Microspore embryogenesis induction by mannitol and TSA results in a complex regulation of epigenetic dynamics and gene expression in bread wheat

18 pags.- 6 Figs. Data availability statement The original contributions presented in the study are included in the article/Supplementary Materials. Further inquiries can be directed to the corresponding author. © 2023 Valero-Rubira, Castillo, Burrell and Valle´s. This is an open-access article dist...

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Autores: Valero-Rubira, Isabel, Castillo Alonso, Ana María, Burrell, María Ángela, Vallés Brau, María Pilar
Formato: artículo
Estado:Versión publicada
Fecha de publicación:2023
País:España
Recursos:Consejo Superior de Investigaciones Científicas (CSIC)
Repositorio:DIGITAL.CSIC. Repositorio Institucional del CSIC
OAI Identifier:oai:digital.csic.es:10261/303963
Acesso em linha:http://hdl.handle.net/10261/303963
Access Level:acceso abierto
Palavra-chave:bread wheat
microspore embryogenesis
mannitol
trichostatin A
histones
epigenetics
Gene expression
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dc.title.none.fl_str_mv Microspore embryogenesis induction by mannitol and TSA results in a complex regulation of epigenetic dynamics and gene expression in bread wheat
title Microspore embryogenesis induction by mannitol and TSA results in a complex regulation of epigenetic dynamics and gene expression in bread wheat
spellingShingle Microspore embryogenesis induction by mannitol and TSA results in a complex regulation of epigenetic dynamics and gene expression in bread wheat
Valero-Rubira, Isabel
bread wheat
microspore embryogenesis
mannitol
trichostatin A
histones
epigenetics
Gene expression
title_short Microspore embryogenesis induction by mannitol and TSA results in a complex regulation of epigenetic dynamics and gene expression in bread wheat
title_full Microspore embryogenesis induction by mannitol and TSA results in a complex regulation of epigenetic dynamics and gene expression in bread wheat
title_fullStr Microspore embryogenesis induction by mannitol and TSA results in a complex regulation of epigenetic dynamics and gene expression in bread wheat
title_full_unstemmed Microspore embryogenesis induction by mannitol and TSA results in a complex regulation of epigenetic dynamics and gene expression in bread wheat
title_sort Microspore embryogenesis induction by mannitol and TSA results in a complex regulation of epigenetic dynamics and gene expression in bread wheat
dc.creator.none.fl_str_mv Valero-Rubira, Isabel
Castillo Alonso, Ana María
Burrell, María Ángela
Vallés Brau, María Pilar
author Valero-Rubira, Isabel
author_facet Valero-Rubira, Isabel
Castillo Alonso, Ana María
Burrell, María Ángela
Vallés Brau, María Pilar
author_role author
author2 Castillo Alonso, Ana María
Burrell, María Ángela
Vallés Brau, María Pilar
author2_role author
author
author
dc.contributor.none.fl_str_mv Ministerio de Ciencia e Innovación (España)
Gobierno de Aragón
Castillo Alonso, Ana María [0000-0002-6143-3227]
Vallés Brau, María Pilar [0000-0002-8649-2362]
Consejo Superior de Investigaciones Científicas [https://ror.org/02gfc7t72]
dc.subject.none.fl_str_mv bread wheat
microspore embryogenesis
mannitol
trichostatin A
histones
epigenetics
Gene expression
topic bread wheat
microspore embryogenesis
mannitol
trichostatin A
histones
epigenetics
Gene expression
description 18 pags.- 6 Figs. Data availability statement The original contributions presented in the study are included in the article/Supplementary Materials. Further inquiries can be directed to the corresponding author. © 2023 Valero-Rubira, Castillo, Burrell and Valle´s. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY).
publishDate 2023
dc.date.none.fl_str_mv 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/10261/303963
url http://hdl.handle.net/10261/303963
dc.language.none.fl_str_mv Inglés
language_invalid_str_mv Inglés
dc.relation.none.fl_str_mv #PLACEHOLDER_PARENT_METADATA_VALUE#
info:eu-repo/grantAgreement/AEI/Plan Estatal de Investigación Científica y Técnica y de Innovación 2017-2020/PID2020-119540RB-I00
The underlying dataset has been published as supplementary material of the article in the publisher platform at DOI: https://doi.org/10.3389/fpls.2022.1058421
https://doi.org/10.3389/fpls.2022.1058421
Sí
dc.rights.none.fl_str_mv info:eu-repo/semantics/openAccess
eu_rights_str_mv openAccess
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
collection DIGITAL.CSIC. Repositorio Institucional del CSIC
repository.name.fl_str_mv
repository.mail.fl_str_mv
_version_ 1869417249733869568
spelling Microspore embryogenesis induction by mannitol and TSA results in a complex regulation of epigenetic dynamics and gene expression in bread wheatValero-Rubira, IsabelCastillo Alonso, Ana MaríaBurrell, María ÁngelaVallés Brau, María Pilarbread wheatmicrospore embryogenesismannitoltrichostatin AhistonesepigeneticsGene expression18 pags.- 6 Figs. Data availability statement The original contributions presented in the study are included in the article/Supplementary Materials. Further inquiries can be directed to the corresponding author. © 2023 Valero-Rubira, Castillo, Burrell and Valle´s. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY).Reprogramming of microspores development towards embryogenesis mediated by stress treatment constitutes the basis of doubled haploid production. Recently, compounds that alter histone post-translational modifications (PTMs) have been reported to enhance microspore embryogenesis (ME), by altering histones acetylation or methylation. However, epigenetic mechanisms underlying ME induction efficiency are poorly understood. In this study, the epigenetic dynamics and the expression of genes associated with histone PTMs and ME induction were studied in two bread wheat cultivars with different ME response. Microspores isolated at 0, 3 and 5 days, treated with 0.7M mannitol (MAN) and 0.7M mannitol plus 0.4µM trichostatin A (TSA), which induced ME more efficiently, were analyzed. An additional control of gametophytic development was included. Microspores epigenetic state at the onset of ME induction was distinctive between cultivars by the ratio of H3 variants and their acetylated forms, the localization and percentage of labeled microspores with H3K9ac, H4K5ac, H4K16ac, H3K9me2 and H3K27me3, and the expression of genes related to pollen development. These results indicated that microspores of the high responding cultivar could be at a less advanced stage in pollen development. MAN and TSA resulted in a hyperacetylation of H3.2, with a greater effect of TSA. Histone PTMs were differentially affected by both treatments, with acetylation being most concerned. The effect of TSA was observed in the H4K5ac localization pattern at 3dT in the mid-low responding cultivar. Three gene networks linked to ME response were identified. TaHDT1, TaHAG2, TaYAO, TaNFD6-A, TabZIPF1 and TaAGO802-B, associated with pollen development, were down-regulated. TaHDA15, TaHAG3, TaHAM, TaYUC11D, Ta-2B-LBD16 TaMS1 and TaDRM3 constituted a network implicated in morphological changes by auxin signaling and cell wall modification up-regulated at 3dT. The last network included TaHDA18, TaHAC1, TaHAC4, TaABI5, TaATG18fD, TaSDG1a-7A and was related to ABA and ethylene hormone signaling pathways, DNA methylation and autophagy processes, reaching the highest expression at 5dT. The results indicated that TSA mainly modified the regulation of genes related to pollen and auxin signaling. This study represents a breakthrough in identifying the epigenetic dynamics and the molecular mechanisms governing ME induction efficiency, with relevance to recalcitrant wheat genotypes and other crops.This research was supported by Project AGL2016-77211-R and PID2020-119540RB-100 from State R&D Program Oriented to the Challenges of the Spanish Society and funds for Reference Research Groups recognized by Diputación General de Aragón, Spain (Group A08-20R). IV-R was funded by the Spanish Ministry of Science and Innovation grant no. BES-2017-080970 (linked to the project AGL2016-77211-R).Peer reviewedFrontiers MediaMinisterio de Ciencia e Innovación (España)Gobierno de AragónCastillo Alonso, Ana María [0000-0002-6143-3227]Vallés Brau, María Pilar [0000-0002-8649-2362]Consejo Superior de Investigaciones Científicas [https://ror.org/02gfc7t72]202320232023info:eu-repo/semantics/articlehttp://purl.org/coar/resource_type/c_6501Publisher's versioninfo:eu-repo/semantics/publishedVersionhttp://hdl.handle.net/10261/303963reponame:DIGITAL.CSIC. Repositorio Institucional del CSICinstname:Consejo Superior de Investigaciones Científicas (CSIC)Inglés#PLACEHOLDER_PARENT_METADATA_VALUE#info:eu-repo/grantAgreement/AEI/Plan Estatal de Investigación Científica y Técnica y de Innovación 2017-2020/PID2020-119540RB-I00The underlying dataset has been published as supplementary material of the article in the publisher platform at DOI: https://doi.org/10.3389/fpls.2022.1058421https://doi.org/10.3389/fpls.2022.1058421Síinfo:eu-repo/semantics/openAccessoai:digital.csic.es:10261/3039632026-05-22T06:33:51Z
score 15.812429

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