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HoxA and HoxD expression in a variety of vertebrate body plan features reveals an ancient origin for the distal Hox program

BACKGROUND: Hox genes are master regulatory genes that specify positional identities during axial development in animals. Discoveries regarding their concerted expression patterns have commanded intense interest due to their complex regulation and specification of body plan features in jawed vertebr...

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Autores principales: Archambeault, Sophie, Taylor, Julia Ann, Crow, Karen D
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2014
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4407844/
https://www.ncbi.nlm.nih.gov/pubmed/25908959
http://dx.doi.org/10.1186/2041-9139-5-44
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author Archambeault, Sophie
Taylor, Julia Ann
Crow, Karen D
author_facet Archambeault, Sophie
Taylor, Julia Ann
Crow, Karen D
author_sort Archambeault, Sophie
collection PubMed
description BACKGROUND: Hox genes are master regulatory genes that specify positional identities during axial development in animals. Discoveries regarding their concerted expression patterns have commanded intense interest due to their complex regulation and specification of body plan features in jawed vertebrates. For example, the posterior HoxD genes switch to an inverted collinear expression pattern in the mouse autopod where HoxD13 switches from a more restricted to a less restricted domain relative to its neighboring gene on the cluster. We refer to this program as the ‘distal phase’ (DP) expression pattern because it occurs in distal regions of paired fins and limbs, and is regulated independently by elements in the 5′ region upstream of the HoxD cluster. However, few taxa have been evaluated with respect to this pattern, and most studies have focused on pectoral fin morphogenesis, which occurs relatively early in development. RESULTS: Here, we demonstrate for the first time that the DP expression pattern occurs with the posterior HoxA genes, and is therefore not solely associated with the HoxD gene cluster. Further, DP Hox expression is not confined to paired fins and limbs, but occurs in a variety of body plan features, including paddlefish barbels - sensory adornments that develop from the first mandibular arch (the former ‘Hox-free zone), and the vent (a medial structure that is analogous to a urethra). We found DP expression of HoxD13 and HoxD12 in the paddlefish barbel; and we present the first evidence for DP expression of the HoxA genes in the hindgut and vent of three ray-finned fishes. The HoxA DP expression pattern is predicted by the recent finding of a shared 5′ regulatory architecture in both the HoxA and HoxD clusters, but has not been previously observed in any body plan feature. CONCLUSIONS: The Hox DP expression pattern appears to be an ancient module that has been co-opted in a variety of structures adorning the vertebrate bauplan. This module provides a shared genetic program that implies deep homology of a variety of distally elongated structures that has played a significant role in the evolution of morphological diversity in vertebrates ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/2041-9139-5-44) contains supplementary material, which is available to authorized users.
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spelling pubmed-44078442015-04-24 HoxA and HoxD expression in a variety of vertebrate body plan features reveals an ancient origin for the distal Hox program Archambeault, Sophie Taylor, Julia Ann Crow, Karen D EvoDevo Research BACKGROUND: Hox genes are master regulatory genes that specify positional identities during axial development in animals. Discoveries regarding their concerted expression patterns have commanded intense interest due to their complex regulation and specification of body plan features in jawed vertebrates. For example, the posterior HoxD genes switch to an inverted collinear expression pattern in the mouse autopod where HoxD13 switches from a more restricted to a less restricted domain relative to its neighboring gene on the cluster. We refer to this program as the ‘distal phase’ (DP) expression pattern because it occurs in distal regions of paired fins and limbs, and is regulated independently by elements in the 5′ region upstream of the HoxD cluster. However, few taxa have been evaluated with respect to this pattern, and most studies have focused on pectoral fin morphogenesis, which occurs relatively early in development. RESULTS: Here, we demonstrate for the first time that the DP expression pattern occurs with the posterior HoxA genes, and is therefore not solely associated with the HoxD gene cluster. Further, DP Hox expression is not confined to paired fins and limbs, but occurs in a variety of body plan features, including paddlefish barbels - sensory adornments that develop from the first mandibular arch (the former ‘Hox-free zone), and the vent (a medial structure that is analogous to a urethra). We found DP expression of HoxD13 and HoxD12 in the paddlefish barbel; and we present the first evidence for DP expression of the HoxA genes in the hindgut and vent of three ray-finned fishes. The HoxA DP expression pattern is predicted by the recent finding of a shared 5′ regulatory architecture in both the HoxA and HoxD clusters, but has not been previously observed in any body plan feature. CONCLUSIONS: The Hox DP expression pattern appears to be an ancient module that has been co-opted in a variety of structures adorning the vertebrate bauplan. This module provides a shared genetic program that implies deep homology of a variety of distally elongated structures that has played a significant role in the evolution of morphological diversity in vertebrates ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/2041-9139-5-44) contains supplementary material, which is available to authorized users. BioMed Central 2014-11-19 /pmc/articles/PMC4407844/ /pubmed/25908959 http://dx.doi.org/10.1186/2041-9139-5-44 Text en © Archambeault et al.; licensee BioMed Central Ltd. 2014 This article is published under license to BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research
Archambeault, Sophie
Taylor, Julia Ann
Crow, Karen D
HoxA and HoxD expression in a variety of vertebrate body plan features reveals an ancient origin for the distal Hox program
title HoxA and HoxD expression in a variety of vertebrate body plan features reveals an ancient origin for the distal Hox program
title_full HoxA and HoxD expression in a variety of vertebrate body plan features reveals an ancient origin for the distal Hox program
title_fullStr HoxA and HoxD expression in a variety of vertebrate body plan features reveals an ancient origin for the distal Hox program
title_full_unstemmed HoxA and HoxD expression in a variety of vertebrate body plan features reveals an ancient origin for the distal Hox program
title_short HoxA and HoxD expression in a variety of vertebrate body plan features reveals an ancient origin for the distal Hox program
title_sort hoxa and hoxd expression in a variety of vertebrate body plan features reveals an ancient origin for the distal hox program
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4407844/
https://www.ncbi.nlm.nih.gov/pubmed/25908959
http://dx.doi.org/10.1186/2041-9139-5-44
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