SoxNeuro and Shavenbaby act cooperatively to shape denticles in the embryonic epidermis of Drosophila

Development. 2017 Jun 15;144(12):2248-2258. doi: 10.1242/dev.150169. Epub 2017 May 15.

Abstract

During development, extracellular signals are integrated by cells to induce the transcriptional circuitry that controls morphogenesis. In the fly epidermis, Wingless (Wg)/Wnt signaling directs cells to produce either a distinctly shaped denticle or no denticle, resulting in a segmental pattern of denticle belts separated by smooth, or 'naked', cuticle. Naked cuticle results from Wg repression of shavenbaby (svb), which encodes a transcription factor required for denticle construction. We have discovered that although the svb promoter responds differentially to altered Wg levels, Svb alone cannot produce the morphological diversity of denticles found in wild-type belts. Instead, a second Wg-responsive transcription factor, SoxNeuro (SoxN), cooperates with Svb to shape the denticles. Co-expressing ectopic SoxN with svb rescued diverse denticle morphologies. Conversely, removing SoxN activity eliminated the residual denticles found in svb mutant embryos. Furthermore, several known Svb target genes are also activated by SoxN, and we have discovered two novel target genes of SoxN that are expressed in denticle-producing cells and that are regulated independently of Svb. We conclude that proper denticle morphogenesis requires transcriptional regulation by both SoxN and Svb.

Keywords: Denticle; Drosophila melanogaster; Morphogenesis; Ovo; Shavenbaby; SoxNeuro; Wingless; Wnt.

MeSH terms

  • Animals
  • Animals, Genetically Modified
  • Binding Sites
  • DNA-Binding Proteins / genetics
  • DNA-Binding Proteins / metabolism*
  • Drosophila Proteins / genetics
  • Drosophila Proteins / metabolism*
  • Drosophila melanogaster / embryology*
  • Drosophila melanogaster / genetics
  • Drosophila melanogaster / metabolism*
  • Epidermis / embryology*
  • Epidermis / metabolism*
  • Gene Expression Regulation, Developmental
  • Genes, Insect
  • Models, Biological
  • Morphogenesis / genetics
  • Morphogenesis / physiology
  • Mutation
  • Promoter Regions, Genetic
  • SOX Transcription Factors / genetics
  • SOX Transcription Factors / metabolism*
  • Signal Transduction
  • Transcription Factors / genetics
  • Transcription Factors / metabolism*
  • Wnt1 Protein / genetics
  • Wnt1 Protein / metabolism

Substances

  • DNA-Binding Proteins
  • Drosophila Proteins
  • SOX Transcription Factors
  • SoxN protein, Drosophila
  • Transcription Factors
  • Wnt1 Protein
  • ovo protein, Drosophila
  • wg protein, Drosophila