Dpp signaling activity requires Pentagone to scale with tissue size in the growing Drosophila wing imaginal disc

PLoS Biol. 2011 Oct;9(10):e1001182. doi: 10.1371/journal.pbio.1001182. Epub 2011 Oct 25.

Abstract

The wing of the fruit fly, Drosophila melanogaster, with its simple, two-dimensional structure, is a model organ well suited for a systems biology approach. The wing arises from an epithelial sac referred to as the wing imaginal disc, which undergoes a phase of massive growth and concomitant patterning during larval stages. The Decapentaplegic (Dpp) morphogen plays a central role in wing formation with its ability to co-coordinately regulate patterning and growth. Here, we asked whether the Dpp signaling activity scales, i.e. expands proportionally, with the growing wing imaginal disc. Using new methods for spatial and temporal quantification of Dpp activity and its scaling properties, we found that the Dpp response scales with the size of the growing tissue. Notably, scaling is not perfect at all positions in the field and the scaling of target gene domains is ensured specifically where they define vein positions. We also found that the target gene domains are not defined at constant concentration thresholds of the downstream Dpp activity gradients P-Mad and Brinker. Most interestingly, Pentagone, an important secreted feedback regulator of the pathway, plays a central role in scaling and acts as an expander of the Dpp gradient during disc growth.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • DNA-Binding Proteins / metabolism
  • Drosophila Proteins / metabolism*
  • Drosophila melanogaster / growth & development*
  • Drosophila melanogaster / metabolism
  • Extracellular Matrix Proteins / metabolism*
  • Female
  • Green Fluorescent Proteins / metabolism
  • Homeodomain Proteins / metabolism
  • Larva / growth & development
  • Larva / metabolism
  • Male
  • Microscopy, Fluorescence
  • Morphogenesis
  • Nerve Tissue Proteins / metabolism
  • Organ Size
  • Phosphorylation
  • Recombinant Fusion Proteins / metabolism
  • Repressor Proteins / metabolism
  • T-Box Domain Proteins / metabolism
  • Transcription Factors / metabolism
  • Wings, Animal / blood supply
  • Wings, Animal / growth & development*

Substances

  • DNA-Binding Proteins
  • Dad protein, Drosophila
  • Drosophila Proteins
  • Extracellular Matrix Proteins
  • Homeodomain Proteins
  • MAD protein, Drosophila
  • Magu protein, Drosophila
  • Nerve Tissue Proteins
  • Recombinant Fusion Proteins
  • Repressor Proteins
  • T-Box Domain Proteins
  • Transcription Factors
  • brk protein, Drosophila
  • dpp protein, Drosophila
  • salm protein, Drosophila
  • bi protein, Drosophila
  • Green Fluorescent Proteins