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...

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Autores principales:	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
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2019
Materias:	cis-regulatory elements holocellulase expression regulatory networks systems biology Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/84b3ebcb298749af94f24047e0eb7c11
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spelling	oai:doaj.org-article:84b3ebcb298749af94f24047e0eb7c112021-12-02T19:46:18ZA Novel Cys2His2 Zinc Finger Homolog of AZF1 Modulates Holocellulase Expression in <italic toggle="yes">Trichoderma reesei</italic>10.1128/mSystems.00161-192379-5077https://doaj.org/article/84b3ebcb298749af94f24047e0eb7c112019-08-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSystems.00161-19https://doaj.org/toc/2379-5077ABSTRACT 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.Amanda Cristina Campos AntonietoKaroline Maria Vieira NogueiraRenato Graciano de PaulaLuísa Czamanski NoraMurilo Henrique Anzolini CassianoMaria-Eugenia GuazzaroniFausto AlmeidaThiago Aparecido da SilvaLaure Nicolas Annick RiesLeandro Jose de AssisGustavo Henrique GoldmanRoberto Nascimento SilvaRafael Silva-RochaAmerican Society for Microbiologyarticlecis-regulatory elementsholocellulase expressionregulatory networkssystems biologyMicrobiologyQR1-502ENmSystems, Vol 4, Iss 4 (2019)
institution	DOAJ
collection	DOAJ
language	EN
topic	cis-regulatory elements holocellulase expression regulatory networks systems biology Microbiology QR1-502
spellingShingle	cis-regulatory elements holocellulase expression regulatory networks systems biology Microbiology QR1-502 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>
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.
format	article
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
title	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_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_sort	novel cys2his2 zinc finger homolog of azf1 modulates holocellulase expression in <italic toggle="yes">trichoderma reesei</italic>
publisher	American Society for Microbiology
publishDate	2019
url	https://doaj.org/article/84b3ebcb298749af94f24047e0eb7c11
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A Novel Cys2His2 Zinc Finger Homolog of AZF1 Modulates Holocellulase Expression in <italic toggle="yes">Trichoderma reesei</italic>

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