Genomic Exaptation and Regulatory Landscape Shifts as Key Mechanisms Enabling Flatworm Terrestrialization

21 pages, 8 figures, supplementary material https://doi.org/10.1093/gbe/evag063.-- Data Availability: The raw data for the transcriptomes generated in this study can be found at the European Nucleotide Archive with Project IDs: PRJEB81501, PRJEB108593 and PRJEB108587. Raw data for the proteomics dat...

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Autores: Carbonetto, Belén, Benítez-Álvarez, Lisandra, García-Vernet, Raquel, Eleftheriadi, Klara, Vargas-Chávez, Carlos, Escudero, Nuria, Salces-Ortiz, Judit, Rojo, Iñaki, Fernández-Álvarez, Fernando Ángel, Alwell, Corey, Chiva, Cristina, Sabidó, Eduard, Mateos, Eduardo, Carbayo, Fernando, Fernández, Rosa
Tipo de recurso: artículo
Estado:Versión publicada
Fecha de publicación:2026
País:España
Institución:Consejo Superior de Investigaciones Científicas (CSIC)
Repositorio:DIGITAL.CSIC. Repositorio Institucional del CSIC
OAI Identifier:oai:dnet:digitalcsic_::0a15b1f1c78d78cfc7463ea11be337ce
Acceso en línea:http://hdl.handle.net/10261/431846
Access Level:acceso abierto
Palabra clave:Phylogenomics
Genome evolution
Platyhelminthes
Transcriptomics
Conserve and sustainably use the oceans, seas and marine resources for sustainable development
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network_name_str España
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dc.title.none.fl_str_mv Genomic Exaptation and Regulatory Landscape Shifts as Key Mechanisms Enabling Flatworm Terrestrialization
title Genomic Exaptation and Regulatory Landscape Shifts as Key Mechanisms Enabling Flatworm Terrestrialization
spellingShingle Genomic Exaptation and Regulatory Landscape Shifts as Key Mechanisms Enabling Flatworm Terrestrialization
Carbonetto, Belén
Phylogenomics
Genome evolution
Platyhelminthes
Transcriptomics
Conserve and sustainably use the oceans, seas and marine resources for sustainable development
title_short Genomic Exaptation and Regulatory Landscape Shifts as Key Mechanisms Enabling Flatworm Terrestrialization
title_full Genomic Exaptation and Regulatory Landscape Shifts as Key Mechanisms Enabling Flatworm Terrestrialization
title_fullStr Genomic Exaptation and Regulatory Landscape Shifts as Key Mechanisms Enabling Flatworm Terrestrialization
title_full_unstemmed Genomic Exaptation and Regulatory Landscape Shifts as Key Mechanisms Enabling Flatworm Terrestrialization
title_sort Genomic Exaptation and Regulatory Landscape Shifts as Key Mechanisms Enabling Flatworm Terrestrialization
dc.creator.none.fl_str_mv Carbonetto, Belén
Benítez-Álvarez, Lisandra
García-Vernet, Raquel
Eleftheriadi, Klara
Vargas-Chávez, Carlos
Escudero, Nuria
Salces-Ortiz, Judit
Rojo, Iñaki
Fernández-Álvarez, Fernando Ángel
Alwell, Corey
Chiva, Cristina
Sabidó, Eduard
Mateos, Eduardo
Carbayo, Fernando
Fernández, Rosa
author Carbonetto, Belén
author_facet Carbonetto, Belén
Benítez-Álvarez, Lisandra
García-Vernet, Raquel
Eleftheriadi, Klara
Vargas-Chávez, Carlos
Escudero, Nuria
Salces-Ortiz, Judit
Rojo, Iñaki
Fernández-Álvarez, Fernando Ángel
Alwell, Corey
Chiva, Cristina
Sabidó, Eduard
Mateos, Eduardo
Carbayo, Fernando
Fernández, Rosa
author_role author
author2 Benítez-Álvarez, Lisandra
García-Vernet, Raquel
Eleftheriadi, Klara
Vargas-Chávez, Carlos
Escudero, Nuria
Salces-Ortiz, Judit
Rojo, Iñaki
Fernández-Álvarez, Fernando Ángel
Alwell, Corey
Chiva, Cristina
Sabidó, Eduard
Mateos, Eduardo
Carbayo, Fernando
Fernández, Rosa
author2_role author
author
author
author
author
author
author
author
author
author
author
author
author
author
dc.contributor.none.fl_str_mv Agencia Estatal de Investigación (España)
Ministerio de Universidades (España)
European Commission
Ministerio de Ciencia e Innovación (España)
Generalitat de Catalunya
dc.subject.none.fl_str_mv Phylogenomics
Genome evolution
Platyhelminthes
Transcriptomics
Conserve and sustainably use the oceans, seas and marine resources for sustainable development
topic Phylogenomics
Genome evolution
Platyhelminthes
Transcriptomics
Conserve and sustainably use the oceans, seas and marine resources for sustainable development
description 21 pages, 8 figures, supplementary material https://doi.org/10.1093/gbe/evag063.-- Data Availability: The raw data for the transcriptomes generated in this study can be found at the European Nucleotide Archive with Project IDs: PRJEB81501, PRJEB108593 and PRJEB108587. Raw data for the proteomics data set can be found at the Proteomics Identifications Database with Project ID: PXD074775. Both at https://www.ebi.ac.uk. A repository containing additional input, intermediate and supporting files can de found here: https://github.com/MetazoaPhylogenomicsLab/Benitez-Alvarez_et_al_2025_Gene_repertoire_evolution_land_planarians
publishDate 2026
dc.date.none.fl_str_mv 2026
2026
2026
dc.type.none.fl_str_mv info:eu-repo/semantics/article
Publisher's version
info:eu-repo/semantics/publishedVersion
format article
status_str publishedVersion
dc.identifier.none.fl_str_mv http://hdl.handle.net/10261/431846
url http://hdl.handle.net/10261/431846
dc.language.none.fl_str_mv Inglés
language_invalid_str_mv Inglés
dc.relation.none.fl_str_mv #PLACEHOLDER_PARENT_METADATA_VALUE#
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info:eu-repo/grantAgreement/EC/H2020/948281
info:eu-repo/grantAgreement/EC/HE/101129751
https://doi.org/10.1093/gbe/evag063
Sí
dc.rights.none.fl_str_mv info:eu-repo/semantics/openAccess
eu_rights_str_mv openAccess
dc.publisher.none.fl_str_mv Oxford University Press
publisher.none.fl_str_mv Oxford University Press
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
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spelling Genomic Exaptation and Regulatory Landscape Shifts as Key Mechanisms Enabling Flatworm TerrestrializationCarbonetto, BelénBenítez-Álvarez, LisandraGarcía-Vernet, RaquelEleftheriadi, KlaraVargas-Chávez, CarlosEscudero, NuriaSalces-Ortiz, JuditRojo, IñakiFernández-Álvarez, Fernando ÁngelAlwell, CoreyChiva, CristinaSabidó, EduardMateos, EduardoCarbayo, FernandoFernández, RosaPhylogenomicsGenome evolutionPlatyhelminthesTranscriptomicsConserve and sustainably use the oceans, seas and marine resources for sustainable development21 pages, 8 figures, supplementary material https://doi.org/10.1093/gbe/evag063.-- Data Availability: The raw data for the transcriptomes generated in this study can be found at the European Nucleotide Archive with Project IDs: PRJEB81501, PRJEB108593 and PRJEB108587. Raw data for the proteomics data set can be found at the Proteomics Identifications Database with Project ID: PXD074775. Both at https://www.ebi.ac.uk. A repository containing additional input, intermediate and supporting files can de found here: https://github.com/MetazoaPhylogenomicsLab/Benitez-Alvarez_et_al_2025_Gene_repertoire_evolution_land_planariansUnderstanding the genomic toolkit that enabled animal terrestrialization, the shift from aquatic to terrestrial habitats, is key to uncovering the evolutionary origins of land biodiversity. Yet, the genomic basis of the physiological and metabolic adaptations required for life on land remains poorly understood across most terrestrial animal phyla. Planarians (Platyhelminthes) offer a powerful model, as only one terrestrial lineage, the Geoplanidae (order Tricladida), is known. Here, we integrated genomics, transcriptomics, and proteomics to explore the genetic changes potentially supporting terrestrial adaptation. We identified a major burst of gene gain in the lineage leading to Tricladida, preceding the radiation of terrestrial planarians. Upon abiotic stress exposure, terrestrial and freshwater species exhibited distinct responses: most differentially expressed genes belonged to orthogroups gained in Tricladida, with over half under strong directional selection in terrestrial flatworms, suggesting their adaptive relevance. Transcriptomic profiles revealed divergent strategies: terrestrial species upregulated ancient genes, while freshwater species downregulated a separate set of ancestral genes. Across all datasets, the abiotic stress–response toolkit in terrestrial planarians was markedly different from freshwater relatives, with significant regulatory divergence. Our results highlight gene gain and co-option, rather than lineage-specific innovations, as key drivers of terrestrial flatworm evolution, emphasizing genomic exaptation and regulatory shifts as central to terrestrialization in Platyhelminthes. This study provides the first genome-wide view of the genetic basis of flatworm terrestrialization and sheds light on broader patterns of animal terrestrial adaptationG-V acknowledges the support of the Margarita Salas grant funded by the Spanish Ministry of Universities and the European Union Next Generation EU/PRTR. RF acknowledges support from the following sources of funding: Ramón y Cajal fellowship (grant agreement no. RYC2017-22492 funded by MCIN/AEI/10.13039/501100011033 and ESF “Investing in your future”), the European Research Council (this project has received funding from the European Research Council (ERC) under the European Union's Horizon 2020 research and innovation programme (grant agreement no. 948281)), the OSCARS project (funding from the European Commission's Horizon Europe Research and Innovation programme under grant agreement no. 101129751) and the Secretaria d’Universitats i Recerca del Departament d’Economia i Coneixement de la Generalitat de Catalunya (AGAUR 2021-SGR00420). FÁF-Á was supported by a Beatriu de Pinós fellowship from Secretaria d'Universitats i Recerca del Departament de Recerca i Universitats of the Generalitat de Catalunya (Ref. BP 2021 00035) and a Ramón y Cajal fellowship (Ref. RYC2023-043494-I) funded by MCIN/AEI/10.13039/501100011033 and FSE+. This research was supported by the Spanish government through the “Severo Ochoa Centre of Excellence” accreditation (CEX2019-000928-S)Peer reviewedOxford University PressAgencia Estatal de Investigación (España)Ministerio de Universidades (España)European CommissionMinisterio de Ciencia e Innovación (España)Generalitat de Catalunya202620262026info:eu-repo/semantics/articlePublisher's versioninfo:eu-repo/semantics/publishedVersionhttp://hdl.handle.net/10261/431846reponame: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/EC/H2020/948281info:eu-repo/grantAgreement/EC/HE/101129751https://doi.org/10.1093/gbe/evag063Síinfo:eu-repo/semantics/openAccessoai:dnet:digitalcsic_::0a15b1f1c78d78cfc7463ea11be337ce2026-05-22T06:33:51Z
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