A dynamic cell recruitment process drives growth of the Drosophila wing by overscaling the vestigial expression pattern

Dev Biol. 2020 Jun 15;462(2):141-151. doi: 10.1016/j.ydbio.2020.03.009. Epub 2020 Mar 19.

Abstract

Organs mainly attain their size by cell growth and proliferation, but sometimes also grow through recruitment of undifferentiated cells. Here we investigate the participation of cell recruitment in establishing the pattern of Vestigial (Vg), the product of the wing selector gene in Drosophila. We find that the Vg pattern overscales along the dorsal-ventral (DV) axis of the wing imaginal disc, i.e., it expands faster than the DV length of the pouch. The overscaling of the Vg pattern cannot be explained by differential proliferation, apoptosis, or oriented-cell divisions, but can be recapitulated by a mathematical model that explicitly considers cell recruitment. When impairing cell recruitment genetically, we find that the Vg pattern almost perfectly scales and adult wings are approximately 20% smaller. Conversely, impairing cell proliferation results in very small wings, suggesting that cell recruitment and cell proliferation additively contribute to organ growth in this system. Furthermore, using fluorescent reporter tools, we provide direct evidence that cell recruitment is initiated between early and mid third-instar larval development. Altogether, our work quantitatively shows when, how, and by how much cell recruitment shapes the Vg pattern and drives growth of the Drosophila wing.

Keywords: Cell recruitment; Drosophila wing disc; Organ growth; Patterning; Scaling; Vestigial.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Body Patterning / genetics*
  • Cell Division
  • Drosophila Proteins / genetics*
  • Drosophila Proteins / metabolism
  • Drosophila melanogaster / embryology
  • Drosophila melanogaster / genetics
  • Gene Expression Regulation, Developmental / genetics
  • Imaginal Discs / growth & development
  • Nuclear Proteins / genetics*
  • Nuclear Proteins / metabolism
  • Signal Transduction
  • Transcription Factors / metabolism
  • Wings, Animal / growth & development*
  • Wnt1 Protein / metabolism

Substances

  • Drosophila Proteins
  • Nuclear Proteins
  • Transcription Factors
  • Wnt1 Protein
  • vg protein, Drosophila