A transient contractile seam promotes epithelial sealing and sequential assembly of body segments

Abstract

In embryos, epithelial sealing proceeds with progressive zipping eventually leading to a scar-free epithelium and ensuring the assembly of body segments in insects and neural tube in mammals. How zipping is mechanically controlled to promote tissue fusion on long distances, remains unclear. Combining physical modeling with genetic and mechanical perturbations, we reveal the existence of a transient contractile seam that generates forces to reduce the zipping angle by force balance, consequently promoting epidermal sealing during Drosophila embryogenesis. The seam is formed by the adhesion of two tissues, the epidermis and amnioserosa, and is stabilized by the tensions generated by the segment boundaries. Once a segment is zipped, the seam disassembles concurrently with the inactivation of the Jun kinase pathway. Thus, we show that epithelial sealing is promoted by a transient actomyosin contractile seam allowing sequential segment assembly.

The research leading to these results has received funding from the Spanish Ministry of Economy and Competitiveness, Plan Nacional, BFU2015-68754, the Spanish Ministry of Science and Innovation, Plan National, PID2019-109117GB-100, funded by MICIU/AEI/10.13039/501100011033 and PID2022-142779NB-100, funded by MICIU/AEI/10.13039/501100011033 and by ERDF, EU, “Centro de Excelencia Severo Ochoa” and to the EMBL partnership. S.R. acknowledges the support by a fellowship from International Human Frontier Science Program, LT0007/2022-L. E.T. acknowledges the support by a fellowship by the UPV/EHU, PIF20/193. L.B. acknowledges the support received from the IKUR Strategy of the Basque Government. This study is part of the PIBA_2023_1_0033 project, funded by the Basque Government under the grant PIBA - PUE 2022. We acknowledge the support of the CERCA Program/Generalitat de Catalunya. This work was supported in part by the Fundaciòn Biofisika Bizkaia and the Basque Excellent Research Centre (BERC) program of the Basque Government.