Evolutionary recruitment of flexible Esrp-dependent splicing programs into diverse embryonic morphogenetic processes

Epithelial-mesenchymal interactions are crucial for the development of numerous animal structures. Thus, unraveling how molecular tools are recruited in different lineages to control interplays between these tissues is key to understanding morphogenetic evolution. Here, we study Esrp genes, which re...

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Autores: Burguera, Demián, Márquez, Yamile, Racioppi, Claudia, Permanyer, Jon, Torres Méndez, Antonio, Esposito, Rosaria, Albuixech Crespo, Beatriz, Fanlo, Lucía, D'Agostino, Ylenia, Gohr, André, Navas Pérez, Enrique, Riesgo, Ana, Cuomo, Claudia, Benvenuto, Giovanna, Christiaen, Lionel A., Martí, Elisa, D'Aniello, Salvatore, Spagnuolo, Antonietta, Ristoratore, Filomena, Arnone, Maria Ina, García Fernàndez, Jordi, Irimia Martínez, Manuel
Tipo de recurso: artículo
Estado:Versión publicada
Fecha de publicación:2017
País:España
Institución:Varias* (Consorci de Biblioteques Universitáries de Catalunya, Centre de Serveis Científics i Acadèmics de Catalunya)
Repositorio:Recercat. Dipósit de la Recerca de Catalunya
OAI Identifier:oai:recercat.cat:10230/34949
Acceso en línea:http://hdl.handle.net/10230/34949
http://dx.doi.org/10.1038/s41467-017-01961-y
Access Level:acceso abierto
Palabra clave:Evolutionary developmental biology
Transcriptomics
Esrp genes
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spelling Evolutionary recruitment of flexible Esrp-dependent splicing programs into diverse embryonic morphogenetic processesBurguera, DemiánMárquez, YamileRacioppi, ClaudiaPermanyer, JonTorres Méndez, AntonioEsposito, RosariaAlbuixech Crespo, BeatrizFanlo, LucíaD'Agostino, YleniaGohr, AndréNavas Pérez, EnriqueRiesgo, AnaCuomo, ClaudiaBenvenuto, GiovannaChristiaen, Lionel A.Martí, ElisaD'Aniello, SalvatoreSpagnuolo, AntoniettaRistoratore, FilomenaArnone, Maria InaGarcía Fernàndez, JordiIrimia Martínez, ManuelEvolutionary developmental biologyTranscriptomicsEsrp genesEpithelial-mesenchymal interactions are crucial for the development of numerous animal structures. Thus, unraveling how molecular tools are recruited in different lineages to control interplays between these tissues is key to understanding morphogenetic evolution. Here, we study Esrp genes, which regulate extensive splicing programs and are essential for mammalian organogenesis. We find that Esrp homologs have been independently recruited for the development of multiple structures across deuterostomes. Although Esrp is involved in a wide variety of ontogenetic processes, our results suggest ancient roles in non-neural ectoderm and regulating specific mesenchymal-to-epithelial transitions in deuterostome ancestors. However, consistent with the extensive rewiring of Esrp-dependent splicing programs between phyla, most developmental defects observed in vertebrate mutants are related to other types of morphogenetic processes. This is likely connected to the origin of an event in Fgfr, which was recruited as an Esrp target in stem chordates and subsequently co-opted into the development of many novel traits in vertebrates.This work has received funding from the European Research Council (ERC) under the European Union's Horizon 2020 research and innovation program (grant agreement No ERC-StG-LS2-637591 to M.I.), the Spanish Ministry of Economy and Competitiveness (grant BFU2014-58908P to J.G.-F, BFU2014-55076-P to M.I., and the 'Centro de Excelencia Severo Ochoa 2013-2017', SEV-2012-0208), and ICREA - Generalitat de Catalunya (Academia Prize to J.G.-F). We acknowledge the support of the CERCA Programme/Generalitat de Catalunya. D.B. held an APIF fellowship from University of Barcelona, Y.M. an EMBO Long Term postdoctoral fellowship (ALTF 1505-2015), C.R. an EMBO long-term fellowship (ALTF 1608-2014), ATM an FPI-SO fellowship.Nature Publishing Group201820182017info:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersionapplication/pdfapplication/pdfhttp://hdl.handle.net/10230/34949http://dx.doi.org/10.1038/s41467-017-01961-yreponame:Recercat. Dipósit de la Recerca de Catalunyainstname:Varias* (Consorci de Biblioteques Universitáries de Catalunya, Centre de Serveis Científics i Acadèmics de Catalunya)InglésNature Communications. 2017 Nov 27;8(1):1799info:eu-repo/grantAgreement/EC/H2020/637591info:eu-repo/grantAgreement/ES/1PE/BFU2014-58908-Pinfo:eu-repo/grantAgreement/ES/1PE/BFU2014-55076-P© The Author(s) 2017. Open Access. This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.http://creativecommons.org/licenses/by/4.0/info:eu-repo/semantics/openAccessoai:recercat.cat:10230/349492026-05-29T05:05:01Z
dc.title.none.fl_str_mv Evolutionary recruitment of flexible Esrp-dependent splicing programs into diverse embryonic morphogenetic processes
title Evolutionary recruitment of flexible Esrp-dependent splicing programs into diverse embryonic morphogenetic processes
spellingShingle Evolutionary recruitment of flexible Esrp-dependent splicing programs into diverse embryonic morphogenetic processes
Burguera, Demián
Evolutionary developmental biology
Transcriptomics
Esrp genes
title_short Evolutionary recruitment of flexible Esrp-dependent splicing programs into diverse embryonic morphogenetic processes
title_full Evolutionary recruitment of flexible Esrp-dependent splicing programs into diverse embryonic morphogenetic processes
title_fullStr Evolutionary recruitment of flexible Esrp-dependent splicing programs into diverse embryonic morphogenetic processes
title_full_unstemmed Evolutionary recruitment of flexible Esrp-dependent splicing programs into diverse embryonic morphogenetic processes
title_sort Evolutionary recruitment of flexible Esrp-dependent splicing programs into diverse embryonic morphogenetic processes
dc.creator.none.fl_str_mv Burguera, Demián
Márquez, Yamile
Racioppi, Claudia
Permanyer, Jon
Torres Méndez, Antonio
Esposito, Rosaria
Albuixech Crespo, Beatriz
Fanlo, Lucía
D'Agostino, Ylenia
Gohr, André
Navas Pérez, Enrique
Riesgo, Ana
Cuomo, Claudia
Benvenuto, Giovanna
Christiaen, Lionel A.
Martí, Elisa
D'Aniello, Salvatore
Spagnuolo, Antonietta
Ristoratore, Filomena
Arnone, Maria Ina
García Fernàndez, Jordi
Irimia Martínez, Manuel
author Burguera, Demián
author_facet Burguera, Demián
Márquez, Yamile
Racioppi, Claudia
Permanyer, Jon
Torres Méndez, Antonio
Esposito, Rosaria
Albuixech Crespo, Beatriz
Fanlo, Lucía
D'Agostino, Ylenia
Gohr, André
Navas Pérez, Enrique
Riesgo, Ana
Cuomo, Claudia
Benvenuto, Giovanna
Christiaen, Lionel A.
Martí, Elisa
D'Aniello, Salvatore
Spagnuolo, Antonietta
Ristoratore, Filomena
Arnone, Maria Ina
García Fernàndez, Jordi
Irimia Martínez, Manuel
author_role author
author2 Márquez, Yamile
Racioppi, Claudia
Permanyer, Jon
Torres Méndez, Antonio
Esposito, Rosaria
Albuixech Crespo, Beatriz
Fanlo, Lucía
D'Agostino, Ylenia
Gohr, André
Navas Pérez, Enrique
Riesgo, Ana
Cuomo, Claudia
Benvenuto, Giovanna
Christiaen, Lionel A.
Martí, Elisa
D'Aniello, Salvatore
Spagnuolo, Antonietta
Ristoratore, Filomena
Arnone, Maria Ina
García Fernàndez, Jordi
Irimia Martínez, Manuel
author2_role author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
dc.subject.none.fl_str_mv Evolutionary developmental biology
Transcriptomics
Esrp genes
topic Evolutionary developmental biology
Transcriptomics
Esrp genes
description Epithelial-mesenchymal interactions are crucial for the development of numerous animal structures. Thus, unraveling how molecular tools are recruited in different lineages to control interplays between these tissues is key to understanding morphogenetic evolution. Here, we study Esrp genes, which regulate extensive splicing programs and are essential for mammalian organogenesis. We find that Esrp homologs have been independently recruited for the development of multiple structures across deuterostomes. Although Esrp is involved in a wide variety of ontogenetic processes, our results suggest ancient roles in non-neural ectoderm and regulating specific mesenchymal-to-epithelial transitions in deuterostome ancestors. However, consistent with the extensive rewiring of Esrp-dependent splicing programs between phyla, most developmental defects observed in vertebrate mutants are related to other types of morphogenetic processes. This is likely connected to the origin of an event in Fgfr, which was recruited as an Esrp target in stem chordates and subsequently co-opted into the development of many novel traits in vertebrates.
publishDate 2017
dc.date.none.fl_str_mv 2017
2018
2018
dc.type.none.fl_str_mv info:eu-repo/semantics/article
info:eu-repo/semantics/publishedVersion
format article
status_str publishedVersion
dc.identifier.none.fl_str_mv http://hdl.handle.net/10230/34949
http://dx.doi.org/10.1038/s41467-017-01961-y
url http://hdl.handle.net/10230/34949
http://dx.doi.org/10.1038/s41467-017-01961-y
dc.language.none.fl_str_mv Inglés
language_invalid_str_mv Inglés
dc.relation.none.fl_str_mv Nature Communications. 2017 Nov 27;8(1):1799
info:eu-repo/grantAgreement/EC/H2020/637591
info:eu-repo/grantAgreement/ES/1PE/BFU2014-58908-P
info:eu-repo/grantAgreement/ES/1PE/BFU2014-55076-P
dc.rights.none.fl_str_mv http://creativecommons.org/licenses/by/4.0/
info:eu-repo/semantics/openAccess
rights_invalid_str_mv http://creativecommons.org/licenses/by/4.0/
eu_rights_str_mv openAccess
dc.format.none.fl_str_mv application/pdf
application/pdf
dc.publisher.none.fl_str_mv Nature Publishing Group
publisher.none.fl_str_mv Nature Publishing Group
dc.source.none.fl_str_mv reponame:Recercat. Dipósit de la Recerca de Catalunya
instname:Varias* (Consorci de Biblioteques Universitáries de Catalunya, Centre de Serveis Científics i Acadèmics de Catalunya)
instname_str Varias* (Consorci de Biblioteques Universitáries de Catalunya, Centre de Serveis Científics i Acadèmics de Catalunya)
reponame_str Recercat. Dipósit de la Recerca de Catalunya
collection Recercat. Dipósit de la Recerca de Catalunya
repository.name.fl_str_mv
repository.mail.fl_str_mv
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