Groucho-dependent repression by sloppy-paired 1 differentially positions anterior pair-rule stripes in the Drosophila embryo

Dev Biol. 2004 Dec 15;276(2):541-51. doi: 10.1016/j.ydbio.2004.09.025.

Abstract

The Drosophila body plan is composed of a linear array of cephalic, thoracic, and abdominal segments along the anterior posterior axis. The number and positions of individual segments are established by a transcriptional network comprised of maternal effect, gap, pair-rule, and segment polarity genes. The sloppy-paired (slp) locus contains two genes (slp1 and slp2) that are expressed in overlapping striped patterns in the presumptive thorax and abdomen. Previous studies suggest that these genes function at the pair-rule and segment polarity levels to establish the spacing and polarity of thoracic and abdominal segments. One of these genes (slp1) is also expressed in a broad anterior domain that appears before the striped patterns. There are severe cephalic defects in slp1 mutants, including the complete loss of the mandibular segment, but the molecular roles played by Slp1 in anterior patterning are not clear. Here, we present evidence that the anterior Slp1 domain acts as a gradient to differentially repress the anteriormost stripes of several different pair-rule genes. This repressive gradient contributes to the precise spatial arrangement of anterior pair-rule stripe borders required for expression of the first engrailed stripe and the formation of the mandibular segment. These results suggest that Slp1 functions as a gap gene-like repressor, in addition to its roles at the pair-rule and segment polarity levels of the hierarchy. The Slp1 protein contains a protein motif (EH1) which mediates binding to the transcriptional corepressor Groucho (Gro). We show that this domain is required for Slp1-mediated repression in vivo.

Publication types

  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, Non-P.H.S.
  • Research Support, U.S. Gov't, P.H.S.

MeSH terms

  • Animals
  • Animals, Genetically Modified
  • Basic Helix-Loop-Helix Transcription Factors
  • Body Patterning*
  • DNA-Binding Proteins / genetics
  • DNA-Binding Proteins / metabolism*
  • Drosophila Proteins / genetics
  • Drosophila Proteins / metabolism*
  • Drosophila melanogaster / embryology*
  • Drosophila melanogaster / physiology
  • Female
  • Gene Expression Regulation, Developmental*
  • Male
  • Morphogenesis
  • Repressor Proteins / genetics
  • Repressor Proteins / metabolism*
  • Transcription Factors / genetics
  • Transcription Factors / metabolism*

Substances

  • Basic Helix-Loop-Helix Transcription Factors
  • DNA-Binding Proteins
  • Drosophila Proteins
  • Repressor Proteins
  • Transcription Factors
  • gro protein, Drosophila
  • slp1 protein, Drosophila