Hemichordate cis-regulatory genomics and the gene expression dynamics of deuterostomes

Deuterostomes are one major group of bilaterians composed by hemichordates and echinoderms (collectively called Ambulacraria) and chordates. Comparative studies between these groups can provide valuable insights into the nature of the last common ancestor of deuterostomes and that of bilaterians. In...

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Autores: Pérez-Posada, Alberto, Lin, Che-Yi, Fan, Tzu-Pei, Lin, Ching-Yi, Chen, Yi-Chih, Gómez-Skarmeta, José Luis, Yu, Jr-Kai, Su, Yi-Hsien, Tena, Juan J.
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:10261/384517
Acceso en línea:http://hdl.handle.net/10261/384517
Access Level:acceso abierto
Palabra clave:Epigenetics
Evolutionary biology
Evolutionary developmental biology
Evolutionary genetics
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dc.title.none.fl_str_mv Hemichordate cis-regulatory genomics and the gene expression dynamics of deuterostomes
title Hemichordate cis-regulatory genomics and the gene expression dynamics of deuterostomes
spellingShingle Hemichordate cis-regulatory genomics and the gene expression dynamics of deuterostomes
Pérez-Posada, Alberto
Epigenetics
Evolutionary biology
Evolutionary developmental biology
Evolutionary genetics
title_short Hemichordate cis-regulatory genomics and the gene expression dynamics of deuterostomes
title_full Hemichordate cis-regulatory genomics and the gene expression dynamics of deuterostomes
title_fullStr Hemichordate cis-regulatory genomics and the gene expression dynamics of deuterostomes
title_full_unstemmed Hemichordate cis-regulatory genomics and the gene expression dynamics of deuterostomes
title_sort Hemichordate cis-regulatory genomics and the gene expression dynamics of deuterostomes
dc.creator.none.fl_str_mv Pérez-Posada, Alberto
Lin, Che-Yi
Fan, Tzu-Pei
Lin, Ching-Yi
Chen, Yi-Chih
Gómez-Skarmeta, José Luis
Yu, Jr-Kai
Su, Yi-Hsien
Tena, Juan J.
author Pérez-Posada, Alberto
author_facet Pérez-Posada, Alberto
Lin, Che-Yi
Fan, Tzu-Pei
Lin, Ching-Yi
Chen, Yi-Chih
Gómez-Skarmeta, José Luis
Yu, Jr-Kai
Su, Yi-Hsien
Tena, Juan J.
author_role author
author2 Lin, Che-Yi
Fan, Tzu-Pei
Lin, Ching-Yi
Chen, Yi-Chih
Gómez-Skarmeta, José Luis
Yu, Jr-Kai
Su, Yi-Hsien
Tena, Juan J.
author2_role author
author
author
author
author
author
author
author
dc.contributor.none.fl_str_mv Ministerio de Ciencia y Tecnología (España)
Academia Sinica (Taiwan)
European Research Council
European Commission
Ministerio de Ciencia, Innovación y Universidades (España)
Agencia Estatal de Investigación (España)
Ministerio de Ciencia e Innovación (España)
Consejo Superior de Investigaciones Científicas [https://ror.org/02gfc7t72]
dc.subject.none.fl_str_mv Epigenetics
Evolutionary biology
Evolutionary developmental biology
Evolutionary genetics
topic Epigenetics
Evolutionary biology
Evolutionary developmental biology
Evolutionary genetics
description Deuterostomes are one major group of bilaterians composed by hemichordates and echinoderms (collectively called Ambulacraria) and chordates. Comparative studies between these groups can provide valuable insights into the nature of the last common ancestor of deuterostomes and that of bilaterians. Indirect development of hemichordates, with larval phases similar to echinoderms and an adult body plan with an anteroposterior polarity like chordates and other bilaterians, makes them a suitable model for studying the molecular basis of development among deuterostomes. However, a comprehensive, quantitative catalogue of gene expression and chromatin dynamics in hemichordates is still lacking. In this study, we analysed the transcriptomes and chromatin accessibility of multiple developmental stages of the indirect-developing hemichordate Ptychodera flava. We observed that P. flava development is underpinned by a biphasic transcriptional program probably controlled by distinct genetic networks. Comparisons with other bilaterian species revealed similar transcriptional and regulatory dynamics during hemichordate gastrulation, cephalochordate neurulation and elongation stages of annelids. By means of regulatory networks analysis and functional validations by transgenesis experiments in echinoderms, we propose that gastrulation is the stage of highest molecular resemblance in deuterostomes and that much of the molecular basis of deuterostome development was probably present in the bilaterian last common ancestor.
publishDate 2024
dc.date.none.fl_str_mv 2024
2025
2025
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Publisher's version
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dc.identifier.none.fl_str_mv http://hdl.handle.net/10261/384517
url http://hdl.handle.net/10261/384517
dc.language.none.fl_str_mv Inglés
language_invalid_str_mv Inglés
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info:eu-repo/grantAgreement/EC/H2020/740041
info:eu-repo/grantAgreement/AEI/Plan Estatal de Investigación Científica y Técnica y de Innovación 2017-2020/PID2019-103921GB-I00
info:eu-repo/grantAgreement/AEI/Plan Estatal de Investigación Científica y Técnica y de Innovación 2021-2023/PID2022-141288NB-I00
The underlying dataset has been published as supplementary material of the article in the publisher platform at DOI https://doi.org/10.1038/s41559-024-02562-x
Pérez-Posada, Alberto; Lin, Che-Yi; Fan, Tzu-Pei; Lin, Ching-Yi; Chen, Yi-Chih; Gómez-Skarmeta, José Luis; Yu, Jr-Kai; Su, Yi-Hsien; Tena, Juan J.; 2024; Ptychodera flava genomics and transcriptomics data [Dataset]; DIGITAL.CSIC; https://doi.org/10.20350/digitalCSIC/16340
Pérez-Posada, Alberto; Lin, Che-Yi; Fan, Tzu-Pei; Lin, Ching-Yi; Chen, Yi-Chih; Gómez-Skarmeta, José Luis; Yu, Jr-Kai; Su, Yi-Hsien; Tena, Juan J.; 2024; Insights into deuterostome evolution from the biphasic transcriptional programmes of hemichordates [Dataset]; GEO - Gene Expression Omnibus; https://doi.org/10.1038/s41559-024-02562-x
Pérez-Posada, Alberto; Lin, Che-Yi; Fan, Tzu-Pei; Lin, Ching-Yi; Chen, Yi-Chih; Gómez-Skarmeta, José Luis; Yu, Jr-Kai; Su, Yi-Hsien; Tena, Juan J.; 2024; Analyses of the Ptychodera flava RNASeq+ATACSeq project [Dataset]; GitHub; https://doi.org/10.1038/s41559-024-02562-x
https://doi.org/10.1038/s41559-024-02562-x

dc.rights.none.fl_str_mv info:eu-repo/semantics/openAccess
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dc.publisher.none.fl_str_mv Springer Nature
publisher.none.fl_str_mv Springer Nature
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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spelling Hemichordate cis-regulatory genomics and the gene expression dynamics of deuterostomesPérez-Posada, AlbertoLin, Che-YiFan, Tzu-PeiLin, Ching-YiChen, Yi-ChihGómez-Skarmeta, José LuisYu, Jr-KaiSu, Yi-HsienTena, Juan J.EpigeneticsEvolutionary biologyEvolutionary developmental biologyEvolutionary geneticsDeuterostomes are one major group of bilaterians composed by hemichordates and echinoderms (collectively called Ambulacraria) and chordates. Comparative studies between these groups can provide valuable insights into the nature of the last common ancestor of deuterostomes and that of bilaterians. Indirect development of hemichordates, with larval phases similar to echinoderms and an adult body plan with an anteroposterior polarity like chordates and other bilaterians, makes them a suitable model for studying the molecular basis of development among deuterostomes. However, a comprehensive, quantitative catalogue of gene expression and chromatin dynamics in hemichordates is still lacking. In this study, we analysed the transcriptomes and chromatin accessibility of multiple developmental stages of the indirect-developing hemichordate Ptychodera flava. We observed that P. flava development is underpinned by a biphasic transcriptional program probably controlled by distinct genetic networks. Comparisons with other bilaterian species revealed similar transcriptional and regulatory dynamics during hemichordate gastrulation, cephalochordate neurulation and elongation stages of annelids. By means of regulatory networks analysis and functional validations by transgenesis experiments in echinoderms, we propose that gastrulation is the stage of highest molecular resemblance in deuterostomes and that much of the molecular basis of deuterostome development was probably present in the bilaterian last common ancestor.This study was supported by the Ministry of Science and Technology, Taiwan (grant no. MOST-110-2326-B-001-006 to Y.-H.S. and grant no. MOST-110-2621-B-001-001-MY3 to J.-K.Y.) and Academia Sinica (AS-GC-111-L01 to Y.-H.S. and J.-K.Y.). J.J.T. and J.L.G.S. were supported by the European Research Council (grant agreement no. 740041) and the Spanish Ministerio de Economía y Competitividad (grant no. PID2019-103921GB-I00). J.J.T. was also funded by the Spanish Ministerio de Ciencia e Innovación (grant no. PID2022-141288NB-I00). We thank A. G. Galvez and P. Firbas for advice with the analyses and M. Van der Sande, S. Frolich and S. Van Heeringen, for their advice with ANANSE. A.P.-P. thanks the rest of the authors and all the members of the Skarmeta/Tena laboratory, as well as J. Solana, D. Salamanca-Diaz and M. Rosselló, for their support during the difficult times of this project.Peer reviewedSpringer NatureMinisterio de Ciencia y Tecnología (España)Academia Sinica (Taiwan)European Research CouncilEuropean CommissionMinisterio de Ciencia, Innovación y Universidades (España)Agencia Estatal de Investigación (España)Ministerio de Ciencia e Innovación (España)Consejo Superior de Investigaciones Científicas [https://ror.org/02gfc7t72]202520252024info:eu-repo/semantics/articlehttp://purl.org/coar/resource_type/c_6501Publisher's versioninfo:eu-repo/semantics/publishedVersionapplication/pdfhttp://hdl.handle.net/10261/384517reponame: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/EC/H2020/740041info:eu-repo/grantAgreement/AEI/Plan Estatal de Investigación Científica y Técnica y de Innovación 2017-2020/PID2019-103921GB-I00info:eu-repo/grantAgreement/AEI/Plan Estatal de Investigación Científica y Técnica y de Innovación 2021-2023/PID2022-141288NB-I00The underlying dataset has been published as supplementary material of the article in the publisher platform at DOI https://doi.org/10.1038/s41559-024-02562-xPérez-Posada, Alberto; Lin, Che-Yi; Fan, Tzu-Pei; Lin, Ching-Yi; Chen, Yi-Chih; Gómez-Skarmeta, José Luis; Yu, Jr-Kai; Su, Yi-Hsien; Tena, Juan J.; 2024; Ptychodera flava genomics and transcriptomics data [Dataset]; DIGITAL.CSIC; https://doi.org/10.20350/digitalCSIC/16340Pérez-Posada, Alberto; Lin, Che-Yi; Fan, Tzu-Pei; Lin, Ching-Yi; Chen, Yi-Chih; Gómez-Skarmeta, José Luis; Yu, Jr-Kai; Su, Yi-Hsien; Tena, Juan J.; 2024; Insights into deuterostome evolution from the biphasic transcriptional programmes of hemichordates [Dataset]; GEO - Gene Expression Omnibus; https://doi.org/10.1038/s41559-024-02562-xPérez-Posada, Alberto; Lin, Che-Yi; Fan, Tzu-Pei; Lin, Ching-Yi; Chen, Yi-Chih; Gómez-Skarmeta, José Luis; Yu, Jr-Kai; Su, Yi-Hsien; Tena, Juan J.; 2024; Analyses of the Ptychodera flava RNASeq+ATACSeq project [Dataset]; GitHub; https://doi.org/10.1038/s41559-024-02562-xhttps://doi.org/10.1038/s41559-024-02562-xSíinfo:eu-repo/semantics/openAccessoai:digital.csic.es:10261/3845172026-05-22T06:33:51Z
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