Deployment of regulatory genes during gastrulation and germ layer specification in a model spiralian mollusc Crepidula

Background: During gastrulation, endoderm and mesoderm are specified from a bipotential precursor (endomesoderm) that is argued to be homologous across bilaterians. Spiralians also generate mesoderm from ectodermal precursors (ectomesoderm), which arises near the blastopore. While a conserved gene r...

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Published in:Developmental dynamics 2015-10, Vol.244 (10), p.1215-1248
Main Authors: Perry, Kimberly J., Lyons, Deirdre C., Truchado‐Garcia, Marta, Fischer, Antje H. L., Helfrich, Lily W., Johansson, Kimberly B., Diamond, Julie C., Grande, Cristina, Henry, Jonathan Q.
Format: Article
Language:English
Subjects:
Animals
anus
Bilateria
blastopore
Crepidula
EMT
endoderm
foregut
Gastrulation
Gene Expression
Genes, Regulator
Germ Layers - metabolism
hindgut
mesoderm
Mollusca
mouth
Organogenesis
Snails - embryology
Snails - genetics
Snails - metabolism
Spiralia
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Summary:Background: During gastrulation, endoderm and mesoderm are specified from a bipotential precursor (endomesoderm) that is argued to be homologous across bilaterians. Spiralians also generate mesoderm from ectodermal precursors (ectomesoderm), which arises near the blastopore. While a conserved gene regulatory network controls specification of endomesoderm in deuterostomes and ecdysozoans, little is known about genes controlling specification or behavior of either source of spiralian mesoderm or the digestive tract. Results: Using the mollusc Crepidula, we examined conserved regulatory factors and compared their expression to fate maps to score expression in the germ layers, blastopore lip, and digestive tract. Many genes were expressed in both ecto‐ and endomesoderm, but only five were expressed in ectomesoderm exclusively. The latter may contribute to epithelial‐to‐mesenchymal transition seen in ectomesoderm. Conclusions: We present the first comparison of genes expressed during spiralian gastrulation in the context of high‐resolution fate maps. We found variation of genes expressed in the blastopore lip, mouth, and cells that will form the anus. Shared expression of many genes in both mesodermal sources suggests that components of the conserved endomesoderm program were either co‐opted for ectomesoderm formation or that ecto‐ and endomesoderm are derived from a common mesodermal precursor that became subdivided into distinct domains during evolution. Developmental Dynamics 244:1215–1248, 2015. © 2015 Wiley Periodicals, Inc. Key Findings This study represents the first broad analysis of regulatory factors during gastrulation and gut development in a representative of the Spiralia, which we relate to well‐established cell‐lineage fate maps. Many regulatory genes are involved in germ layer specification and gut development, and are expressed in cells of the blastopore lip during gastrulation. We found shared expression of many regulatory genes, suggesting that the conserved endomesodermal GRN may have been co‐opted during the evolution of ectomesoderm. Differences in gene expression between ecto‐ and endomesoderm may be related to morphogenetic events such as EMT, which takes place in ectomesoderm. We compare the expression of regulatory factors during the development of mesoderm and components of the digestive system, in various spiralians to examine proposed scenarios related to the evolution of these tissues.
ISSN:1058-8388
1097-0177
DOI:10.1002/dvdy.24308