Diverse Cis-Regulatory Mechanisms Contribute to Expression Evolution of Tandem Gene Duplicates

Detalhes bibliográficos
Autor(a) principal: Baudouin-Gonzalez, Luís
Data de Publicação: 2017
Outros Autores: Santos, Marília A., Tempesta, Camille, Sucena, Élio, Roch, Fernando, Tanaka, Kohtaro
Tipo de documento: Artigo
Idioma: eng
Título da fonte: Repositório Científico de Acesso Aberto de Portugal (Repositórios Cientìficos)
Texto Completo: http://hdl.handle.net/10400.7/803
Resumo: Pairs of duplicated genes generally display a combination of conserved expression patterns inherited from their unduplicated ancestor and newly acquired domains. However, how the cis-regulatory architecture of duplicated loci evolves to produce these expression patterns is poorly understood. We have directly examined the gene-regulatory evolution of two tandem duplicates, the Drosophila Ly6 genes CG9336 and CG9338, which arose at the base of the drosophilids between 40 and 60 million years ago. Comparing the expression patterns of the two paralogs in four Drosophila species with that of the unduplicated ortholog in the tephritid Ceratitis capitata, we show that they diverged from each other as well as from the unduplicated ortholog. Moreover, the expression divergence appears to have occurred close to the duplication event and also more recently in a lineage-specific manner. The comparison of the tissue-specific cis-regulatory modules (CRMs) controlling the paralog expression in the four Drosophila species indicates that diverse cis-regulatory mechanisms, including the novel tissue-specific enhancers, differential inactivation, and enhancer sharing, contributed to the expression evolution. Our analysis also reveals a surprisingly variable cis-regulatory architecture, in which the CRMs driving conserved expression domains change in number, location, and specificity. Altogether, this study provides a detailed historical account that uncovers a highly dynamic picture of how the paralog expression patterns and their underlying cis-regulatory landscape evolve. We argue that our findings will encourage studying cis-regulatory evolution at the whole-locus level in order to understand how interactions between enhancers and other regulatory levels shape the evolution of gene expression.
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spelling Diverse Cis-Regulatory Mechanisms Contribute to Expression Evolution of Tandem Gene Duplicatescis-regulatory evolutionenhancerDrosophilagene duplicationgene regulationPairs of duplicated genes generally display a combination of conserved expression patterns inherited from their unduplicated ancestor and newly acquired domains. However, how the cis-regulatory architecture of duplicated loci evolves to produce these expression patterns is poorly understood. We have directly examined the gene-regulatory evolution of two tandem duplicates, the Drosophila Ly6 genes CG9336 and CG9338, which arose at the base of the drosophilids between 40 and 60 million years ago. Comparing the expression patterns of the two paralogs in four Drosophila species with that of the unduplicated ortholog in the tephritid Ceratitis capitata, we show that they diverged from each other as well as from the unduplicated ortholog. Moreover, the expression divergence appears to have occurred close to the duplication event and also more recently in a lineage-specific manner. The comparison of the tissue-specific cis-regulatory modules (CRMs) controlling the paralog expression in the four Drosophila species indicates that diverse cis-regulatory mechanisms, including the novel tissue-specific enhancers, differential inactivation, and enhancer sharing, contributed to the expression evolution. Our analysis also reveals a surprisingly variable cis-regulatory architecture, in which the CRMs driving conserved expression domains change in number, location, and specificity. Altogether, this study provides a detailed historical account that uncovers a highly dynamic picture of how the paralog expression patterns and their underlying cis-regulatory landscape evolve. We argue that our findings will encourage studying cis-regulatory evolution at the whole-locus level in order to understand how interactions between enhancers and other regulatory levels shape the evolution of gene expression.Oxford University PressARCABaudouin-Gonzalez, LuísSantos, Marília A.Tempesta, CamilleSucena, ÉlioRoch, FernandoTanaka, Kohtaro2018-10-01T00:30:08Z2017-092017-09-01T00:00:00Zinfo:eu-repo/semantics/publishedVersioninfo:eu-repo/semantics/articleapplication/pdfhttp://hdl.handle.net/10400.7/803eng10.1093/molbev/msx237info:eu-repo/semantics/openAccessreponame:Repositório Científico de Acesso Aberto de Portugal (Repositórios Cientìficos)instname:Agência para a Sociedade do Conhecimento (UMIC) - FCT - Sociedade da Informaçãoinstacron:RCAAP2024-11-21T14:21:10Zoai:arca.igc.gulbenkian.pt:10400.7/803Portal AgregadorONGhttps://www.rcaap.pt/oai/openairemluisa.alvim@gmail.comopendoar:71602024-11-21T14:21:10Repositório Científico de Acesso Aberto de Portugal (Repositórios Cientìficos) - Agência para a Sociedade do Conhecimento (UMIC) - FCT - Sociedade da Informaçãofalse
dc.title.none.fl_str_mv Diverse Cis-Regulatory Mechanisms Contribute to Expression Evolution of Tandem Gene Duplicates
title Diverse Cis-Regulatory Mechanisms Contribute to Expression Evolution of Tandem Gene Duplicates
spellingShingle Diverse Cis-Regulatory Mechanisms Contribute to Expression Evolution of Tandem Gene Duplicates
Baudouin-Gonzalez, Luís
cis-regulatory evolution
enhancer
Drosophila
gene duplication
gene regulation
title_short Diverse Cis-Regulatory Mechanisms Contribute to Expression Evolution of Tandem Gene Duplicates
title_full Diverse Cis-Regulatory Mechanisms Contribute to Expression Evolution of Tandem Gene Duplicates
title_fullStr Diverse Cis-Regulatory Mechanisms Contribute to Expression Evolution of Tandem Gene Duplicates
title_full_unstemmed Diverse Cis-Regulatory Mechanisms Contribute to Expression Evolution of Tandem Gene Duplicates
title_sort Diverse Cis-Regulatory Mechanisms Contribute to Expression Evolution of Tandem Gene Duplicates
author Baudouin-Gonzalez, Luís
author_facet Baudouin-Gonzalez, Luís
Santos, Marília A.
Tempesta, Camille
Sucena, Élio
Roch, Fernando
Tanaka, Kohtaro
author_role author
author2 Santos, Marília A.
Tempesta, Camille
Sucena, Élio
Roch, Fernando
Tanaka, Kohtaro
author2_role author
author
author
author
author
dc.contributor.none.fl_str_mv ARCA
dc.contributor.author.fl_str_mv Baudouin-Gonzalez, Luís
Santos, Marília A.
Tempesta, Camille
Sucena, Élio
Roch, Fernando
Tanaka, Kohtaro
dc.subject.por.fl_str_mv cis-regulatory evolution
enhancer
Drosophila
gene duplication
gene regulation
topic cis-regulatory evolution
enhancer
Drosophila
gene duplication
gene regulation
description Pairs of duplicated genes generally display a combination of conserved expression patterns inherited from their unduplicated ancestor and newly acquired domains. However, how the cis-regulatory architecture of duplicated loci evolves to produce these expression patterns is poorly understood. We have directly examined the gene-regulatory evolution of two tandem duplicates, the Drosophila Ly6 genes CG9336 and CG9338, which arose at the base of the drosophilids between 40 and 60 million years ago. Comparing the expression patterns of the two paralogs in four Drosophila species with that of the unduplicated ortholog in the tephritid Ceratitis capitata, we show that they diverged from each other as well as from the unduplicated ortholog. Moreover, the expression divergence appears to have occurred close to the duplication event and also more recently in a lineage-specific manner. The comparison of the tissue-specific cis-regulatory modules (CRMs) controlling the paralog expression in the four Drosophila species indicates that diverse cis-regulatory mechanisms, including the novel tissue-specific enhancers, differential inactivation, and enhancer sharing, contributed to the expression evolution. Our analysis also reveals a surprisingly variable cis-regulatory architecture, in which the CRMs driving conserved expression domains change in number, location, and specificity. Altogether, this study provides a detailed historical account that uncovers a highly dynamic picture of how the paralog expression patterns and their underlying cis-regulatory landscape evolve. We argue that our findings will encourage studying cis-regulatory evolution at the whole-locus level in order to understand how interactions between enhancers and other regulatory levels shape the evolution of gene expression.
publishDate 2017
dc.date.none.fl_str_mv 2017-09
2017-09-01T00:00:00Z
2018-10-01T00:30:08Z
dc.type.status.fl_str_mv info:eu-repo/semantics/publishedVersion
dc.type.driver.fl_str_mv info:eu-repo/semantics/article
format article
status_str publishedVersion
dc.identifier.uri.fl_str_mv http://hdl.handle.net/10400.7/803
url http://hdl.handle.net/10400.7/803
dc.language.iso.fl_str_mv eng
language eng
dc.relation.none.fl_str_mv 10.1093/molbev/msx237
dc.rights.driver.fl_str_mv info:eu-repo/semantics/openAccess
eu_rights_str_mv openAccess
dc.format.none.fl_str_mv 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 reponame:Repositório Científico de Acesso Aberto de Portugal (Repositórios Cientìficos)
instname:Agência para a Sociedade do Conhecimento (UMIC) - FCT - Sociedade da Informação
instacron:RCAAP
instname_str Agência para a Sociedade do Conhecimento (UMIC) - FCT - Sociedade da Informação
instacron_str RCAAP
institution RCAAP
reponame_str Repositório Científico de Acesso Aberto de Portugal (Repositórios Cientìficos)
collection Repositório Científico de Acesso Aberto de Portugal (Repositórios Cientìficos)
repository.name.fl_str_mv Repositório Científico de Acesso Aberto de Portugal (Repositórios Cientìficos) - Agência para a Sociedade do Conhecimento (UMIC) - FCT - Sociedade da Informação
repository.mail.fl_str_mv mluisa.alvim@gmail.com
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