Co-elimination and survival in gene network evolution: dismantling the RA-signaling in a chordate

The bloom of Genomics is revealing gene loss as a pervasive evolutionary force generating genetic diversity that shapes the evolution of species. Outside bacteria and yeast, however, the understanding of the process of gene loss remains elusive, especially in the evolution of animal species. Here, u...

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Autores: Martí-Solans, Josep, Belyaeva, Olga V., Torres Águila, Nuria Paz, Kedishvili, Natalia Y., Albalat Rodríguez, Ricard, Cañestro García, Cristian
Tipo de recurso: artículo
Estado:Versión aceptada para publicación
Fecha de publicación:2016
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:2445/198069
Acceso en línea:https://hdl.handle.net/2445/198069
Access Level:acceso abierto
Palabra clave:Cordats
Genòmica
Chordata
Genomics
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spelling Co-elimination and survival in gene network evolution: dismantling the RA-signaling in a chordateMartí-Solans, JosepBelyaeva, Olga V.Torres Águila, Nuria PazKedishvili, Natalia Y.Albalat Rodríguez, RicardCañestro García, CristianCordatsGenòmicaChordataGenomicsThe bloom of Genomics is revealing gene loss as a pervasive evolutionary force generating genetic diversity that shapes the evolution of species. Outside bacteria and yeast, however, the understanding of the process of gene loss remains elusive, especially in the evolution of animal species. Here, using the dismantling of the retinoic acid metabolic gene network (RA-MGN) in the chordate Oikopleura dioica as a case study, we combine approaches of comparative genomics, phylogenetics, biochemistry and developmental biology to investigate the mutational robustness associated to biased patterns of gene loss. We demonstrate the absence of alternative pathways for RA-synthesis in O. dioica, which suggests that gene losses of RA-MGN were not compensated by mutational robustness, but occurred in a scenario of regressive evolution. In addition, the lack of drastic phenotypic changes associated to the loss of RA-signaling provides an example of the inverse paradox of Evo-Devo. This work illustrates how the identification of patterns of gene co-elimination - in our case five losses (Rdh10, Rdh16, Bco1, Aldh1a and Cyp26)- is a useful strategy to recognize gene network modules associated to distinct functions. Our work also illustrates how the identification of survival genes helps to recognize neofunctionalization events and ancestral functions. Thus, the survival and extensive duplication of Cco and RdhE2 in O. dioica correlated with the acquisition of complex compartmentalization of expression domains in the digestive system and a process of enzymatic neofunctionalization of the Cco, while the surviving Aldh8 could be related to its ancestral housekeeping role against toxic aldehydes.Oxford University Press2023202320162023info:eu-repo/semantics/articleinfo:eu-repo/semantics/acceptedVersion16 p.application/pdfapplication/pdfhttps://hdl.handle.net/2445/198069Articles publicats en revistes (Genètica, Microbiologia i Estadística)reponame:Recercat. Dipósit de la Recerca de Catalunyainstname:Varias* (Consorci de Biblioteques Universitáries de Catalunya, Centre de Serveis Científics i Acadèmics de Catalunya)InglésVersió postprint del document publicat a: https://doi.org/10.1093/molbev/msw118Molecular Biology and Evolution, 2016, vol. 33, num. 9, p. 2401-2416https://doi.org/10.1093/molbev/msw118(c) Martí-Solans, Josep et al., 2016info:eu-repo/semantics/openAccessoai:recercat.cat:2445/1980692026-05-29T05:05:01Z
dc.title.none.fl_str_mv Co-elimination and survival in gene network evolution: dismantling the RA-signaling in a chordate
title Co-elimination and survival in gene network evolution: dismantling the RA-signaling in a chordate
spellingShingle Co-elimination and survival in gene network evolution: dismantling the RA-signaling in a chordate
Martí-Solans, Josep
Cordats
Genòmica
Chordata
Genomics
title_short Co-elimination and survival in gene network evolution: dismantling the RA-signaling in a chordate
title_full Co-elimination and survival in gene network evolution: dismantling the RA-signaling in a chordate
title_fullStr Co-elimination and survival in gene network evolution: dismantling the RA-signaling in a chordate
title_full_unstemmed Co-elimination and survival in gene network evolution: dismantling the RA-signaling in a chordate
title_sort Co-elimination and survival in gene network evolution: dismantling the RA-signaling in a chordate
dc.creator.none.fl_str_mv Martí-Solans, Josep
Belyaeva, Olga V.
Torres Águila, Nuria Paz
Kedishvili, Natalia Y.
Albalat Rodríguez, Ricard
Cañestro García, Cristian
author Martí-Solans, Josep
author_facet Martí-Solans, Josep
Belyaeva, Olga V.
Torres Águila, Nuria Paz
Kedishvili, Natalia Y.
Albalat Rodríguez, Ricard
Cañestro García, Cristian
author_role author
author2 Belyaeva, Olga V.
Torres Águila, Nuria Paz
Kedishvili, Natalia Y.
Albalat Rodríguez, Ricard
Cañestro García, Cristian
author2_role author
author
author
author
author
dc.subject.none.fl_str_mv Cordats
Genòmica
Chordata
Genomics
topic Cordats
Genòmica
Chordata
Genomics
description The bloom of Genomics is revealing gene loss as a pervasive evolutionary force generating genetic diversity that shapes the evolution of species. Outside bacteria and yeast, however, the understanding of the process of gene loss remains elusive, especially in the evolution of animal species. Here, using the dismantling of the retinoic acid metabolic gene network (RA-MGN) in the chordate Oikopleura dioica as a case study, we combine approaches of comparative genomics, phylogenetics, biochemistry and developmental biology to investigate the mutational robustness associated to biased patterns of gene loss. We demonstrate the absence of alternative pathways for RA-synthesis in O. dioica, which suggests that gene losses of RA-MGN were not compensated by mutational robustness, but occurred in a scenario of regressive evolution. In addition, the lack of drastic phenotypic changes associated to the loss of RA-signaling provides an example of the inverse paradox of Evo-Devo. This work illustrates how the identification of patterns of gene co-elimination - in our case five losses (Rdh10, Rdh16, Bco1, Aldh1a and Cyp26)- is a useful strategy to recognize gene network modules associated to distinct functions. Our work also illustrates how the identification of survival genes helps to recognize neofunctionalization events and ancestral functions. Thus, the survival and extensive duplication of Cco and RdhE2 in O. dioica correlated with the acquisition of complex compartmentalization of expression domains in the digestive system and a process of enzymatic neofunctionalization of the Cco, while the surviving Aldh8 could be related to its ancestral housekeeping role against toxic aldehydes.
publishDate 2016
dc.date.none.fl_str_mv 2016
2023
2023
2023
dc.type.none.fl_str_mv info:eu-repo/semantics/article
info:eu-repo/semantics/acceptedVersion
format article
status_str acceptedVersion
dc.identifier.none.fl_str_mv https://hdl.handle.net/2445/198069
url https://hdl.handle.net/2445/198069
dc.language.none.fl_str_mv Inglés
language_invalid_str_mv Inglés
dc.relation.none.fl_str_mv Versió postprint del document publicat a: https://doi.org/10.1093/molbev/msw118
Molecular Biology and Evolution, 2016, vol. 33, num. 9, p. 2401-2416
https://doi.org/10.1093/molbev/msw118
dc.rights.none.fl_str_mv (c) Martí-Solans, Josep et al., 2016
info:eu-repo/semantics/openAccess
rights_invalid_str_mv (c) Martí-Solans, Josep et al., 2016
eu_rights_str_mv openAccess
dc.format.none.fl_str_mv 16 p.
application/pdf
application/pdf
dc.publisher.none.fl_str_mv Oxford University Press
publisher.none.fl_str_mv Oxford University Press
dc.source.none.fl_str_mv Articles publicats en revistes (Genètica, Microbiologia i Estadística)
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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