A low affinity cis-regulatory BMP response element restricts target gene activation to subsets of Drosophila neurons

Elife. 2020 Oct 30:9:e59650. doi: 10.7554/eLife.59650.

Abstract

Retrograde BMP signaling and canonical pMad/Medea-mediated transcription regulate diverse target genes across subsets of Drosophila efferent neurons, to differentiate neuropeptidergic neurons and promote motor neuron terminal maturation. How a common BMP signal regulates diverse target genes across many neuronal subsets remains largely unresolved, although available evidence implicates subset-specific transcription factor codes rather than differences in BMP signaling. Here we examine the cis-regulatory mechanisms restricting BMP-induced FMRFa neuropeptide expression to Tv4-neurons. We find that pMad/Medea bind at an atypical, low affinity motif in the FMRFa enhancer. Converting this motif to high affinity caused ectopic enhancer activity and eliminated Tv4-neuron expression. In silico searches identified additional motif instances functional in other efferent neurons, implicating broader functions for this motif in BMP-dependent enhancer activity. Thus, differential interpretation of a common BMP signal, conferred by low affinity pMad/Medea binding motifs, can contribute to the specification of BMP target genes in efferent neuron subsets.

Keywords: D. melanogaster; bmp-activated smad transcription factors; cis-regulatory bmp response element; low affinity binding motif; neuroscience.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Bone Morphogenetic Proteins / genetics
  • Bone Morphogenetic Proteins / metabolism*
  • Drosophila Proteins / genetics
  • Drosophila Proteins / metabolism
  • Drosophila melanogaster / genetics
  • Drosophila melanogaster / metabolism*
  • Gene Expression Regulation
  • Neurons / metabolism*
  • Response Elements*
  • Signal Transduction
  • Smad4 Protein / genetics
  • Smad4 Protein / metabolism

Substances

  • Bone Morphogenetic Proteins
  • Drosophila Proteins
  • Med protein, Drosophila
  • Smad4 Protein