Molecular, phylogenetic and developmental analyses of Sall proteins in bilaterians

Background: Sall (Spalt-like) proteins are zinc-finger transcription factors involved in a number of biological processes. They have only been studied in a few model organisms, such as Drosophila melanogaster, Caenorhabditis elegans, Schmidtea mediterranea and some vertebrates. Further taxon samplin...

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Autores: Lorente-Sorolla, José, Truchado-García, Marta, Perry, Kimberly J., Henry, Jonathan Q., Grande, Cristina
Tipo de recurso: artículo
Estado:Versión publicada
Fecha de publicación:2018
País:España
Institución:Consejo Superior de Investigaciones Científicas (CSIC)
Repositorio:DIGITAL.CSIC. Repositorio Institucional del CSIC
OAI Identifier:oai:digital.csic.es:10261/179674
Acceso en línea:http://hdl.handle.net/10261/179674
Access Level:acceso abierto
Palabra clave:Sall
Lottia gigantea
Spalt
Protein domains
Gene evolution
Spiralia
Gastropoda
Crepidula fornicata
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spelling Molecular, phylogenetic and developmental analyses of Sall proteins in bilateriansLorente-Sorolla, JoséTruchado-García, MartaPerry, Kimberly J.Henry, Jonathan Q.Grande, CristinaSallLottia giganteaSpaltProtein domainsGene evolutionSpiraliaGastropodaCrepidula fornicataBackground: Sall (Spalt-like) proteins are zinc-finger transcription factors involved in a number of biological processes. They have only been studied in a few model organisms, such as Drosophila melanogaster, Caenorhabditis elegans, Schmidtea mediterranea and some vertebrates. Further taxon sampling is critical to understand the evolution and diversification of this protein and its functional roles in animals. Results: Using genome and transcriptome mining, we confirmed the presence of sall genes in a range of additional animal taxa, for which their presence had not yet been described. We show that sall genes are broadly conserved across the Bilateria, and likely appeared in the bilaterian stem lineage. Our analysis of the protein domains shows that the characteristic arrangement of the multiple zinc-finger domains is conserved in bilaterians and may represent the ancient arrangement of this family of transcription factors. We also show the existence of a previously unknown zinc-finger domain. In situ hybridization was used to describe the gene expression patterns in embryonic and larval stages in two species of snails: Crepidula fornicata and Lottia gigantea. In L. gigantea, sall presents maternal expression, although later on the expression is restricted to the A and B quadrants during gastrulation and larval stage. In C. fornicata, sall has no maternal expression and it is expressed mainly in the A, C and D quadrants during blastula stages and in an asymmetric fashion during the larval stage. Discussion:Our results suggest that the bilaterian common ancestor had a Sall protein with at least six zinc-finger domains. The evolution of Sall proteins in bilaterians might have occurred mostly as a result of the loss of protein domains and gene duplications leading to diversification. The new evidence complements previous studies in highlighting an important role of Sall proteins in bilaterian development. Our results show maternal expression of sall in the snail L. gigantea, but not C. fornicata. The asymmetric expression shown in the ectoderm of the trochophore larva of snails is probably related to shell/mantle development. The observed sall expression in cephalic tissue in snails and some other bilaterians suggests a possible ancestral role of sall in neural development in bilaterians.Spanish MEC (Ministerio de Economia y Competividad)Peer ReviewedMinisterio de Economía y Competitividad (España)Consejo Superior de Investigaciones Científicas [https://ror.org/02gfc7t72]2019201920182019info:eu-repo/semantics/articlehttp://purl.org/coar/resource_type/c_6501Publisher's versioninfo:eu-repo/semantics/publishedVersionhttp://hdl.handle.net/10261/179674reponame:DIGITAL.CSIC. Repositorio Institucional del CSICinstname:Consejo Superior de Investigaciones Científicas (CSIC)InglésSíinfo:eu-repo/semantics/openAccessoai:digital.csic.es:10261/1796742026-05-22T06:33:51Z
dc.title.none.fl_str_mv Molecular, phylogenetic and developmental analyses of Sall proteins in bilaterians
title Molecular, phylogenetic and developmental analyses of Sall proteins in bilaterians
spellingShingle Molecular, phylogenetic and developmental analyses of Sall proteins in bilaterians
Lorente-Sorolla, José
Sall
Lottia gigantea
Spalt
Protein domains
Gene evolution
Spiralia
Gastropoda
Crepidula fornicata
title_short Molecular, phylogenetic and developmental analyses of Sall proteins in bilaterians
title_full Molecular, phylogenetic and developmental analyses of Sall proteins in bilaterians
title_fullStr Molecular, phylogenetic and developmental analyses of Sall proteins in bilaterians
title_full_unstemmed Molecular, phylogenetic and developmental analyses of Sall proteins in bilaterians
title_sort Molecular, phylogenetic and developmental analyses of Sall proteins in bilaterians
dc.creator.none.fl_str_mv Lorente-Sorolla, José
Truchado-García, Marta
Perry, Kimberly J.
Henry, Jonathan Q.
Grande, Cristina
author Lorente-Sorolla, José
author_facet Lorente-Sorolla, José
Truchado-García, Marta
Perry, Kimberly J.
Henry, Jonathan Q.
Grande, Cristina
author_role author
author2 Truchado-García, Marta
Perry, Kimberly J.
Henry, Jonathan Q.
Grande, Cristina
author2_role author
author
author
author
dc.contributor.none.fl_str_mv Ministerio de Economía y Competitividad (España)
Consejo Superior de Investigaciones Científicas [https://ror.org/02gfc7t72]
dc.subject.none.fl_str_mv Sall
Lottia gigantea
Spalt
Protein domains
Gene evolution
Spiralia
Gastropoda
Crepidula fornicata
topic Sall
Lottia gigantea
Spalt
Protein domains
Gene evolution
Spiralia
Gastropoda
Crepidula fornicata
description Background: Sall (Spalt-like) proteins are zinc-finger transcription factors involved in a number of biological processes. They have only been studied in a few model organisms, such as Drosophila melanogaster, Caenorhabditis elegans, Schmidtea mediterranea and some vertebrates. Further taxon sampling is critical to understand the evolution and diversification of this protein and its functional roles in animals. Results: Using genome and transcriptome mining, we confirmed the presence of sall genes in a range of additional animal taxa, for which their presence had not yet been described. We show that sall genes are broadly conserved across the Bilateria, and likely appeared in the bilaterian stem lineage. Our analysis of the protein domains shows that the characteristic arrangement of the multiple zinc-finger domains is conserved in bilaterians and may represent the ancient arrangement of this family of transcription factors. We also show the existence of a previously unknown zinc-finger domain. In situ hybridization was used to describe the gene expression patterns in embryonic and larval stages in two species of snails: Crepidula fornicata and Lottia gigantea. In L. gigantea, sall presents maternal expression, although later on the expression is restricted to the A and B quadrants during gastrulation and larval stage. In C. fornicata, sall has no maternal expression and it is expressed mainly in the A, C and D quadrants during blastula stages and in an asymmetric fashion during the larval stage. Discussion:Our results suggest that the bilaterian common ancestor had a Sall protein with at least six zinc-finger domains. The evolution of Sall proteins in bilaterians might have occurred mostly as a result of the loss of protein domains and gene duplications leading to diversification. The new evidence complements previous studies in highlighting an important role of Sall proteins in bilaterian development. Our results show maternal expression of sall in the snail L. gigantea, but not C. fornicata. The asymmetric expression shown in the ectoderm of the trochophore larva of snails is probably related to shell/mantle development. The observed sall expression in cephalic tissue in snails and some other bilaterians suggests a possible ancestral role of sall in neural development in bilaterians.
publishDate 2018
dc.date.none.fl_str_mv 2018
2019
2019
2019
dc.type.none.fl_str_mv info:eu-repo/semantics/article
http://purl.org/coar/resource_type/c_6501
Publisher's version
info:eu-repo/semantics/publishedVersion
format article
status_str publishedVersion
dc.identifier.none.fl_str_mv http://hdl.handle.net/10261/179674
url http://hdl.handle.net/10261/179674
dc.language.none.fl_str_mv Inglés
language_invalid_str_mv Inglés
dc.relation.none.fl_str_mv Sí
dc.rights.none.fl_str_mv info:eu-repo/semantics/openAccess
eu_rights_str_mv openAccess
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
repository.mail.fl_str_mv
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score 15,812429

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