Systematic characterization of Ustilago maydis sirtuins shows Sir2 as a modulator of pathogenic gene expression

Phytopathogenic fungi must adapt to the different environmental conditions found during infection and avoid the immune response of the plant. For these adaptations, fungi must tightly control gene expression, allowing sequential changes in transcriptional programs. In addition to transcription facto...

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Autores: Navarrete, Blanca, Ibeas, José I., Barrales, Ramón R.
Tipo de documento: artigo
Estado:Versão publicada
Data de publicação:2023
País:España
Recursos:Consejo Superior de Investigaciones Científicas (CSIC)
Repositório:DIGITAL.CSIC. Repositorio Institucional del CSIC
OAI Identifier:oai:digital.csic.es:10261/336932
Acesso em linha:http://hdl.handle.net/10261/336932
Access Level:Acceso aberto
Palavra-chave:Sirtuins
Phytopathogenesis
HDAC
Histone deacetylases
Gene regulation
Plant infection
Filamentation
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spelling Systematic characterization of Ustilago maydis sirtuins shows Sir2 as a modulator of pathogenic gene expressionNavarrete, BlancaIbeas, José I.Barrales, Ramón R.SirtuinsPhytopathogenesisHDACHistone deacetylasesGene regulationPlant infectionFilamentationPhytopathogenic fungi must adapt to the different environmental conditions found during infection and avoid the immune response of the plant. For these adaptations, fungi must tightly control gene expression, allowing sequential changes in transcriptional programs. In addition to transcription factors, chromatin modification is used by eukaryotic cells as a different layer of transcriptional control. Specifically, the acetylation of histones is one of the chromatin modifications with a strong impact on gene expression. Hyperacetylated regions usually correlate with high transcription and hypoacetylated areas with low transcription. Thus, histone deacetylases (HDACs) commonly act as repressors of transcription. One member of the family of HDACs is represented by sirtuins, which are deacetylases dependent on NAD+, and, thus, their activity is considered to be related to the physiological stage of the cells. This property makes sirtuins good regulators during environmental changes. However, only a few examples exist, and with differences in the extent of the implication of the role of sirtuins during fungal phytopathogenesis. In this work, we have performed a systematic study of sirtuins in the maize pathogen Ustilago maydis, finding Sir2 to be involved in the dimorphic switch from yeast cell to filament and pathogenic development. Specifically, the deletion of sir2 promotes filamentation, whereas its overexpression highly reduces tumor formation in the plant. Moreover, transcriptomic analysis revealed that Sir2 represses genes that are expressed during biotrophism development. Interestingly, our results suggest that this repressive effect is not through histone deacetylation, indicating a different target of Sir2 in this fungus.This research was supported by MCIN/AEI/10.13039/501100011033/FEDER, grant numbers BIO2016-80180-P and PID2019-110477GB-I00 to JII. BN was awarded by grant BES-2017- 079765 MCIN/AEI/FEDER.Peer reviewedFrontiers MediaMinisterio de Ciencia, Innovación y Universidades (España)Agencia Estatal de Investigación (España)Ministerio de Economía y Competitividad (España)Consejo Superior de Investigaciones Científicas [https://ror.org/02gfc7t72]2023202320232023info:eu-repo/semantics/articlehttp://purl.org/coar/resource_type/c_6501Publisher's versioninfo:eu-repo/semantics/publishedVersionapplication/pdfhttp://hdl.handle.net/10261/336932reponame:DIGITAL.CSIC. Repositorio Institucional del CSICinstname:Consejo Superior de Investigaciones Científicas (CSIC)Inglés#PLACEHOLDER_PARENT_METADATA_VALUE##PLACEHOLDER_PARENT_METADATA_VALUE##PLACEHOLDER_PARENT_METADATA_VALUE#info:eu-repo/grantAgreement/MINECO//BIO2016-80180-Pinfo:eu-repo/grantAgreement/AEI/Plan Estatal de Investigación Científica y Técnica y de Innovación 2017-2020/PID2019-110477GB-I00info:eu-repo/grantAgreement/AEI/Plan Estatal de Investigación Científica y Técnica y de Innovación 2017-2020/BES-2017-079765The underlying dataset has been published as supplementary material of the article in the publisher platform at DOI https://doi.org/10.3389/fmicb.2023.1157990http://dx.doi.org/10.3389/fmicb.2023.1157990Síinfo:eu-repo/semantics/openAccessoai:digital.csic.es:10261/3369322026-05-22T06:33:51Z
dc.title.none.fl_str_mv Systematic characterization of Ustilago maydis sirtuins shows Sir2 as a modulator of pathogenic gene expression
title Systematic characterization of Ustilago maydis sirtuins shows Sir2 as a modulator of pathogenic gene expression
spellingShingle Systematic characterization of Ustilago maydis sirtuins shows Sir2 as a modulator of pathogenic gene expression
Navarrete, Blanca
Sirtuins
Phytopathogenesis
HDAC
Histone deacetylases
Gene regulation
Plant infection
Filamentation
title_short Systematic characterization of Ustilago maydis sirtuins shows Sir2 as a modulator of pathogenic gene expression
title_full Systematic characterization of Ustilago maydis sirtuins shows Sir2 as a modulator of pathogenic gene expression
title_fullStr Systematic characterization of Ustilago maydis sirtuins shows Sir2 as a modulator of pathogenic gene expression
title_full_unstemmed Systematic characterization of Ustilago maydis sirtuins shows Sir2 as a modulator of pathogenic gene expression
title_sort Systematic characterization of Ustilago maydis sirtuins shows Sir2 as a modulator of pathogenic gene expression
dc.creator.none.fl_str_mv Navarrete, Blanca
Ibeas, José I.
Barrales, Ramón R.
author Navarrete, Blanca
author_facet Navarrete, Blanca
Ibeas, José I.
Barrales, Ramón R.
author_role author
author2 Ibeas, José I.
Barrales, Ramón R.
author2_role author
author
dc.contributor.none.fl_str_mv Ministerio de Ciencia, Innovación y Universidades (España)
Agencia Estatal de Investigación (España)
Ministerio de Economía y Competitividad (España)
Consejo Superior de Investigaciones Científicas [https://ror.org/02gfc7t72]
dc.subject.none.fl_str_mv Sirtuins
Phytopathogenesis
HDAC
Histone deacetylases
Gene regulation
Plant infection
Filamentation
topic Sirtuins
Phytopathogenesis
HDAC
Histone deacetylases
Gene regulation
Plant infection
Filamentation
description Phytopathogenic fungi must adapt to the different environmental conditions found during infection and avoid the immune response of the plant. For these adaptations, fungi must tightly control gene expression, allowing sequential changes in transcriptional programs. In addition to transcription factors, chromatin modification is used by eukaryotic cells as a different layer of transcriptional control. Specifically, the acetylation of histones is one of the chromatin modifications with a strong impact on gene expression. Hyperacetylated regions usually correlate with high transcription and hypoacetylated areas with low transcription. Thus, histone deacetylases (HDACs) commonly act as repressors of transcription. One member of the family of HDACs is represented by sirtuins, which are deacetylases dependent on NAD+, and, thus, their activity is considered to be related to the physiological stage of the cells. This property makes sirtuins good regulators during environmental changes. However, only a few examples exist, and with differences in the extent of the implication of the role of sirtuins during fungal phytopathogenesis. In this work, we have performed a systematic study of sirtuins in the maize pathogen Ustilago maydis, finding Sir2 to be involved in the dimorphic switch from yeast cell to filament and pathogenic development. Specifically, the deletion of sir2 promotes filamentation, whereas its overexpression highly reduces tumor formation in the plant. Moreover, transcriptomic analysis revealed that Sir2 represses genes that are expressed during biotrophism development. Interestingly, our results suggest that this repressive effect is not through histone deacetylation, indicating a different target of Sir2 in this fungus.
publishDate 2023
dc.date.none.fl_str_mv 2023
2023
2023
2023
dc.type.none.fl_str_mv info:eu-repo/semantics/article
http://purl.org/coar/resource_type/c_6501
Publisher's version
info:eu-repo/semantics/publishedVersion
format article
status_str publishedVersion
dc.identifier.none.fl_str_mv http://hdl.handle.net/10261/336932
url http://hdl.handle.net/10261/336932
dc.language.none.fl_str_mv Inglés
language_invalid_str_mv Inglés
dc.relation.none.fl_str_mv #PLACEHOLDER_PARENT_METADATA_VALUE#
#PLACEHOLDER_PARENT_METADATA_VALUE#
#PLACEHOLDER_PARENT_METADATA_VALUE#
info:eu-repo/grantAgreement/MINECO//BIO2016-80180-P
info:eu-repo/grantAgreement/AEI/Plan Estatal de Investigación Científica y Técnica y de Innovación 2017-2020/PID2019-110477GB-I00
info:eu-repo/grantAgreement/AEI/Plan Estatal de Investigación Científica y Técnica y de Innovación 2017-2020/BES-2017-079765
The underlying dataset has been published as supplementary material of the article in the publisher platform at DOI https://doi.org/10.3389/fmicb.2023.1157990
http://dx.doi.org/10.3389/fmicb.2023.1157990
Sí
dc.rights.none.fl_str_mv info:eu-repo/semantics/openAccess
eu_rights_str_mv openAccess
dc.format.none.fl_str_mv application/pdf
dc.publisher.none.fl_str_mv Frontiers Media
publisher.none.fl_str_mv Frontiers Media
dc.source.none.fl_str_mv reponame:DIGITAL.CSIC. Repositorio Institucional del CSIC
instname:Consejo Superior de Investigaciones Científicas (CSIC)
instname_str Consejo Superior de Investigaciones Científicas (CSIC)
reponame_str DIGITAL.CSIC. Repositorio Institucional del CSIC
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