Abstract
The modulation of developmental biochemical pathways by mechanical cues is an emerging feature of animal development, but its evolutionary origins have not been explored. Here we show that a common mechanosensitive pathway involving β-catenin specifies early mesodermal identity at gastrulation in zebrafish and Drosophila. Mechanical strains developed by zebrafish epiboly and Drosophila mesoderm invagination trigger the phosphorylation of β-catenin–tyrosine-667. This leads to the release of β-catenin into the cytoplasm and nucleus, where it triggers and maintains, respectively, the expression of zebrafish brachyury orthologue notail and of Drosophila Twist, both crucial transcription factors for early mesoderm identity. The role of the β-catenin mechanosensitive pathway in mesoderm identity has been conserved over the large evolutionary distance separating zebrafish and Drosophila. This suggests mesoderm mechanical induction dating back to at least the last bilaterian common ancestor more than 570 million years ago, the period during which mesoderm is thought to have emerged.
Highlights
The modulation of developmental biochemical pathways by mechanical cues is an emerging feature of animal development, but its evolutionary origins have not been explored
By performing b-cat immunostainings on zebrafish embryos, we found that marginal b-cat nuclear translocation initiates during the first 20 min of the epiboly morphogenetic movement (Fig. 1b,d,f, dome stage)
In wild-type (WT) fish ntl expression was observed in cells characterized by nuclear b-cat only, indicating that ntl transcription is a cell autonomous response to b-cat nuclear translocation (Supplementary Fig. S1c). b-cat transcriptional activity is necessary for initiation of ntl expression in zebrafish, suggesting that ntl expression is under the control of Wnt ligands that are known to activate b-cat transcriptiondependent events[24]
Summary
The modulation of developmental biochemical pathways by mechanical cues is an emerging feature of animal development, but its evolutionary origins have not been explored. We find that the onset of morphogenetic movements in zebrafish embryos (epiboly) and in Drosophila embryos (mesoderm invagination) triggers the mechanotransductive activation of the phosphorylation of the Y667-b-cat site that impairs its interaction with E-cadherins This leads to its release from the junctions to the nucleus, in the strained mesodermal tissue of the gastrulating embryos. As a consequence, mechanical induction of mesoderm-specific b-cat target genes expression in the strained mesodermal tissue of both species: brachyury (bra) ortholog notail (ntl) in zebrafish and Twist in Drosophila This is, to our knowledge, the first report of an evolutionarily conserved mechanosensitive pathway having a major role in the developmental establishment of the body plan, in this case in early mesoderm specification. Our results suggest a common mechanotransductive origin of mesoderm emergence for Bilateria and is the first demonstration of a role for b-cat in early mesoderm determination in an ecdysozoan (Drosophila melanogaster)[1,15,16,17]
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