Unravelling the complex duplication history of deuterostome glycerol transporters

Transmembrane glycerol transport is an ancient biophysical property that evolved in selected subfamilies of water channel (aquaporin) proteins. Here, we conducted broad level genome (>550) and transcriptome (>300) analyses to unravel the duplication history of the glycerol-transporting channel...

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Detalles Bibliográficos
Autores: Yilmaz, Ozlem, Chauvigné, François, Ferré, Alba, Nilsen, Frank, Fjelldal, Per Gunnar, Cerdà, Joan, Finn, Roderick Nigel
Tipo de recurso: artículo
Fecha de publicación:2020
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:20.500.12327/1055
Acceso en línea:http://hdl.handle.net/20.500.12327/1055
https://doi.org/10.3390/cells9071663
Access Level:acceso abierto
Palabra clave:637
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spelling Unravelling the complex duplication history of deuterostome glycerol transportersYilmaz, OzlemChauvigné, FrançoisFerré, AlbaNilsen, FrankFjelldal, Per GunnarCerdà, JoanFinn, Roderick Nigel637Transmembrane glycerol transport is an ancient biophysical property that evolved in selected subfamilies of water channel (aquaporin) proteins. Here, we conducted broad level genome (>550) and transcriptome (>300) analyses to unravel the duplication history of the glycerol-transporting channels (glps) in Deuterostomia. We found that tandem duplication (TD) was the major mechanism of gene expansion in echinoderms and hemichordates, which, together with whole genome duplications (WGD) in the chordate lineage, continued to shape the genomic repertoires in craniates. Molecular phylogenies indicated that aqp3-like and aqp13-like channels were the probable stem subfamilies in craniates, with WGD generating aqp9 and aqp10 in gnathostomes but aqp7 arising through TD in Osteichthyes. We uncovered separate examples of gene translocations, gene conversion, and concerted evolution in humans, teleosts, and starfishes, with DNA transposons the likely drivers of gene rearrangements in paleotetraploid salmonids. Currently, gene copy numbers and BLAST are poor predictors of orthologous relationships due to asymmetric glp gene evolution in the different lineages. Such asymmetries can impact estimations of divergence times by millions of years. Experimental investigations of the salmonid channels demonstrated that approximately half of the 20 ancestral paralogs are functional, with neofunctionalization occurring at the transcriptional level rather than the protein transport properties. The combined findings resolve the origins and diversification of glps over >800 million years old and thus form the novel basis for proposing a pandeuterostome glp gene nomenclature.info:eu-repo/semantics/publishedVersionMDPIProducció AnimalAqüicultura2020info:eu-repo/semantics/article29http://hdl.handle.net/20.500.12327/1055https://doi.org/10.3390/cells9071663reponame:Recercat. Dipósit de la Recerca de Catalunyainstname:Varias* (Consorci de Biblioteques Universitáries de Catalunya, Centre de Serveis Científics i Acadèmics de Catalunya)InglésCellsMINECO/Programa Estatal de promoción del talento y su empleabilidad en I+D+I/RYC-2015-17103/ES/ /MINECO/Programa Estatal de I+D+I orientada a los retos de la sociedad/AGL2016-76802-R/ES/Canales de agua e ionicos como nuevos marcadores de estrés oxidativo y cinemáticos de la calidad del esperma en teleosteos marinos/SPERMIOPORINAttribution 4.0 Internationalhttp://creativecommons.org/licenses/by/4.0/info:eu-repo/semantics/openAccessoai:recercat.cat:20.500.12327/10552026-05-29T05:05:01Z
dc.title.none.fl_str_mv Unravelling the complex duplication history of deuterostome glycerol transporters
title Unravelling the complex duplication history of deuterostome glycerol transporters
spellingShingle Unravelling the complex duplication history of deuterostome glycerol transporters
Yilmaz, Ozlem
637
title_short Unravelling the complex duplication history of deuterostome glycerol transporters
title_full Unravelling the complex duplication history of deuterostome glycerol transporters
title_fullStr Unravelling the complex duplication history of deuterostome glycerol transporters
title_full_unstemmed Unravelling the complex duplication history of deuterostome glycerol transporters
title_sort Unravelling the complex duplication history of deuterostome glycerol transporters
dc.creator.none.fl_str_mv Yilmaz, Ozlem
Chauvigné, François
Ferré, Alba
Nilsen, Frank
Fjelldal, Per Gunnar
Cerdà, Joan
Finn, Roderick Nigel
author Yilmaz, Ozlem
author_facet Yilmaz, Ozlem
Chauvigné, François
Ferré, Alba
Nilsen, Frank
Fjelldal, Per Gunnar
Cerdà, Joan
Finn, Roderick Nigel
author_role author
author2 Chauvigné, François
Ferré, Alba
Nilsen, Frank
Fjelldal, Per Gunnar
Cerdà, Joan
Finn, Roderick Nigel
author2_role author
author
author
author
author
author
dc.contributor.none.fl_str_mv Producció Animal
Aqüicultura
dc.subject.none.fl_str_mv 637
topic 637
description Transmembrane glycerol transport is an ancient biophysical property that evolved in selected subfamilies of water channel (aquaporin) proteins. Here, we conducted broad level genome (>550) and transcriptome (>300) analyses to unravel the duplication history of the glycerol-transporting channels (glps) in Deuterostomia. We found that tandem duplication (TD) was the major mechanism of gene expansion in echinoderms and hemichordates, which, together with whole genome duplications (WGD) in the chordate lineage, continued to shape the genomic repertoires in craniates. Molecular phylogenies indicated that aqp3-like and aqp13-like channels were the probable stem subfamilies in craniates, with WGD generating aqp9 and aqp10 in gnathostomes but aqp7 arising through TD in Osteichthyes. We uncovered separate examples of gene translocations, gene conversion, and concerted evolution in humans, teleosts, and starfishes, with DNA transposons the likely drivers of gene rearrangements in paleotetraploid salmonids. Currently, gene copy numbers and BLAST are poor predictors of orthologous relationships due to asymmetric glp gene evolution in the different lineages. Such asymmetries can impact estimations of divergence times by millions of years. Experimental investigations of the salmonid channels demonstrated that approximately half of the 20 ancestral paralogs are functional, with neofunctionalization occurring at the transcriptional level rather than the protein transport properties. The combined findings resolve the origins and diversification of glps over >800 million years old and thus form the novel basis for proposing a pandeuterostome glp gene nomenclature.
publishDate 2020
dc.date.none.fl_str_mv 2020
dc.type.none.fl_str_mv info:eu-repo/semantics/article
format article
dc.identifier.none.fl_str_mv http://hdl.handle.net/20.500.12327/1055
https://doi.org/10.3390/cells9071663
url http://hdl.handle.net/20.500.12327/1055
https://doi.org/10.3390/cells9071663
dc.language.none.fl_str_mv Inglés
language_invalid_str_mv Inglés
dc.relation.none.fl_str_mv Cells
MINECO/Programa Estatal de promoción del talento y su empleabilidad en I+D+I/RYC-2015-17103/ES/ /
MINECO/Programa Estatal de I+D+I orientada a los retos de la sociedad/AGL2016-76802-R/ES/Canales de agua e ionicos como nuevos marcadores de estrés oxidativo y cinemáticos de la calidad del esperma en teleosteos marinos/SPERMIOPORIN
dc.rights.none.fl_str_mv Attribution 4.0 International
http://creativecommons.org/licenses/by/4.0/
info:eu-repo/semantics/openAccess
rights_invalid_str_mv Attribution 4.0 International
http://creativecommons.org/licenses/by/4.0/
eu_rights_str_mv openAccess
dc.format.none.fl_str_mv 29
dc.publisher.none.fl_str_mv MDPI
publisher.none.fl_str_mv MDPI
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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score 15,811543

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