Comprehensive Analysis of a cis-Regulatory Region Reveals Pleiotropy in Enhancer Function

Autores
Preger Ben Noon, Ella; Sabarís Di Lorenzo, Gonzalo Julián; Ortiz, Daniela M.; Sager, Jonathan; Liebowitz, Anna; Stern, David L.; Frankel, Nicolás
Año de publicación
2018
Idioma
inglés
Tipo de recurso
artículo
Estado
versión publicada
Descripción
Developmental genes can have complex cis-regulatory regions with multiple enhancers. Early work revealed remarkable modularity of enhancers, whereby distinct DNA regions drive gene expression in defined spatiotemporal domains. Nevertheless, a few reports have shown that enhancers function in multiple developmental stages, implying that enhancers can be pleiotropic. Here, we have studied the activity of the enhancers of the shavenbaby gene throughout D. melanogaster development. We found that all seven shavenbaby enhancers drive expression in multiple tissues and developmental stages. We explored how enhancer pleiotropy is encoded in two of these enhancers. In one enhancer, the same transcription factor binding sites contribute to embryonic and pupal expression, revealing site pleiotropy, whereas for a second enhancer, these roles are encoded by distinct sites. Enhancer pleiotropy may be a common feature of cis-regulatory regions of developmental genes, and site pleiotropy may constrain enhancer evolution in some cases. Preger-Ben Noon et al. find that shavenbaby gene enhancers contain regulatory information for driving several expression patterns (i.e., enhancers are pleiotropic) and that, in some cases, the transcription factor binding sites that activate these enhancers are reused during development.
Fil: Preger Ben Noon, Ella. Howard Hughes Medical Institute; Estados Unidos
Fil: Sabarís Di Lorenzo, Gonzalo Julián. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Ciudad Universitaria. Instituto de Ecología, Genética y Evolución de Buenos Aires. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales. Instituto de Ecología, Genética y Evolución de Buenos Aires; Argentina
Fil: Ortiz, Daniela M.. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Ciudad Universitaria. Instituto de Ecología, Genética y Evolución de Buenos Aires. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales. Instituto de Ecología, Genética y Evolución de Buenos Aires; Argentina
Fil: Sager, Jonathan. Howard Hughes Medical Institute; Estados Unidos
Fil: Liebowitz, Anna. University of Princeton; Estados Unidos
Fil: Stern, David L.. Howard Hughes Medical Institute; Estados Unidos
Fil: Frankel, Nicolás. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Ciudad Universitaria. Instituto de Ecología, Genética y Evolución de Buenos Aires. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales. Instituto de Ecología, Genética y Evolución de Buenos Aires; Argentina
Materia
DROSOPHILA
ENHANCER
GENE REGULATION
PLEITROPY
SHAVENBABY
Nivel de accesibilidad
acceso abierto
Condiciones de uso
https://creativecommons.org/licenses/by-nc-nd/2.5/ar/
Repositorio
CONICET Digital (CONICET)
Institución
Consejo Nacional de Investigaciones Científicas y Técnicas
OAI Identificador
oai:ri.conicet.gov.ar:11336/96571
Acceder
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oai_identifier_str oai:ri.conicet.gov.ar:11336/96571
network_acronym_str CONICETDig
repository_id_str 3498
network_name_str CONICET Digital (CONICET)
spelling Comprehensive Analysis of a cis-Regulatory Region Reveals Pleiotropy in Enhancer FunctionPreger Ben Noon, EllaSabarís Di Lorenzo, Gonzalo JuliánOrtiz, Daniela M.Sager, JonathanLiebowitz, AnnaStern, David L.Frankel, NicolásDROSOPHILAENHANCERGENE REGULATIONPLEITROPYSHAVENBABYhttps://purl.org/becyt/ford/1.6https://purl.org/becyt/ford/1Developmental genes can have complex cis-regulatory regions with multiple enhancers. Early work revealed remarkable modularity of enhancers, whereby distinct DNA regions drive gene expression in defined spatiotemporal domains. Nevertheless, a few reports have shown that enhancers function in multiple developmental stages, implying that enhancers can be pleiotropic. Here, we have studied the activity of the enhancers of the shavenbaby gene throughout D. melanogaster development. We found that all seven shavenbaby enhancers drive expression in multiple tissues and developmental stages. We explored how enhancer pleiotropy is encoded in two of these enhancers. In one enhancer, the same transcription factor binding sites contribute to embryonic and pupal expression, revealing site pleiotropy, whereas for a second enhancer, these roles are encoded by distinct sites. Enhancer pleiotropy may be a common feature of cis-regulatory regions of developmental genes, and site pleiotropy may constrain enhancer evolution in some cases. Preger-Ben Noon et al. find that shavenbaby gene enhancers contain regulatory information for driving several expression patterns (i.e., enhancers are pleiotropic) and that, in some cases, the transcription factor binding sites that activate these enhancers are reused during development.Fil: Preger Ben Noon, Ella. Howard Hughes Medical Institute; Estados UnidosFil: Sabarís Di Lorenzo, Gonzalo Julián. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Ciudad Universitaria. Instituto de Ecología, Genética y Evolución de Buenos Aires. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales. Instituto de Ecología, Genética y Evolución de Buenos Aires; ArgentinaFil: Ortiz, Daniela M.. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Ciudad Universitaria. Instituto de Ecología, Genética y Evolución de Buenos Aires. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales. Instituto de Ecología, Genética y Evolución de Buenos Aires; ArgentinaFil: Sager, Jonathan. Howard Hughes Medical Institute; Estados UnidosFil: Liebowitz, Anna. University of Princeton; Estados UnidosFil: Stern, David L.. Howard Hughes Medical Institute; Estados UnidosFil: Frankel, Nicolás. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Ciudad Universitaria. Instituto de Ecología, Genética y Evolución de Buenos Aires. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales. Instituto de Ecología, Genética y Evolución de Buenos Aires; ArgentinaElsevier2018-03info:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersionhttp://purl.org/coar/resource_type/c_6501info:ar-repo/semantics/articuloapplication/pdfapplication/pdfapplication/pdfhttp://hdl.handle.net/11336/96571Preger Ben Noon, Ella; Sabarís Di Lorenzo, Gonzalo Julián; Ortiz, Daniela M.; Sager, Jonathan; Liebowitz, Anna; et al.; Comprehensive Analysis of a cis-Regulatory Region Reveals Pleiotropy in Enhancer Function; Elsevier; Cell Reports; 22; 11; 3-2018; 3021-30312211-1247CONICET DigitalCONICETenginfo:eu-repo/semantics/altIdentifier/url/https://www.sciencedirect.com/science/article/pii/S2211124718302687info:eu-repo/semantics/altIdentifier/doi/10.1016/j.celrep.2018.02.073info:eu-repo/semantics/openAccesshttps://creativecommons.org/licenses/by-nc-nd/2.5/ar/reponame:CONICET Digital (CONICET)instname:Consejo Nacional de Investigaciones Científicas y Técnicas2025-09-29T10:47:38Zoai:ri.conicet.gov.ar:11336/96571instacron: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 10:47:38.924CONICET Digital (CONICET) - Consejo Nacional de Investigaciones Científicas y Técnicasfalse
dc.title.none.fl_str_mv Comprehensive Analysis of a cis-Regulatory Region Reveals Pleiotropy in Enhancer Function
title Comprehensive Analysis of a cis-Regulatory Region Reveals Pleiotropy in Enhancer Function
spellingShingle Comprehensive Analysis of a cis-Regulatory Region Reveals Pleiotropy in Enhancer Function
Preger Ben Noon, Ella
DROSOPHILA
ENHANCER
GENE REGULATION
PLEITROPY
SHAVENBABY
title_short Comprehensive Analysis of a cis-Regulatory Region Reveals Pleiotropy in Enhancer Function
title_full Comprehensive Analysis of a cis-Regulatory Region Reveals Pleiotropy in Enhancer Function
title_fullStr Comprehensive Analysis of a cis-Regulatory Region Reveals Pleiotropy in Enhancer Function
title_full_unstemmed Comprehensive Analysis of a cis-Regulatory Region Reveals Pleiotropy in Enhancer Function
title_sort Comprehensive Analysis of a cis-Regulatory Region Reveals Pleiotropy in Enhancer Function
dc.creator.none.fl_str_mv Preger Ben Noon, Ella
Sabarís Di Lorenzo, Gonzalo Julián
Ortiz, Daniela M.
Sager, Jonathan
Liebowitz, Anna
Stern, David L.
Frankel, Nicolás
author Preger Ben Noon, Ella
author_facet Preger Ben Noon, Ella
Sabarís Di Lorenzo, Gonzalo Julián
Ortiz, Daniela M.
Sager, Jonathan
Liebowitz, Anna
Stern, David L.
Frankel, Nicolás
author_role author
author2 Sabarís Di Lorenzo, Gonzalo Julián
Ortiz, Daniela M.
Sager, Jonathan
Liebowitz, Anna
Stern, David L.
Frankel, Nicolás
author2_role author
author
author
author
author
author
dc.subject.none.fl_str_mv DROSOPHILA
ENHANCER
GENE REGULATION
PLEITROPY
SHAVENBABY
topic DROSOPHILA
ENHANCER
GENE REGULATION
PLEITROPY
SHAVENBABY
purl_subject.fl_str_mv https://purl.org/becyt/ford/1.6
https://purl.org/becyt/ford/1
dc.description.none.fl_txt_mv Developmental genes can have complex cis-regulatory regions with multiple enhancers. Early work revealed remarkable modularity of enhancers, whereby distinct DNA regions drive gene expression in defined spatiotemporal domains. Nevertheless, a few reports have shown that enhancers function in multiple developmental stages, implying that enhancers can be pleiotropic. Here, we have studied the activity of the enhancers of the shavenbaby gene throughout D. melanogaster development. We found that all seven shavenbaby enhancers drive expression in multiple tissues and developmental stages. We explored how enhancer pleiotropy is encoded in two of these enhancers. In one enhancer, the same transcription factor binding sites contribute to embryonic and pupal expression, revealing site pleiotropy, whereas for a second enhancer, these roles are encoded by distinct sites. Enhancer pleiotropy may be a common feature of cis-regulatory regions of developmental genes, and site pleiotropy may constrain enhancer evolution in some cases. Preger-Ben Noon et al. find that shavenbaby gene enhancers contain regulatory information for driving several expression patterns (i.e., enhancers are pleiotropic) and that, in some cases, the transcription factor binding sites that activate these enhancers are reused during development.
Fil: Preger Ben Noon, Ella. Howard Hughes Medical Institute; Estados Unidos
Fil: Sabarís Di Lorenzo, Gonzalo Julián. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Ciudad Universitaria. Instituto de Ecología, Genética y Evolución de Buenos Aires. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales. Instituto de Ecología, Genética y Evolución de Buenos Aires; Argentina
Fil: Ortiz, Daniela M.. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Ciudad Universitaria. Instituto de Ecología, Genética y Evolución de Buenos Aires. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales. Instituto de Ecología, Genética y Evolución de Buenos Aires; Argentina
Fil: Sager, Jonathan. Howard Hughes Medical Institute; Estados Unidos
Fil: Liebowitz, Anna. University of Princeton; Estados Unidos
Fil: Stern, David L.. Howard Hughes Medical Institute; Estados Unidos
Fil: Frankel, Nicolás. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Ciudad Universitaria. Instituto de Ecología, Genética y Evolución de Buenos Aires. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales. Instituto de Ecología, Genética y Evolución de Buenos Aires; Argentina
description Developmental genes can have complex cis-regulatory regions with multiple enhancers. Early work revealed remarkable modularity of enhancers, whereby distinct DNA regions drive gene expression in defined spatiotemporal domains. Nevertheless, a few reports have shown that enhancers function in multiple developmental stages, implying that enhancers can be pleiotropic. Here, we have studied the activity of the enhancers of the shavenbaby gene throughout D. melanogaster development. We found that all seven shavenbaby enhancers drive expression in multiple tissues and developmental stages. We explored how enhancer pleiotropy is encoded in two of these enhancers. In one enhancer, the same transcription factor binding sites contribute to embryonic and pupal expression, revealing site pleiotropy, whereas for a second enhancer, these roles are encoded by distinct sites. Enhancer pleiotropy may be a common feature of cis-regulatory regions of developmental genes, and site pleiotropy may constrain enhancer evolution in some cases. Preger-Ben Noon et al. find that shavenbaby gene enhancers contain regulatory information for driving several expression patterns (i.e., enhancers are pleiotropic) and that, in some cases, the transcription factor binding sites that activate these enhancers are reused during development.
publishDate 2018
dc.date.none.fl_str_mv 2018-03
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/11336/96571
Preger Ben Noon, Ella; Sabarís Di Lorenzo, Gonzalo Julián; Ortiz, Daniela M.; Sager, Jonathan; Liebowitz, Anna; et al.; Comprehensive Analysis of a cis-Regulatory Region Reveals Pleiotropy in Enhancer Function; Elsevier; Cell Reports; 22; 11; 3-2018; 3021-3031
2211-1247
CONICET Digital
CONICET
url http://hdl.handle.net/11336/96571
identifier_str_mv Preger Ben Noon, Ella; Sabarís Di Lorenzo, Gonzalo Julián; Ortiz, Daniela M.; Sager, Jonathan; Liebowitz, Anna; et al.; Comprehensive Analysis of a cis-Regulatory Region Reveals Pleiotropy in Enhancer Function; Elsevier; Cell Reports; 22; 11; 3-2018; 3021-3031
2211-1247
CONICET Digital
CONICET
dc.language.none.fl_str_mv eng
language eng
dc.relation.none.fl_str_mv info:eu-repo/semantics/altIdentifier/url/https://www.sciencedirect.com/science/article/pii/S2211124718302687
info:eu-repo/semantics/altIdentifier/doi/10.1016/j.celrep.2018.02.073
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
application/pdf
dc.publisher.none.fl_str_mv Elsevier
publisher.none.fl_str_mv Elsevier
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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score 13.070432

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