Sex Differences in Drosophila Somatic Gene Expression: Variation and Regulation by doublesex

G3 (Bethesda). 2016 Jul 7;6(7):1799-808. doi: 10.1534/g3.116.027961.

Abstract

Sex differences in gene expression have been widely studied in Drosophila melanogaster Sex differences vary across strains, but many molecular studies focus on only a single strain, or on genes that show sexually dimorphic expression in many strains. How extensive variability is and whether this variability occurs among genes regulated by sex determination hierarchy terminal transcription factors is unknown. To address these questions, we examine differences in sexually dimorphic gene expression between two strains in Drosophila adult head tissues. We also examine gene expression in doublesex (dsx) mutant strains to determine which sex-differentially expressed genes are regulated by DSX, and the mode by which DSX regulates expression. We find substantial variation in sex-differential expression. The sets of genes with sexually dimorphic expression in each strain show little overlap. The prevalence of different DSX regulatory modes also varies between the two strains. Neither the patterns of DSX DNA occupancy, nor mode of DSX regulation explain why some genes show consistent sex-differential expression across strains. We find that the genes identified as regulated by DSX in this study are enriched with known sites of DSX DNA occupancy. Finally, we find that sex-differentially expressed genes and genes regulated by DSX are highly enriched on the fourth chromosome. These results provide insights into a more complete pool of potential DSX targets, as well as revealing the molecular flexibility of DSX regulation.

Keywords: Drosophila; Genetics of Sex; RNA-seq; doublesex; gene expression; sex bias; sex determination; sex hierarchy; transcriptome.

MeSH terms

  • Animals
  • Chromosome Mapping
  • DNA / genetics
  • DNA / metabolism
  • DNA-Binding Proteins / genetics*
  • DNA-Binding Proteins / metabolism
  • Drosophila Proteins / genetics*
  • Drosophila Proteins / metabolism
  • Drosophila melanogaster / genetics*
  • Drosophila melanogaster / growth & development
  • Drosophila melanogaster / metabolism
  • Female
  • Gene Expression Regulation, Developmental*
  • Male
  • Nerve Tissue Proteins / genetics
  • Nerve Tissue Proteins / metabolism
  • Nuclear Proteins / genetics
  • Nuclear Proteins / metabolism
  • Protein Binding
  • Protein Interaction Mapping
  • RNA-Binding Proteins / genetics
  • RNA-Binding Proteins / metabolism
  • Ribonucleoproteins / genetics
  • Ribonucleoproteins / metabolism
  • Sex Characteristics*
  • Sex Determination Processes*
  • Transcription Factors / genetics
  • Transcription Factors / metabolism
  • Transcriptome*

Substances

  • DNA-Binding Proteins
  • DSX protein, Drosophila
  • Drosophila Proteins
  • Nerve Tissue Proteins
  • Nuclear Proteins
  • RNA-Binding Proteins
  • Ribonucleoproteins
  • Sxl protein, Drosophila
  • Tra protein, Drosophila
  • Transcription Factors
  • fru protein, Drosophila
  • msl-2 protein, Drosophila
  • tra2 protein, Drosophila
  • DNA