Abstract
BackgroundHox 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.ResultsHere, 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.ConclusionsThe 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 vertebratesElectronic supplementary materialThe online version of this article (doi:10.1186/2041-9139-5-44) contains supplementary material, which is available to authorized users.
Highlights
Hox genes are master regulatory genes that specify positional identities during axial development in animals
By investigating a broader range of developmental stages and novel structures in a variety of lineages, we demonstrate that Hox genes are expressed in an anterior domain that is a derivative of pharyngeal arch I, which has not been previously documented in any taxon
We demonstrate that the Hox distal phase’ (DP) expression pattern is a feature of the posterior HoxA genes, indicating that the DP pattern of Hox expression is not restricted to appendages or the HoxD genes, nor is it associated with any particular novelty
Summary
Hox genes are master regulatory genes that specify positional identities during axial development in animals. Developmental regulatory genes that occur in all bilaterians They are arranged in clusters and play a key role in animal development by specifying positional identities through nested and overlapping expression domains. This pattern of collinear Hox expression is sometimes called the ‘general Hox strategy,’ in part, because an alternative, inverted expression pattern has been observed with the 5′ (posterior) HoxD genes in distal regions of vertebrate fins and limbs The latter is associated with a switch in cis-regulatory regions [4] from the telomeric side of the cluster (3′) to the centromeric side (5′) [5,6], and is manifest as a broader expression domain of the (5′) gene relative to its 3′ neighbor on the cluster. Both proximal and distal expression patterns meet the definition of collinearity, but are differentiated with respect to their regulatory regions and the relative expression patterns of the genes in closest proximity to the active regulatory region
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