Abstract
BackgroundThe evolutionary mechanisms involved in shaping complex gene regulatory networks (GRN) that encode for morphologically similar structures in distantly related animals remain elusive. In this context, echinoderm larval skeletons found in brittle stars and sea urchins provide an ideal system. Here, we characterize for the first time the development of the larval skeleton in the ophiuroid Amphiura filiformis and compare it systematically with its counterpart in sea urchin.ResultsWe show that ophiuroids and euechinoids, that split at least 480 Million years ago (Mya), have remarkable similarities in tempo and mode of skeletal development. Despite morphological and ontological similarities, our high-resolution study of the dynamics of genetic regulatory states in A. filiformis highlights numerous differences in the architecture of their underlying GRNs. Importantly, the A.filiformispplx, the closest gene to the sea urchin double negative gate (DNG) repressor pmar1, fails to drive the skeletogenic program in sea urchin, showing important evolutionary differences in protein function. hesC, the second repressor of the DNG, is co-expressed with most of the genes that are repressed in sea urchin, indicating the absence of direct repression of tbr, ets1/2, and delta in A. filiformis. Furthermore, the absence of expression in later stages of brittle star skeleton development of key regulatory genes, such as foxb and dri, shows significantly different regulatory states.ConclusionOur data fill up an important gap in the picture of larval mesoderm in echinoderms and allows us to explore the evolutionary implications relative to the recently established phylogeny of echinoderm classes. In light of recent studies on other echinoderms, our data highlight a high evolutionary plasticity of the same nodes throughout evolution of echinoderm skeletogenesis. Finally, gene duplication, protein function diversification, and cis-regulatory element evolution all contributed to shape the regulatory program for larval skeletogenesis in different branches of echinoderms.Electronic supplementary materialThe online version of this article (doi:10.1186/s13227-015-0039-x) contains supplementary material, which is available to authorized users.
Highlights
The evolutionary mechanisms involved in shaping complex gene regulatory networks (GRN) that encode for morphologically similar structures in distantly related animals remain elusive
A. filiformis differs from euechinoid sea urchin development in the lack of micromeres at the vegetal pole (Fig. 1a, 6hpf ), and in the early appearance of morphological evidence for animal–vegetal and oral–aboral axes (Fig. 1a, 16hpf and 23hpf )
In both organisms skeletogenesis is preceded by the ingression of mesenchymal cells prior to gastrulation (Fig. 1a, 23 hpf ), and the two bilaterally arranged spicules are formed just underneath the ectoderm within two clusters of mesenchymal cells located at the boundary with the invaginating endoderm as identified by calcein staining (Fig. 1a, 30 hpf )
Summary
The evolutionary mechanisms involved in shaping complex gene regulatory networks (GRN) that encode for morphologically similar structures in distantly related animals remain elusive. In this context, echinoderm larval skeletons found in brittle stars and sea urchins provide an ideal system. Many studies in different organisms have analyzed complex developmental GRNs [1, 3,4,5], little is known about the mechanisms of rewiring during evolution, and most studies, with few exceptions [6,7,8], remain at the level of single nodes. Important evolutionary changes of transcription factors have been reported at the level of functional domains and binding specificity (for review [14, 15])
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