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

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 multipl...

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Autores principales: Preger-Ben Noon, E., Sabarís, G., Ortiz, D.M., Sager, J., Liebowitz, A., Stern, D.L., Frankel, N.
Formato: JOUR
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Acceso en línea:http://hdl.handle.net/20.500.12110/paper_22111247_v22_n11_p3021_PregerBenNoon
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spelling todo:paper_22111247_v22_n11_p3021_PregerBenNoon2023-10-03T16:40:30Z Comprehensive Analysis of a cis-Regulatory Region Reveals Pleiotropy in Enhancer Function Preger-Ben Noon, E. Sabarís, G. Ortiz, D.M. Sager, J. Liebowitz, A. Stern, D.L. Frankel, N. Drosophila enhancer gene regulation pleitropy shavenbaby transcription factor adult animal experiment animal tissue Article binding site controlled study developmental gene developmental stage Drosophila melanogaster embryo enhancer region female gene gene activity gene expression gene function genetic code genetic regulation insect development male nonhuman pleiotropy priority journal svb gene 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. © 2018 The Author(s) JOUR info:eu-repo/semantics/openAccess http://creativecommons.org/licenses/by/2.5/ar http://hdl.handle.net/20.500.12110/paper_22111247_v22_n11_p3021_PregerBenNoon
institution Universidad de Buenos Aires
institution_str I-28
repository_str R-134
collection Biblioteca Digital - Facultad de Ciencias Exactas y Naturales (UBA)
topic Drosophila
enhancer
gene regulation
pleitropy
shavenbaby
transcription factor
adult
animal experiment
animal tissue
Article
binding site
controlled study
developmental gene
developmental stage
Drosophila melanogaster
embryo
enhancer region
female
gene
gene activity
gene expression
gene function
genetic code
genetic regulation
insect development
male
nonhuman
pleiotropy
priority journal
svb gene
spellingShingle Drosophila
enhancer
gene regulation
pleitropy
shavenbaby
transcription factor
adult
animal experiment
animal tissue
Article
binding site
controlled study
developmental gene
developmental stage
Drosophila melanogaster
embryo
enhancer region
female
gene
gene activity
gene expression
gene function
genetic code
genetic regulation
insect development
male
nonhuman
pleiotropy
priority journal
svb gene
Preger-Ben Noon, E.
Sabarís, G.
Ortiz, D.M.
Sager, J.
Liebowitz, A.
Stern, D.L.
Frankel, N.
Comprehensive Analysis of a cis-Regulatory Region Reveals Pleiotropy in Enhancer Function
topic_facet Drosophila
enhancer
gene regulation
pleitropy
shavenbaby
transcription factor
adult
animal experiment
animal tissue
Article
binding site
controlled study
developmental gene
developmental stage
Drosophila melanogaster
embryo
enhancer region
female
gene
gene activity
gene expression
gene function
genetic code
genetic regulation
insect development
male
nonhuman
pleiotropy
priority journal
svb gene
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. © 2018 The Author(s)
format JOUR
author Preger-Ben Noon, E.
Sabarís, G.
Ortiz, D.M.
Sager, J.
Liebowitz, A.
Stern, D.L.
Frankel, N.
author_facet Preger-Ben Noon, E.
Sabarís, G.
Ortiz, D.M.
Sager, J.
Liebowitz, A.
Stern, D.L.
Frankel, N.
author_sort Preger-Ben Noon, E.
title Comprehensive Analysis of a cis-Regulatory Region Reveals Pleiotropy in Enhancer Function
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
url http://hdl.handle.net/20.500.12110/paper_22111247_v22_n11_p3021_PregerBenNoon
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