A gene necessary for normal male courtship, yellow, acts downstream of fruitless in the Drosophila melanogaster larval brain

J Neurobiol. 2003 Apr;55(1):53-72. doi: 10.1002/neu.10196.

Abstract

The fruitless (fru) gene is a member of the Drosophila melanogaster somatic sex determination genetic pathway. Although it has been hypothesized that the primary function of fru is to regulate a genetic hierarchy specifying development of adult male courtship behavior, genes acting downstream of fru have not yet been identified. Here we demonstrate that the yellow (y) gene is genetically downstream of fru in the 3(rd)-instar larval brain. Yellow protein is present at elevated levels in neuroblasts, which also show expression of male-specific FRU proteins, compared to control neuroblasts without FRU. A location for y downstream of fru in a genetic pathway was experimentally demonstrated by analysis of fru mutants lacking transcription of zinc-finger DNA binding domains, and of animals with temporal, spatial, or sexual mis-expression of male-specific FRU. A subset of fru and y mutants is known to reduce levels of a specific behavioral component of the male courtship ritual, wing extension, and FRU and Yellow were detected in the general region of the brain whose maleness is necessary for development of that behavior. We therefore hypothesized that ectopic expression of Yellow in the 3(rd)-instar brain, in a y null background, would rescue low levels of wing extension and male competitive mating success, and this was found to be the case. Overall, these data suggest that y is a downstream member of the fru branch of the D. melanogaster sex determination hierarchy, where it plays a currently unknown role in the development of adult male wing extension during courtship.

Publication types

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

MeSH terms

  • Animals
  • Blotting, Western / methods
  • Brain / physiology*
  • Central Nervous System / anatomy & histology
  • Central Nervous System / growth & development
  • Central Nervous System / metabolism
  • Courtship*
  • Drosophila Proteins*
  • Drosophila melanogaster
  • Female
  • Gene Expression Regulation, Developmental
  • Immunohistochemistry / methods
  • Insect Proteins / genetics
  • Insect Proteins / metabolism
  • Insect Proteins / physiology*
  • Larva / genetics
  • Larva / growth & development
  • Larva / physiology*
  • Male
  • Microscopy, Confocal / methods
  • Models, Genetic
  • Mutation
  • Nerve Tissue Proteins / genetics*
  • Nerve Tissue Proteins / metabolism
  • Neurons / metabolism
  • Sex Differentiation / physiology
  • Sexual Behavior, Animal / physiology
  • Transcription Factors / genetics*
  • Transcription Factors / metabolism
  • Transcription, Genetic
  • Up-Regulation
  • Zinc Fingers / physiology

Substances

  • Drosophila Proteins
  • Insect Proteins
  • Nerve Tissue Proteins
  • Transcription Factors
  • fru protein, Drosophila
  • y protein, Drosophila