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
- Institución
- Consejo Nacional de Investigaciones Científicas y Técnicas
- OAI Identificador
- oai:ri.conicet.gov.ar:11336/226936
Ver los metadatos del registro completo
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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 Técnicas2025-09-29T09:37:16Zoai: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:34982025-09-29 09:37:17.071CONICET 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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1844613173651439616 |
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13.070432 |