Two consecutive microtubule-based epithelial seaming events mediate dorsal closure in the scuttle fly Megaselia abdita

Elife. 2018 Mar 14:7:e33807. doi: 10.7554/eLife.33807.

Abstract

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.

Keywords: Megaselia abdita; developmental biology; dorsal closure; evolution of development (evo-devo); evolutionary biology; extraembryonic tissue (serosa/amnion); genomics; microtubule cytoskeleton; stem cells; tissue seaming.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Amnion / growth & development
  • Animals
  • Body Patterning / genetics*
  • Diptera / genetics*
  • Diptera / growth & development
  • Drosophila Proteins / genetics*
  • Drosophila melanogaster / genetics
  • Drosophila melanogaster / growth & development
  • Embryonic Development / genetics
  • Epidermal Cells / metabolism
  • Epidermis / growth & development
  • Epithelial Cells / cytology
  • Gene Expression Regulation, Developmental / genetics
  • Humans
  • Infant, Newborn
  • MAP Kinase Kinase 4 / genetics
  • Microtubules / genetics*
  • Signal Transduction / genetics

Substances

  • Drosophila Proteins
  • dpp protein, Drosophila
  • MAP Kinase Kinase 4

Grants and funding

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.