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PLoS Genet December 23, 2010; 6 (12): e1001259.
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Ancestral regulatory circuits governing ectoderm patterning downstream of Nodal and BMP2/4 revealed by gene regulatory network analysis in an echinoderm.

Saudemont A , Haillot E , Mekpoh F , Bessodes N , Quirin M , Lapraz F , Duboc V , Röttinger E , Range R , Oisel A , Besnardeau L , Wincker P , Lepage T .

Echinoderms, which are phylogenetically related to vertebrates and produce large numbers of transparent embryos that can be experimentally manipulated, offer many advantages for the analysis of the gene regulatory networks (GRN) regulating germ layer formation. During development of the sea urchin embryo, the ectoderm is the source of signals that pattern all three germ layers along the dorsal-ventral axis. How this signaling center controls patterning and morphogenesis of the embryo is not understood. Here, we report a large-scale analysis of the GRN deployed in response to the activity of this signaling center in the embryos of the Mediterranean sea urchin Paracentrotus lividus, in which studies with high spatial resolution are possible. By using a combination of in situ hybridization screening, overexpression of mRNA, recombinant ligand treatments, and morpholino-based loss-of-function studies, we identified a cohort of transcription factors and signaling molecules expressed in the ventral ectoderm, dorsal ectoderm, and interposed neurogenic ("ciliary band") region in response to the known key signaling molecules Nodal and BMP2/4 and defined the epistatic relationships between the most important genes. The resultant GRN showed a number of striking features. First, Nodal was found to be essential for the expression of all ventral and dorsal marker genes, and BMP2/4 for all dorsal genes. Second, goosecoid was identified as a central player in a regulatory sub-circuit controlling mouth formation, while tbx2/3 emerged as a critical factor for differentiation of the dorsal ectoderm. Finally, and unexpectedly, a neurogenic ectoderm regulatory circuit characterized by expression of "ciliary band" genes was triggered in the absence of TGF beta signaling. We propose a novel model for ectoderm regionalization, in which neural ectoderm is the default fate in the absence of TGF beta signaling, and suggest that the stomodeal and neural subcircuits that we uncovered may represent ancient regulatory pathways controlling embryonic patterning.

PubMed ID: 21203442
PMC ID: PMC3009687
Article link: PLoS Genet

Species referenced: Echinodermata
Genes referenced: arid3a bmp2 bmpr1b chrd CyIIIa dlxl fgfr3 foxa1 foxe3l foxg1 gsk3a hnf6 hoxal irak1bp1 irx4 lefty1 LOC100887844 LOC100893907 LOC105438994 LOC115921237 LOC115925415 LOC574897 LOC575170 LOC578814 LOC581325 LOC583082 msx1 Nk1 nkx1 nkx2-2 nodall onecut2 otx2 pax2 pax2l pole sox2 tbx2 univin wnt8a zfhx4
Morpholinos: LOC583063 MO1 LOC583063 MO2 LOC593908 MO1 arid3a MO4 arid3a MO5 bmp2 MO3 bmp2 MO5 bmpr1b MO1 chrd MO3 chrd MO4 dlxl MO2 dlxl MO3 fgf MO2 fgf MO3 foxa1 MO3 foxa1 MO4 foxg1 MO3 foxg1 MO4 gscl MO3 gscl MO4 hoxal MO1 hoxal MO3 irx4 MO1 irx4 MO3 lefty1 MO2 lefty1 MO5 msx1 MO3 msx1 MO4 nkx1 MO2 nkx1 MO3 nkx2-2 MO2 nkx2-2 MO3 nodall MO8 nodall MO9 onecut2 MO4 onecut2 MO5 sox2 MO3 sox2 MO4 tbx2 MO2 tbx2 MO3 tbxt MO3 tbxt MO4 univin MO1 univin MO2 wnt8a MO5 wnt8a MO6

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References [+] :
Affolter, Nuclear interpretation of Dpp signaling in Drosophila. 2001, Pubmed