.art-84b3ebcb298749af94f24047e0eb7c11 |
| institution | Directory Open Access Journal |
| issn | 2379-5077 |
| language | English |
| last_indexed | 2024-12-14T23:41:50Z |
| publishDate | 2019-08-01 |
| publisher | American Society for Microbiology |
| record_format | Article |
| series | mSystems |
| spelling | doaj.art-84b3ebcb298749af94f24047e0eb7c112022-12-21T22:43:30ZengAmerican Society for MicrobiologymSystems2379-50772019-08-014410.1128/mSystems.00161-19A Novel Cys2His2 Zinc Finger Homolog of AZF1 Modulates Holocellulase Expression in <italic toggle="yes">Trichoderma reesei</italic>Amanda Cristina Campos Antonieto0Karoline Maria Vieira Nogueira1Renato Graciano de Paula2Luísa Czamanski Nora3Murilo Henrique Anzolini Cassiano4Maria-Eugenia Guazzaroni5Fausto Almeida6Thiago Aparecido da Silva7Laure Nicolas Annick Ries8Leandro Jose de Assis9Gustavo Henrique Goldman10Roberto Nascimento Silva11Rafael Silva-Rocha12FMRP—University of São Paulo, Ribeirão Preto, SP, BrazilFMRP—University of São Paulo, Ribeirão Preto, SP, BrazilFMRP—University of São Paulo, Ribeirão Preto, SP, BrazilFMRP—University of São Paulo, Ribeirão Preto, SP, BrazilFMRP—University of São Paulo, Ribeirão Preto, SP, BrazilFFCLRP—University of São Paulo, Ribeirão Preto, SP, BrazilFMRP—University of São Paulo, Ribeirão Preto, SP, BrazilFMRP—University of São Paulo, Ribeirão Preto, SP, BrazilFCFRP—University of São Paulo, Ribeirão Preto, SP, BrazilFCFRP—University of São Paulo, Ribeirão Preto, SP, BrazilFCFRP—University of São Paulo, Ribeirão Preto, SP, BrazilFMRP—University of São Paulo, Ribeirão Preto, SP, BrazilFMRP—University of São Paulo, Ribeirão Preto, SP, BrazilABSTRACT Filamentous fungi are remarkable producers of enzymes dedicated to the degradation of sugar polymers found in the plant cell wall. Here, we integrated transcriptomic data to identify novel transcription factors (TFs) related to the control of gene expression of lignocellulosic hydrolases in Trichoderma reesei and Aspergillus nidulans. Using various sets of differentially expressed genes, we identified some putative cis-regulatory elements that were related to known binding sites for Saccharomyces cerevisiae TFs. Comparative genomics allowed the identification of six transcriptional factors in filamentous fungi that have corresponding S. cerevisiae homologs. Additionally, a knockout strain of T. reesei lacking one of these TFs (S. cerevisiae AZF1 homolog) displayed strong reductions in the levels of expression of several cellulase-encoding genes in response to both Avicel and sugarcane bagasse, revealing a new player in the complex regulatory network operating in filamentous fungi during plant biomass degradation. Finally, RNA sequencing (RNA-seq) analysis showed the scope of the AZF1 homologue in regulating a number of processes in T. reesei, and chromatin immunoprecipitation-quantitative PCR (ChIP-qPCR) provided evidence for the direct interaction of this TF in the promoter regions of cel7a, cel45a, and swo. Therefore, we identified here a novel TF which plays a positive effect in the expression of cellulase-encoding genes in T. reesei. IMPORTANCE In this work, we used a systems biology approach to map new regulatory interactions in Trichoderma reesei controlling the expression of genes encoding cellulase and hemicellulase. By integrating transcriptomics related to complex biomass degradation, we were able to identify a novel transcriptional regulator which is able to activate the expression of these genes in response to two different cellulose sources. In vivo experimental validation confirmed the role of this new regulator in several other processes related to carbon source utilization and nutrient transport. Therefore, this work revealed novel forms of regulatory interaction in this model system for plant biomass deconstruction and also represented a new approach that could be easy applied to other organisms.https://journals.asm.org/doi/10.1128/mSystems.00161-19cis-regulatory elementsholocellulase expressionregulatory networkssystems biology |
| spellingShingle | Amanda Cristina Campos Antonieto Karoline Maria Vieira Nogueira Renato Graciano de Paula Luísa Czamanski Nora Murilo Henrique Anzolini Cassiano Maria-Eugenia Guazzaroni Fausto Almeida Thiago Aparecido da Silva Laure Nicolas Annick Ries Leandro Jose de Assis Gustavo Henrique Goldman Roberto Nascimento Silva Rafael Silva-Rocha A Novel Cys2His2 Zinc Finger Homolog of AZF1 Modulates Holocellulase Expression in <italic toggle="yes">Trichoderma reesei</italic> mSystems cis-regulatory elements holocellulase expression regulatory networks systems biology |
| title | A Novel Cys2His2 Zinc Finger Homolog of AZF1 Modulates Holocellulase Expression in <italic toggle="yes">Trichoderma reesei</italic> |
| title_full | A Novel Cys2His2 Zinc Finger Homolog of AZF1 Modulates Holocellulase Expression in <italic toggle="yes">Trichoderma reesei</italic> |
| title_fullStr | A Novel Cys2His2 Zinc Finger Homolog of AZF1 Modulates Holocellulase Expression in <italic toggle="yes">Trichoderma reesei</italic> |
| title_full_unstemmed | A Novel Cys2His2 Zinc Finger Homolog of AZF1 Modulates Holocellulase Expression in <italic toggle="yes">Trichoderma reesei</italic> |
| title_short | A Novel Cys2His2 Zinc Finger Homolog of AZF1 Modulates Holocellulase Expression in <italic toggle="yes">Trichoderma reesei</italic> |
| title_sort | novel cys2his2 zinc finger homolog of azf1 modulates holocellulase expression in italic toggle yes trichoderma reesei italic |
| topic | cis-regulatory elements holocellulase expression regulatory networks systems biology |
| url | https://journals.asm.org/doi/10.1128/mSystems.00161-19 |
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