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Appendage expression driven by the Hoxd Global Control Region is an ancient gnathostome feature.

ABSTRACT: The evolutionary transition of the fins of fish into tetrapod limbs involved genetic changes to developmental systems that resulted in novel skeletal patterns and functions. Approaches to understanding this issue have entailed the search for antecedents of limb structure in fossils, genes, and embryos. Comparative genetic analyses have produced ambiguous results: although studies of posterior Hox genes from homology group 13 (Hoxa-13 and Hoxd-13) reveal similarities in gene expression between the distal segments of fins and limbs, this functional homology has not been supported by genomic comparisons of the activity of their cis-regulatory elements, namely the Hoxd Global Control Region. Here, we show that cis-regulatory elements driving Hoxd gene expression in distal limbs are present in fish. Using an interspecies transgenesis approach, we find functional conservation between gnathostome Hoxd enhancers, demonstrating that orthologous sequences from tetrapods, zebrafish and skate can drive reporter gene expression in mouse limbs and zebrafish fins. Our results support the notion that some of the novelties associated with tetrapod limbs arose by modification of deeply conserved cis- and trans-acting mechanisms of Hox regulation in gnathostomes.

SUBMITTER: Schneider I

PROVIDER: S-EPMC3150877 | biostudies-literature | 2011 Aug

REPOSITORIES: biostudies-literature

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Appendage expression driven by the Hoxd Global Control Region is an ancient gnathostome feature.

Schneider Igor I Aneas Ivy I Gehrke Andrew R AR Dahn Randall D RD Nobrega Marcelo A MA Shubin Neil H NH

Proceedings of the National Academy of Sciences of the United States of America 20110715 31

The evolutionary transition of the fins of fish into tetrapod limbs involved genetic changes to developmental systems that resulted in novel skeletal patterns and functions. Approaches to understanding this issue have entailed the search for antecedents of limb structure in fossils, genes, and embryos. Comparative genetic analyses have produced ambiguous results: although studies of posterior Hox genes from homology group 13 (Hoxa-13 and Hoxd-13) reveal similarities in gene expression between th ...[more]

PMID: 21765002

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Project description: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 vertebrates.

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Appendage expression driven by the Hoxd Global Control Region is an ancient gnathostome feature.

Publications

Appendage expression driven by the Hoxd Global Control Region is an ancient gnathostome feature.

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