Cell type-specific responses to wingless, hedgehog and decapentaplegic are essential for patterning early eye-antenna disc in Drosophila

PLoS One. 2015 Apr 7;10(4):e0121999. doi: 10.1371/journal.pone.0121999. eCollection 2015.

Abstract

The Drosophila eye-antenna imaginal disc (ead) is a flattened sac of two-layered epithelia, from which most head structures are derived. Secreted morphogens like Wingless (Wg), Hedgehog (Hh), and Decapentaplegic (Dpp) are important for early patterning of ead, but the underlying mechanisms are still largely unknown. To understand how these morphogens function in the ead of early larval stages, we used wg-LacZ and dpp-Gal4 markers for the examination of wild-type and mutant eads. We found that the ead immediately after hatching was crescent-shaped with the Bolwig's nerve at the ventral edge, suggesting that it consists of dorsal domain. In a subsequent step, transcriptional induction of dpp in the cells along the Bolwig's nerve was followed by rapid growth of the ventral domain. Both Wg and Hh were required for the formation of the ventral domain. Wg was crucial for the growth of the entire ead, but Hh was essential for cell division only in the dorsal domain. In the ventral domain, Hh regulated dpp transcription. Based on these data, we propose that signaling among distinct groups of cells expressing Wg, Dpp, or Hh in the ead of the first-instar larvae are critical for coordinated growth and patterning of ead.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Body Patterning / physiology*
  • Drosophila Proteins / metabolism*
  • Drosophila melanogaster / embryology
  • Drosophila melanogaster / genetics
  • Drosophila melanogaster / growth & development*
  • Eye / embryology
  • Eye / growth & development*
  • Eye / metabolism
  • Female
  • Gene Expression Regulation, Developmental*
  • Hedgehog Proteins / metabolism*
  • Immunoenzyme Techniques
  • Male
  • Morphogenesis
  • Mutation / genetics
  • Signal Transduction
  • Wnt1 Protein / metabolism*

Substances

  • Drosophila Proteins
  • Hedgehog Proteins
  • Wnt1 Protein
  • dpp protein, Drosophila
  • wg protein, Drosophila
  • hh protein, Drosophila

Grants and funding

This research was supported by a KAIST Grant G04080077, N10100001, and National Research Foundation R1A1A301573. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.