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An arthropod cis-regulatory element functioning in sensory organ precursor development dates back to the Cambrian

BACKGROUND: An increasing number of publications demonstrate conservation of function of cis-regulatory elements without sequence similarity. In invertebrates such functional conservation has only been shown for closely related species. Here we demonstrate the existence of an ancient arthropod regul...

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Autores principales: Ayyar, Savita, Negre, Barbara, Simpson, Pat, Stollewerk, Angelika
Formato: Texto
Lenguaje:English
Publicado: BioMed Central 2010
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC2958161/
https://www.ncbi.nlm.nih.gov/pubmed/20868489
http://dx.doi.org/10.1186/1741-7007-8-127
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author Ayyar, Savita
Negre, Barbara
Simpson, Pat
Stollewerk, Angelika
author_facet Ayyar, Savita
Negre, Barbara
Simpson, Pat
Stollewerk, Angelika
author_sort Ayyar, Savita
collection PubMed
description BACKGROUND: An increasing number of publications demonstrate conservation of function of cis-regulatory elements without sequence similarity. In invertebrates such functional conservation has only been shown for closely related species. Here we demonstrate the existence of an ancient arthropod regulatory element that functions during the selection of neural precursors. The activity of genes of the achaete-scute (ac-sc) family endows cells with neural potential. An essential, conserved characteristic of proneural genes is their ability to restrict their own activity to single or a small number of progenitor cells from their initially broad domains of expression. This is achieved through a process called lateral inhibition. A regulatory element, the sensory organ precursor enhancer (SOPE), is required for this process. First identified in Drosophila, the SOPE contains discrete binding sites for four regulatory factors. The SOPE of the Drosophila asense gene is situated in the 5' UTR. RESULTS: Through a manual comparison of consensus binding site sequences we have been able to identify a SOPE in UTR sequences of asense-like genes in species belonging to all four arthropod groups (Crustacea, Myriapoda, Chelicerata and Insecta). The SOPEs of the spider Cupiennius salei and the insect Tribolium castaneum are shown to be functional in transgenic Drosophila. This would place the origin of this regulatory sequence as far back as the last common ancestor of the Arthropoda, that is, in the Cambrian, 550 million years ago. CONCLUSIONS: The SOPE is not detectable by inter-specific sequence comparison, raising the possibility that other ancient regulatory modules in invertebrates might have escaped detection.
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spelling pubmed-29581612010-10-21 An arthropod cis-regulatory element functioning in sensory organ precursor development dates back to the Cambrian Ayyar, Savita Negre, Barbara Simpson, Pat Stollewerk, Angelika BMC Biol Research Article BACKGROUND: An increasing number of publications demonstrate conservation of function of cis-regulatory elements without sequence similarity. In invertebrates such functional conservation has only been shown for closely related species. Here we demonstrate the existence of an ancient arthropod regulatory element that functions during the selection of neural precursors. The activity of genes of the achaete-scute (ac-sc) family endows cells with neural potential. An essential, conserved characteristic of proneural genes is their ability to restrict their own activity to single or a small number of progenitor cells from their initially broad domains of expression. This is achieved through a process called lateral inhibition. A regulatory element, the sensory organ precursor enhancer (SOPE), is required for this process. First identified in Drosophila, the SOPE contains discrete binding sites for four regulatory factors. The SOPE of the Drosophila asense gene is situated in the 5' UTR. RESULTS: Through a manual comparison of consensus binding site sequences we have been able to identify a SOPE in UTR sequences of asense-like genes in species belonging to all four arthropod groups (Crustacea, Myriapoda, Chelicerata and Insecta). The SOPEs of the spider Cupiennius salei and the insect Tribolium castaneum are shown to be functional in transgenic Drosophila. This would place the origin of this regulatory sequence as far back as the last common ancestor of the Arthropoda, that is, in the Cambrian, 550 million years ago. CONCLUSIONS: The SOPE is not detectable by inter-specific sequence comparison, raising the possibility that other ancient regulatory modules in invertebrates might have escaped detection. BioMed Central 2010-09-24 /pmc/articles/PMC2958161/ /pubmed/20868489 http://dx.doi.org/10.1186/1741-7007-8-127 Text en Copyright ©2010 Ayyar et al; licensee BioMed Central Ltd. http://creativecommons.org/licenses/by/2.0 This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
spellingShingle Research Article
Ayyar, Savita
Negre, Barbara
Simpson, Pat
Stollewerk, Angelika
An arthropod cis-regulatory element functioning in sensory organ precursor development dates back to the Cambrian
title An arthropod cis-regulatory element functioning in sensory organ precursor development dates back to the Cambrian
title_full An arthropod cis-regulatory element functioning in sensory organ precursor development dates back to the Cambrian
title_fullStr An arthropod cis-regulatory element functioning in sensory organ precursor development dates back to the Cambrian
title_full_unstemmed An arthropod cis-regulatory element functioning in sensory organ precursor development dates back to the Cambrian
title_short An arthropod cis-regulatory element functioning in sensory organ precursor development dates back to the Cambrian
title_sort arthropod cis-regulatory element functioning in sensory organ precursor development dates back to the cambrian
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC2958161/
https://www.ncbi.nlm.nih.gov/pubmed/20868489
http://dx.doi.org/10.1186/1741-7007-8-127
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