Complex transcriptional regulation and independent evolution of fungal-like traits in a relative of animals

Cell-type specification through differential genome regulation is a hallmark of complex multicellularity. However, it remains unclear how this process evolved during the transition from unicellular to multicellular organisms. To address this question, we investigated transcriptional dynamics in the...

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Detalles Bibliográficos
Autores: de Mendoza, Alex, Suga, Hiroshi, Permanyer, Jon, Irimia Martínez, Manuel, Ruíz Trillo, Iñaki
Tipo de recurso: artículo
Estado:Versión publicada
Fecha de publicación:2015
País:España
Institución:Universitat Pompeu Fabra
Repositorio:Repositorio Digital de la UPF
OAI Identifier:oai:repositori.upf.edu:10230/26877
Acceso en línea:http://hdl.handle.net/10230/26877
http://dx.doi.org/10.1016/10.7554/eLife.08904
Access Level:acceso abierto
Palabra clave:Biologia del desenvolupament
Cèl·lules mare
Alternative splicing
Comparative genomics
Developmental biology
Evolutionary biology
Genomics
Lateral gene transfer
lincRNA
Multicellularity
Secretome
Stem cells
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oai_identifier_str oai:repositori.upf.edu:10230/26877
network_acronym_str ES
network_name_str España
repository_id_str
spelling Complex transcriptional regulation and independent evolution of fungal-like traits in a relative of animalsde Mendoza, AlexSuga, HiroshiPermanyer, JonIrimia Martínez, ManuelRuíz Trillo, IñakiBiologia del desenvolupamentCèl·lules mareAlternative splicingComparative genomicsDevelopmental biologyEvolutionary biologyGenomicsLateral gene transferlincRNAMulticellularitySecretomeStem cellsCell-type specification through differential genome regulation is a hallmark of complex multicellularity. However, it remains unclear how this process evolved during the transition from unicellular to multicellular organisms. To address this question, we investigated transcriptional dynamics in the ichthyosporean Creolimax fragrantissima, a relative of animals that undergoes coenocytic development. We find that Creolimax utilizes dynamic regulation of alternative splicing, long inter-genic non-coding RNAs and co-regulated gene modules associated with animal multicellularity in a cell-type specific manner. Moreover, our study suggests that the different cell types of the three closest animal relatives (ichthyosporeans, filastereans and choanoflagellates) are the product of lineage-specific innovations. Additionally, a proteomic survey of the secretome reveals adaptations to a fungal-like lifestyle. In summary, the diversity of cell types among protistan relatives of animals and their complex genome regulation demonstrates that the last unicellular ancestor of animals was already capable of elaborate specification of cell types.Funding: European Research Council ERC-2007-StG-206883 to Alex de Mendoza, Hiroshi Suga, Iñaki Ruiz-Trillo. Ministerio de Economía y Competitividad BFU-2011-23434 to Alex de Mendoza. European Research Council ERC-2012-Co-616960 Alex de Mendoza. Japan Society for the Promotion of Science Research Activity to Hiroshi Suga. Center for Genomic Regulation Core funding to Jon Permanyer, Manuel Irimia Hiroshi Suga, Iñaki Ruiz-Trillo.eLife201620162015info:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersionapplication/pdfapplication/pdfhttp://hdl.handle.net/10230/26877http://dx.doi.org/10.1016/10.7554/eLife.08904reponame:Repositorio Digital de la UPFinstname:Universitat Pompeu FabraInglésElife. 2015; 4: e08904© Copyright de Mendoza et al./nThis article is distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use and redistribution provided that the original author and source are credited.http://creativecommons.org/licenses/by/4.0/info:eu-repo/semantics/openAccessoai:repositori.upf.edu:10230/268772026-06-12T07:21:37Z
dc.title.none.fl_str_mv Complex transcriptional regulation and independent evolution of fungal-like traits in a relative of animals
title Complex transcriptional regulation and independent evolution of fungal-like traits in a relative of animals
spellingShingle Complex transcriptional regulation and independent evolution of fungal-like traits in a relative of animals
de Mendoza, Alex
Biologia del desenvolupament
Cèl·lules mare
Alternative splicing
Comparative genomics
Developmental biology
Evolutionary biology
Genomics
Lateral gene transfer
lincRNA
Multicellularity
Secretome
Stem cells
title_short Complex transcriptional regulation and independent evolution of fungal-like traits in a relative of animals
title_full Complex transcriptional regulation and independent evolution of fungal-like traits in a relative of animals
title_fullStr Complex transcriptional regulation and independent evolution of fungal-like traits in a relative of animals
title_full_unstemmed Complex transcriptional regulation and independent evolution of fungal-like traits in a relative of animals
title_sort Complex transcriptional regulation and independent evolution of fungal-like traits in a relative of animals
dc.creator.none.fl_str_mv de Mendoza, Alex
Suga, Hiroshi
Permanyer, Jon
Irimia Martínez, Manuel
Ruíz Trillo, Iñaki
author de Mendoza, Alex
author_facet de Mendoza, Alex
Suga, Hiroshi
Permanyer, Jon
Irimia Martínez, Manuel
Ruíz Trillo, Iñaki
author_role author
author2 Suga, Hiroshi
Permanyer, Jon
Irimia Martínez, Manuel
Ruíz Trillo, Iñaki
author2_role author
author
author
author
dc.subject.none.fl_str_mv Biologia del desenvolupament
Cèl·lules mare
Alternative splicing
Comparative genomics
Developmental biology
Evolutionary biology
Genomics
Lateral gene transfer
lincRNA
Multicellularity
Secretome
Stem cells
topic Biologia del desenvolupament
Cèl·lules mare
Alternative splicing
Comparative genomics
Developmental biology
Evolutionary biology
Genomics
Lateral gene transfer
lincRNA
Multicellularity
Secretome
Stem cells
description Cell-type specification through differential genome regulation is a hallmark of complex multicellularity. However, it remains unclear how this process evolved during the transition from unicellular to multicellular organisms. To address this question, we investigated transcriptional dynamics in the ichthyosporean Creolimax fragrantissima, a relative of animals that undergoes coenocytic development. We find that Creolimax utilizes dynamic regulation of alternative splicing, long inter-genic non-coding RNAs and co-regulated gene modules associated with animal multicellularity in a cell-type specific manner. Moreover, our study suggests that the different cell types of the three closest animal relatives (ichthyosporeans, filastereans and choanoflagellates) are the product of lineage-specific innovations. Additionally, a proteomic survey of the secretome reveals adaptations to a fungal-like lifestyle. In summary, the diversity of cell types among protistan relatives of animals and their complex genome regulation demonstrates that the last unicellular ancestor of animals was already capable of elaborate specification of cell types.
publishDate 2015
dc.date.none.fl_str_mv 2015
2016
2016
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/10230/26877
http://dx.doi.org/10.1016/10.7554/eLife.08904
url http://hdl.handle.net/10230/26877
http://dx.doi.org/10.1016/10.7554/eLife.08904
dc.language.none.fl_str_mv Inglés
language_invalid_str_mv Inglés
dc.relation.none.fl_str_mv Elife. 2015; 4: e08904
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 eLife
publisher.none.fl_str_mv eLife
dc.source.none.fl_str_mv reponame:Repositorio Digital de la UPF
instname:Universitat Pompeu Fabra
instname_str Universitat Pompeu Fabra
reponame_str Repositorio Digital de la UPF
collection Repositorio Digital de la UPF
repository.name.fl_str_mv
repository.mail.fl_str_mv
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