Open Access Research

Conservation of shh cis-regulatory architecture of the coelacanth is consistent with its ancestral phylogenetic position

Michael Lang16, Yavor Hadzhiev2, Nicol Siegel17, Chris T Amemiya5, Carolina Parada48, Uwe Strähle3, May-Britt Becker19, Ferenc Müller23* and Axel Meyer1*

Author Affiliations

1 Department of Biology, University of Konstanz, 78457 Konstanz, Germany

2 Department of Medical and Molecular Genetics, University of Birmingham, Birmingham B15 2TT, UK

3 Karlsruhe Institute of Technology, Institute for Toxicology and Genetics, 76021 Karlsruhe, Germany

4 Developmental Biology Group, Universitat Pompeu Fabra, Parc de Recerca Biomèdica de Barcelona, 08003 Barcelona, Spain

5 Benaroya Research Institute at Virginia Mason, Seattle, WA 98101, USA

6 Development and Neurobiology Program, Jacques Monod Institute, 75013 Paris, France

7 Medical University of Vienna, Medical Genetics, 1090 Vienna, Austria

8 Center for Craniofacial Molecular Biology, University of Southern California, Los Angeles, CA 90030, USA

9 Exzellenzcluster CellNetworks, INF 267, 69120 Heidelberg, Germany

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EvoDevo 2010, 1:11  doi:10.1186/2041-9139-1-11

Published: 3 November 2010

Abstract

Background

The modern coelacanth (Latimeria) is the extant taxon of a basal sarcopterygian lineage and sister group to tetrapods. Apart from certain apomorphic traits, its morphology is characterized by a high degree of retention of ancestral vertebrate structures and little morphological change. An insight into the molecular evolution that may explain the unchanged character of Latimeria morphology requires the analysis of the expression patterns of developmental regulator genes and their cis-regulatory modules (CRMs).

Results

We describe the comparative and functional analysis of the sonic hedgehog (shh) genomic region of Latimeria menadoensis. Several putative enhancers in the Latimeria shh locus have been identified by comparisons to sarcopterygian and actinopterygian extant species. Specific sequence conservation with all known actinopterygian enhancer elements has been detected. However, these elements are selectively missing in more recently diverged actinopterygian and sarcopterygian species. The functionality of the putative Latimeria enhancers was confirmed by reporter gene expression analysis in transient transgenic zebrafish and chick embryos.

Conclusions

Latimeria shh CRMs represent the ancestral set of enhancers that have emerged before the split of lobe-finned and ray-finned fishes. In contrast to lineage-specific losses and differentiations in more derived lineages, Latimeria shh enhancers reveal low levels of sequence diversification. High overall sequence conservation of shh conserved noncoding elements (CNE) is consistent with the general trend of high levels of conservation of noncoding DNA in the slowly evolving Latimeria genome.