Parallel duplication and loss of aquaporin-coding genes during the “out of the sea” transition as potential key drivers of animal terrestrialization

Autores
Martínez Redondo, Gemma I.; Simón Guerrero, Carolina; Arístide, Leandro; Balart García, Pau; Tonzo, Vanina; Fernández, Rosa
Año de publicación
2023
Idioma
inglés
Tipo de recurso
artículo
Estado
versión publicada
Descripción
One of the most important physiological challenges animals had to overcome during terrestrialization (i.e., the transition from sea to land) was water loss, which alters their osmotic and hydric homeostasis. Aquaporins are a superfamily of membrane water transporters heavily involved in osmoregulatory processes. Their diversity and evolutionary dynamics in most animal lineages remain unknown, hampering our understanding of their role in marine–terrestrial transitions. Here, we interrogated aquaporin gene repertoire evolution across the main terrestrial animal lineages. We annotated aquaporin-coding genes in genomic data from 458 species from seven animal phyla where terrestrialization episodes occurred. We then explored aquaporin gene evolutionary dynamics to assess differences between terrestrial and aquatic species through phylogenomics and phylogenetic comparative methods. Our results revealed parallel aquaporin-coding gene duplications during the ecological transition from marine to nonmarine environments (e.g., brackish, freshwater and terrestrial), rather than from aquatic to terrestrial ones, with some notable duplications in ancient lineages. In contrast, we also recovered a significantly lower number of superaquaporin genes in terrestrial arthropods, suggesting that more efficient oxygen homeostasis in land arthropods might be linked to a reduction in this type of aquaporin. Our results thus indicate that aquaporin-coding gene duplication and loss might have been one of the key steps towards the evolution of osmoregulation across animals, facilitating the “out of the sea” transition and ultimately the colonization of land.
Fil: Martínez Redondo, Gemma I.. Consejo Superior de Investigaciones Científicas; España
Fil: Simón Guerrero, Carolina. Consejo Superior de Investigaciones Científicas; España
Fil: Arístide, Leandro. Universidad Nacional Arturo Jauretche. Unidad Ejecutora de Estudios en Neurociencias y Sistemas Complejos. Provincia de Buenos Aires. Ministerio de Salud. Hospital Alta Complejidad en Red El Cruce Dr. Néstor Carlos Kirchner Samic. Unidad Ejecutora de Estudios en Neurociencias y Sistemas Complejos. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - La Plata. Unidad Ejecutora de Estudios en Neurociencias y Sistemas Complejos; Argentina
Fil: Balart García, Pau. Consejo Superior de Investigaciones Científicas; España
Fil: Tonzo, Vanina. Consejo Superior de Investigaciones Científicas; España
Fil: Fernández, Rosa. Consejo Superior de Investigaciones Científicas; España
Materia
EVOLUTION
GENOMICS/PROTEOMICS
INVERTEBRATES
MACROEVOLUTION
MOLECULAR
TRANSCRIPTOMICS
Nivel de accesibilidad
acceso abierto
Condiciones de uso
https://creativecommons.org/licenses/by-nc-nd/2.5/ar/
Repositorio
CONICET Digital (CONICET)
Institución
Consejo Nacional de Investigaciones Científicas y Técnicas
OAI Identificador
oai:ri.conicet.gov.ar:11336/226936
Acceder
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repository_id_str 3498
network_name_str CONICET Digital (CONICET)
spelling Parallel duplication and loss of aquaporin-coding genes during the “out of the sea” transition as potential key drivers of animal terrestrializationMartínez Redondo, Gemma I.Simón Guerrero, CarolinaArístide, LeandroBalart García, PauTonzo, VaninaFernández, RosaEVOLUTIONGENOMICS/PROTEOMICSINVERTEBRATESMACROEVOLUTIONMOLECULARTRANSCRIPTOMICShttps://purl.org/becyt/ford/1.6https://purl.org/becyt/ford/1One of the most important physiological challenges animals had to overcome during terrestrialization (i.e., the transition from sea to land) was water loss, which alters their osmotic and hydric homeostasis. Aquaporins are a superfamily of membrane water transporters heavily involved in osmoregulatory processes. Their diversity and evolutionary dynamics in most animal lineages remain unknown, hampering our understanding of their role in marine–terrestrial transitions. Here, we interrogated aquaporin gene repertoire evolution across the main terrestrial animal lineages. We annotated aquaporin-coding genes in genomic data from 458 species from seven animal phyla where terrestrialization episodes occurred. We then explored aquaporin gene evolutionary dynamics to assess differences between terrestrial and aquatic species through phylogenomics and phylogenetic comparative methods. Our results revealed parallel aquaporin-coding gene duplications during the ecological transition from marine to nonmarine environments (e.g., brackish, freshwater and terrestrial), rather than from aquatic to terrestrial ones, with some notable duplications in ancient lineages. In contrast, we also recovered a significantly lower number of superaquaporin genes in terrestrial arthropods, suggesting that more efficient oxygen homeostasis in land arthropods might be linked to a reduction in this type of aquaporin. Our results thus indicate that aquaporin-coding gene duplication and loss might have been one of the key steps towards the evolution of osmoregulation across animals, facilitating the “out of the sea” transition and ultimately the colonization of land.Fil: Martínez Redondo, Gemma I.. Consejo Superior de Investigaciones Científicas; EspañaFil: Simón Guerrero, Carolina. Consejo Superior de Investigaciones Científicas; EspañaFil: Arístide, Leandro. Universidad Nacional Arturo Jauretche. Unidad Ejecutora de Estudios en Neurociencias y Sistemas Complejos. Provincia de Buenos Aires. Ministerio de Salud. Hospital Alta Complejidad en Red El Cruce Dr. Néstor Carlos Kirchner Samic. Unidad Ejecutora de Estudios en Neurociencias y Sistemas Complejos. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - La Plata. Unidad Ejecutora de Estudios en Neurociencias y Sistemas Complejos; ArgentinaFil: Balart García, Pau. Consejo Superior de Investigaciones Científicas; EspañaFil: Tonzo, Vanina. Consejo Superior de Investigaciones Científicas; EspañaFil: Fernández, Rosa. Consejo Superior de Investigaciones Científicas; EspañaWiley Blackwell Publishing, Inc2023-04info:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersionhttp://purl.org/coar/resource_type/c_6501info:ar-repo/semantics/articuloapplication/pdfapplication/pdfhttp://hdl.handle.net/11336/226936Martínez Redondo, Gemma I.; Simón Guerrero, Carolina; Arístide, Leandro; Balart García, Pau; Tonzo, Vanina; et al.; Parallel duplication and loss of aquaporin-coding genes during the “out of the sea” transition as potential key drivers of animal terrestrialization; Wiley Blackwell Publishing, Inc; Molecular Ecology; 32; 8; 4-2023; 2022-20400962-1083CONICET DigitalCONICETenginfo:eu-repo/semantics/altIdentifier/doi/10.1111/mec.16854info:eu-repo/semantics/openAccesshttps://creativecommons.org/licenses/by-nc-nd/2.5/ar/reponame:CONICET Digital (CONICET)instname:Consejo Nacional de Investigaciones Científicas y Técnicas2025-10-22T11:05:25Zoai:ri.conicet.gov.ar:11336/226936instacron:CONICETInstitucionalhttp://ri.conicet.gov.ar/Organismo científico-tecnológicoNo correspondehttp://ri.conicet.gov.ar/oai/requestdasensio@conicet.gov.ar; lcarlino@conicet.gov.arArgentinaNo correspondeNo correspondeNo correspondeopendoar:34982025-10-22 11:05:25.89CONICET Digital (CONICET) - Consejo Nacional de Investigaciones Científicas y Técnicasfalse
dc.title.none.fl_str_mv Parallel duplication and loss of aquaporin-coding genes during the “out of the sea” transition as potential key drivers of animal terrestrialization
title Parallel duplication and loss of aquaporin-coding genes during the “out of the sea” transition as potential key drivers of animal terrestrialization
spellingShingle Parallel duplication and loss of aquaporin-coding genes during the “out of the sea” transition as potential key drivers of animal terrestrialization
Martínez Redondo, Gemma I.
EVOLUTION
GENOMICS/PROTEOMICS
INVERTEBRATES
MACROEVOLUTION
MOLECULAR
TRANSCRIPTOMICS
title_short Parallel duplication and loss of aquaporin-coding genes during the “out of the sea” transition as potential key drivers of animal terrestrialization
title_full Parallel duplication and loss of aquaporin-coding genes during the “out of the sea” transition as potential key drivers of animal terrestrialization
title_fullStr Parallel duplication and loss of aquaporin-coding genes during the “out of the sea” transition as potential key drivers of animal terrestrialization
title_full_unstemmed Parallel duplication and loss of aquaporin-coding genes during the “out of the sea” transition as potential key drivers of animal terrestrialization
title_sort Parallel duplication and loss of aquaporin-coding genes during the “out of the sea” transition as potential key drivers of animal terrestrialization
dc.creator.none.fl_str_mv Martínez Redondo, Gemma I.
Simón Guerrero, Carolina
Arístide, Leandro
Balart García, Pau
Tonzo, Vanina
Fernández, Rosa
author Martínez Redondo, Gemma I.
author_facet Martínez Redondo, Gemma I.
Simón Guerrero, Carolina
Arístide, Leandro
Balart García, Pau
Tonzo, Vanina
Fernández, Rosa
author_role author
author2 Simón Guerrero, Carolina
Arístide, Leandro
Balart García, Pau
Tonzo, Vanina
Fernández, Rosa
author2_role author
author
author
author
author
dc.subject.none.fl_str_mv EVOLUTION
GENOMICS/PROTEOMICS
INVERTEBRATES
MACROEVOLUTION
MOLECULAR
TRANSCRIPTOMICS
topic EVOLUTION
GENOMICS/PROTEOMICS
INVERTEBRATES
MACROEVOLUTION
MOLECULAR
TRANSCRIPTOMICS
purl_subject.fl_str_mv https://purl.org/becyt/ford/1.6
https://purl.org/becyt/ford/1
dc.description.none.fl_txt_mv One of the most important physiological challenges animals had to overcome during terrestrialization (i.e., the transition from sea to land) was water loss, which alters their osmotic and hydric homeostasis. Aquaporins are a superfamily of membrane water transporters heavily involved in osmoregulatory processes. Their diversity and evolutionary dynamics in most animal lineages remain unknown, hampering our understanding of their role in marine–terrestrial transitions. Here, we interrogated aquaporin gene repertoire evolution across the main terrestrial animal lineages. We annotated aquaporin-coding genes in genomic data from 458 species from seven animal phyla where terrestrialization episodes occurred. We then explored aquaporin gene evolutionary dynamics to assess differences between terrestrial and aquatic species through phylogenomics and phylogenetic comparative methods. Our results revealed parallel aquaporin-coding gene duplications during the ecological transition from marine to nonmarine environments (e.g., brackish, freshwater and terrestrial), rather than from aquatic to terrestrial ones, with some notable duplications in ancient lineages. In contrast, we also recovered a significantly lower number of superaquaporin genes in terrestrial arthropods, suggesting that more efficient oxygen homeostasis in land arthropods might be linked to a reduction in this type of aquaporin. Our results thus indicate that aquaporin-coding gene duplication and loss might have been one of the key steps towards the evolution of osmoregulation across animals, facilitating the “out of the sea” transition and ultimately the colonization of land.
Fil: Martínez Redondo, Gemma I.. Consejo Superior de Investigaciones Científicas; España
Fil: Simón Guerrero, Carolina. Consejo Superior de Investigaciones Científicas; España
Fil: Arístide, Leandro. Universidad Nacional Arturo Jauretche. Unidad Ejecutora de Estudios en Neurociencias y Sistemas Complejos. Provincia de Buenos Aires. Ministerio de Salud. Hospital Alta Complejidad en Red El Cruce Dr. Néstor Carlos Kirchner Samic. Unidad Ejecutora de Estudios en Neurociencias y Sistemas Complejos. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - La Plata. Unidad Ejecutora de Estudios en Neurociencias y Sistemas Complejos; Argentina
Fil: Balart García, Pau. Consejo Superior de Investigaciones Científicas; España
Fil: Tonzo, Vanina. Consejo Superior de Investigaciones Científicas; España
Fil: Fernández, Rosa. Consejo Superior de Investigaciones Científicas; España
description One of the most important physiological challenges animals had to overcome during terrestrialization (i.e., the transition from sea to land) was water loss, which alters their osmotic and hydric homeostasis. Aquaporins are a superfamily of membrane water transporters heavily involved in osmoregulatory processes. Their diversity and evolutionary dynamics in most animal lineages remain unknown, hampering our understanding of their role in marine–terrestrial transitions. Here, we interrogated aquaporin gene repertoire evolution across the main terrestrial animal lineages. We annotated aquaporin-coding genes in genomic data from 458 species from seven animal phyla where terrestrialization episodes occurred. We then explored aquaporin gene evolutionary dynamics to assess differences between terrestrial and aquatic species through phylogenomics and phylogenetic comparative methods. Our results revealed parallel aquaporin-coding gene duplications during the ecological transition from marine to nonmarine environments (e.g., brackish, freshwater and terrestrial), rather than from aquatic to terrestrial ones, with some notable duplications in ancient lineages. In contrast, we also recovered a significantly lower number of superaquaporin genes in terrestrial arthropods, suggesting that more efficient oxygen homeostasis in land arthropods might be linked to a reduction in this type of aquaporin. Our results thus indicate that aquaporin-coding gene duplication and loss might have been one of the key steps towards the evolution of osmoregulation across animals, facilitating the “out of the sea” transition and ultimately the colonization of land.
publishDate 2023
dc.date.none.fl_str_mv 2023-04
dc.type.none.fl_str_mv info:eu-repo/semantics/article
info:eu-repo/semantics/publishedVersion
http://purl.org/coar/resource_type/c_6501
info:ar-repo/semantics/articulo
format article
status_str publishedVersion
dc.identifier.none.fl_str_mv http://hdl.handle.net/11336/226936
Martínez Redondo, Gemma I.; Simón Guerrero, Carolina; Arístide, Leandro; Balart García, Pau; Tonzo, Vanina; et al.; Parallel duplication and loss of aquaporin-coding genes during the “out of the sea” transition as potential key drivers of animal terrestrialization; Wiley Blackwell Publishing, Inc; Molecular Ecology; 32; 8; 4-2023; 2022-2040
0962-1083
CONICET Digital
CONICET
url http://hdl.handle.net/11336/226936
identifier_str_mv Martínez Redondo, Gemma I.; Simón Guerrero, Carolina; Arístide, Leandro; Balart García, Pau; Tonzo, Vanina; et al.; Parallel duplication and loss of aquaporin-coding genes during the “out of the sea” transition as potential key drivers of animal terrestrialization; Wiley Blackwell Publishing, Inc; Molecular Ecology; 32; 8; 4-2023; 2022-2040
0962-1083
CONICET Digital
CONICET
dc.language.none.fl_str_mv eng
language eng
dc.relation.none.fl_str_mv info:eu-repo/semantics/altIdentifier/doi/10.1111/mec.16854
dc.rights.none.fl_str_mv info:eu-repo/semantics/openAccess
https://creativecommons.org/licenses/by-nc-nd/2.5/ar/
eu_rights_str_mv openAccess
rights_invalid_str_mv https://creativecommons.org/licenses/by-nc-nd/2.5/ar/
dc.format.none.fl_str_mv application/pdf
application/pdf
dc.publisher.none.fl_str_mv Wiley Blackwell Publishing, Inc
publisher.none.fl_str_mv Wiley Blackwell Publishing, Inc
dc.source.none.fl_str_mv reponame:CONICET Digital (CONICET)
instname:Consejo Nacional de Investigaciones Científicas y Técnicas
reponame_str CONICET Digital (CONICET)
collection CONICET Digital (CONICET)
instname_str Consejo Nacional de Investigaciones Científicas y Técnicas
repository.name.fl_str_mv CONICET Digital (CONICET) - Consejo Nacional de Investigaciones Científicas y Técnicas
repository.mail.fl_str_mv dasensio@conicet.gov.ar; lcarlino@conicet.gov.ar
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score 12.982451

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