Abstract
BackgroundThe 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).ResultsWe 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.ConclusionsLatimeria 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.
Highlights
The modern coelacanth (Latimeria) is the extant taxon of a basal sarcopterygian lineage and sister group to tetrapods
Isolation of the Latimeria sonic hedgehog locus Three variants of hedgehog exon 2 [GenBank accession numbers FJ603041, FJ603042 and FJ603043] sequences were obtained by polymerase chain reaction (PCR) from genomic DNA of Latimeria chalumnae using degenerate primers
The shh-specific paralog was deduced from DNA sequence comparisons and used as a probe to screen a Latimeria menadoensis BAC (Bacterial Artificial Chromosome) library [41]
Summary
The modern coelacanth (Latimeria) is the extant taxon of a basal sarcopterygian lineage and sister group to tetrapods. Strong DNA sequence conservation of enhancers of developmental regulator genes [3,4,5,6,7,8] implies purifying selection to keep such regions preserved across species and functionally constrained in their cis-regulatory functions. Its species diversity is considered to have remained low within its long time of existence of at least 360 million years [19], with a certain peak of species abundance in the Triassic and Jurassic eras. Concomitant with this reduced species divergence, its morphology has remained almost unchanged [20]. The orthologous Otx enhancers FM and AM [24] and the HoxC8 early enhancer [25] revealed strong conservation in DNA sequence and in enhancer expression in mouse transgenic experiments
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