Increase of histone acetylation by suberoylanilide hydroxamic acid enhances microspore reprogramming and expression of somatic embryogenesis transcription factors in Brassica napus

In vivo, microspores in the anthers follow the gametophytic development pathway, culminating in the formation of pollen grains. Conversely, in vitro, under stress treatments, microspores can be reprogrammed into totipotent cells, initiating an embryogenic pathway that produces haploid and double-hap...

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Autores: Pérez-Pérez, Yolanda, Berenguer, Eduardo, Carneros, Elena, Testillano, Pilar S.
Tipo de recurso: artículo
Estado:Versión publicada
Fecha de publicación:2024
País:España
Institución:Consejo Superior de Investigaciones Científicas (CSIC)
Repositorio:DIGITAL.CSIC. Repositorio Institucional del CSIC
OAI Identifier:oai:digital.csic.es:10261/374169
Acceso en línea:http://hdl.handle.net/10261/374169
Access Level:acceso abierto
Palabra clave:Microspore embryogenesis
Pollen development
Epigenetics
Histone post-translational modifications
SAHA
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spelling Increase of histone acetylation by suberoylanilide hydroxamic acid enhances microspore reprogramming and expression of somatic embryogenesis transcription factors in Brassica napusPérez-Pérez, YolandaBerenguer, EduardoCarneros, ElenaTestillano, Pilar S.Microspore embryogenesisPollen developmentEpigeneticsHistone post-translational modificationsSAHAIn vivo, microspores in the anthers follow the gametophytic development pathway, culminating in the formation of pollen grains. Conversely, in vitro, under stress treatments, microspores can be reprogrammed into totipotent cells, initiating an embryogenic pathway that produces haploid and double-haploid embryos, which are important biotechnological tools in plant breeding. There is growing evidence that epigenetic reprogramming occurs during microspore embryogenesis through DNA methylation, but less is known about the role of histone modifications. This study investigates the dynamics of histone acetylation during the two microspore developmental pathways, microspore embryogenesis and pollen development, in Brassica napus. We analyzed histone H3 and H4 acetylation levels, histone acetyltransferase (HAT) activity and expression of HAC5 acetyltransferase using immunofluorescence, enzymatic activity assays, ELISA-like tests, and qPCR. Results showed a decrease in global histone acetylation levels during pollen maturation, correlated with reduced HAT activity and downregulation of the BnHAC5-like gene. In contrast, stress-induced microspore reprogramming led to increased histone acetylation levels, enhanced HAT activity, and upregulation of BnHAC5-like. Treatment with suberoylanilide hydroxamic acid (SAHA), a histone deacetylase inhibitor widely used in animal research but barely applied to plants, enhanced microspore embryogenesis initiation and proembryo formation, while increased histone acetylation levels. SAHA-treated proembryos showed higher expression than control of key embryogenesis transcription factors BnFUS3, BnAGL15, and BnLEC2, suggesting that histone hyperacetylation facilitates transcriptional activation of essential genes for somatic embryogenesis initiation. These findings provided new insights into the epigenetic regulation of this process and revealed new opportunities with histone epigenetic regulator inhibitors, to improve microspore embryogenesis induction for crop improvement.Supported by Projects PID2020–113018RB-I00 and PID2023–146824OB-I00 (funded by MCIN/AEI /10.13039/501100011033), TED2021-129633B-I00 and CPP2021–008750 (funded by MCIN/AEI /10.13039/501100011033 and NextGenerationEU/ PRTR).Peer reviewedElsevierMinisterio de Ciencia e Innovación (España)Agencia Estatal de Investigación (España)European CommissionPérez-Pérez, Yolanda [0000-0001-9490-098X]Berenguer, Eduardo [0000-0002-0902-1057]Carneros, Elena [0000-0003-2066-6320]Testillano, Pilar S. [0000-0003-4509-7646]Consejo Superior de Investigaciones Científicas [https://ror.org/02gfc7t72]202420242025info:eu-repo/semantics/articlehttp://purl.org/coar/resource_type/c_6501Publisher's versioninfo:eu-repo/semantics/publishedVersionhttp://hdl.handle.net/10261/374169reponame:DIGITAL.CSIC. Repositorio Institucional del CSICinstname:Consejo Superior de Investigaciones Científicas (CSIC)Inglés#PLACEHOLDER_PARENT_METADATA_VALUE##PLACEHOLDER_PARENT_METADATA_VALUE#info:eu-repo/grantAgreement/AEI/Plan Estatal de Investigación Científica y Técnica y de Innovación 2017-2020/PID2020-113018RB-I00info:eu-repo/grantAgreement/AEI/Plan Estatal de Investigación Científica y Técnica y de Innovación 2021-2023/CPP2021-008750https://doi.org/10.1016/j.plantsci.2024.112318Síinfo:eu-repo/semantics/openAccessoai:digital.csic.es:10261/3741692026-05-22T06:33:51Z
dc.title.none.fl_str_mv Increase of histone acetylation by suberoylanilide hydroxamic acid enhances microspore reprogramming and expression of somatic embryogenesis transcription factors in Brassica napus
title Increase of histone acetylation by suberoylanilide hydroxamic acid enhances microspore reprogramming and expression of somatic embryogenesis transcription factors in Brassica napus
spellingShingle Increase of histone acetylation by suberoylanilide hydroxamic acid enhances microspore reprogramming and expression of somatic embryogenesis transcription factors in Brassica napus
Pérez-Pérez, Yolanda
Microspore embryogenesis
Pollen development
Epigenetics
Histone post-translational modifications
SAHA
title_short Increase of histone acetylation by suberoylanilide hydroxamic acid enhances microspore reprogramming and expression of somatic embryogenesis transcription factors in Brassica napus
title_full Increase of histone acetylation by suberoylanilide hydroxamic acid enhances microspore reprogramming and expression of somatic embryogenesis transcription factors in Brassica napus
title_fullStr Increase of histone acetylation by suberoylanilide hydroxamic acid enhances microspore reprogramming and expression of somatic embryogenesis transcription factors in Brassica napus
title_full_unstemmed Increase of histone acetylation by suberoylanilide hydroxamic acid enhances microspore reprogramming and expression of somatic embryogenesis transcription factors in Brassica napus
title_sort Increase of histone acetylation by suberoylanilide hydroxamic acid enhances microspore reprogramming and expression of somatic embryogenesis transcription factors in Brassica napus
dc.creator.none.fl_str_mv Pérez-Pérez, Yolanda
Berenguer, Eduardo
Carneros, Elena
Testillano, Pilar S.
author Pérez-Pérez, Yolanda
author_facet Pérez-Pérez, Yolanda
Berenguer, Eduardo
Carneros, Elena
Testillano, Pilar S.
author_role author
author2 Berenguer, Eduardo
Carneros, Elena
Testillano, Pilar S.
author2_role author
author
author
dc.contributor.none.fl_str_mv Ministerio de Ciencia e Innovación (España)
Agencia Estatal de Investigación (España)
European Commission
Pérez-Pérez, Yolanda [0000-0001-9490-098X]
Berenguer, Eduardo [0000-0002-0902-1057]
Carneros, Elena [0000-0003-2066-6320]
Testillano, Pilar S. [0000-0003-4509-7646]
Consejo Superior de Investigaciones Científicas [https://ror.org/02gfc7t72]
dc.subject.none.fl_str_mv Microspore embryogenesis
Pollen development
Epigenetics
Histone post-translational modifications
SAHA
topic Microspore embryogenesis
Pollen development
Epigenetics
Histone post-translational modifications
SAHA
description In vivo, microspores in the anthers follow the gametophytic development pathway, culminating in the formation of pollen grains. Conversely, in vitro, under stress treatments, microspores can be reprogrammed into totipotent cells, initiating an embryogenic pathway that produces haploid and double-haploid embryos, which are important biotechnological tools in plant breeding. There is growing evidence that epigenetic reprogramming occurs during microspore embryogenesis through DNA methylation, but less is known about the role of histone modifications. This study investigates the dynamics of histone acetylation during the two microspore developmental pathways, microspore embryogenesis and pollen development, in Brassica napus. We analyzed histone H3 and H4 acetylation levels, histone acetyltransferase (HAT) activity and expression of HAC5 acetyltransferase using immunofluorescence, enzymatic activity assays, ELISA-like tests, and qPCR. Results showed a decrease in global histone acetylation levels during pollen maturation, correlated with reduced HAT activity and downregulation of the BnHAC5-like gene. In contrast, stress-induced microspore reprogramming led to increased histone acetylation levels, enhanced HAT activity, and upregulation of BnHAC5-like. Treatment with suberoylanilide hydroxamic acid (SAHA), a histone deacetylase inhibitor widely used in animal research but barely applied to plants, enhanced microspore embryogenesis initiation and proembryo formation, while increased histone acetylation levels. SAHA-treated proembryos showed higher expression than control of key embryogenesis transcription factors BnFUS3, BnAGL15, and BnLEC2, suggesting that histone hyperacetylation facilitates transcriptional activation of essential genes for somatic embryogenesis initiation. These findings provided new insights into the epigenetic regulation of this process and revealed new opportunities with histone epigenetic regulator inhibitors, to improve microspore embryogenesis induction for crop improvement.
publishDate 2024
dc.date.none.fl_str_mv 2024
2024
2025
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/10261/374169
url http://hdl.handle.net/10261/374169
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#
info:eu-repo/grantAgreement/AEI/Plan Estatal de Investigación Científica y Técnica y de Innovación 2017-2020/PID2020-113018RB-I00
info:eu-repo/grantAgreement/AEI/Plan Estatal de Investigación Científica y Técnica y de Innovación 2021-2023/CPP2021-008750
https://doi.org/10.1016/j.plantsci.2024.112318
Sí
dc.rights.none.fl_str_mv info:eu-repo/semantics/openAccess
eu_rights_str_mv openAccess
dc.publisher.none.fl_str_mv Elsevier
publisher.none.fl_str_mv Elsevier
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
collection DIGITAL.CSIC. Repositorio Institucional del CSIC
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