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Two consecutive microtubule-based epithelial seaming events mediate dorsal closure in the scuttle fly Megaselia abdita
Fraire-Zamora, Juan José; Jaeger, Johannes, 1973-; Solon, Jérôme
Evolution of morphogenesis is generally associated with changes in genetic regulation. Here, we report evidence indicating that dorsal closure, a conserved morphogenetic process in dipterans, evolved as the consequence of rearrangements in epithelial organization rather than signaling regulation. In Drosophila melanogaster, dorsal closure consists of a two-tissue system where the contraction of extraembryonic amnioserosa and a JNK/Dpp-dependent epidermal actomyosin cable result in microtubule-dependent seaming of the epidermis. We find that dorsal closure in Megaselia abdita, a three-tissue system comprising serosa, amnion and epidermis, differs in morphogenetic rearrangements despite conservation of JNK/Dpp signaling. In addition to an actomyosin cable, M. abdita dorsal closure is driven by the rupture and contraction of the serosa and the consecutive microtubule-dependent seaming of amnion and epidermis. Our study indicates that the evolutionary transition to a reduced system of dorsal closure involves simplification of the seaming process without changing the signaling pathways of closure progression.
We would like to thank Eva Jiménez-Guri, Karl Wotton, and Arturo D’Angelo for reagents and invaluable technical advice during the development of the project. We thank Steffen Lemke for providing training and technical advice as well as Jordi Casanova and Petra Stockinger for discussions and critical reading of the manuscript. All confocal imaging was done at the CRG Advanced Light Microscopy Unit. JJF-Z was supported by a CRG International Interdisciplinary Postdoctoral Programme (INTERPOD) fellowship, co-funded by Marie Curie Actions. We acknowledge support from the Spanish Ministry of Economy and Competitiveness to the EMBL partnership, 'Centro de Excelencia Severo Ochoa', the, Plan Nacional BFU2015-68754-P (MINECO) and the CERCA programme/Generalitat de Catalunya.
-Megaselia abdita
-Developmental biology
-Dorsal closure
-Evolution of development (evo-devo)
-Evolutionary biology
-Extraembryonic tissue (serosa/amnion)
-Genomics
-Microtubule cytoskeleton
-Stem cells
-Tissue seaming
© 2018, Fraire-Zamora et al. This article is distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use and redistribution provided that the original author and source are credited.
http://creativecommons.org/licenses/by/4.0/
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