The structure and evolution of cis-regulatory regions: the shavenbaby story

Philos Trans R Soc Lond B Biol Sci. 2013 Nov 11;368(1632):20130028. doi: 10.1098/rstb.2013.0028. Print 2013 Dec 19.

Abstract

In this paper, we provide a historical account of the contribution of a single line of research to our current understanding of the structure of cis-regulatory regions and the genetic basis for morphological evolution. We revisit the experiments that shed light on the evolution of larval cuticular patterns within the genus Drosophila and the evolution and structure of the shavenbaby gene. We describe the experiments that led to the discovery that multiple genetic changes in the cis-regulatory region of shavenbaby caused the loss of dorsal cuticular hairs (quaternary trichomes) in first instar larvae of Drosophila sechellia. We also discuss the experiments that showed that the convergent loss of quaternary trichomes in D. sechellia and Drosophila ezoana was generated by parallel genetic changes in orthologous enhancers of shavenbaby. We discuss the observation that multiple shavenbaby enhancers drive overlapping patterns of expression in the embryo and that these apparently redundant enhancers ensure robust shavenbaby expression and trichome morphogenesis under stressful conditions. All together, these data, collected over 13 years, provide a fundamental case study in the fields of gene regulation and morphological evolution, and highlight the importance of prolonged, detailed studies of single genes.

Keywords: cis-regulatory evolution; cis-regulatory structure; evolution of enhancer function; morphological change; shavenbaby gene.

Publication types

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

MeSH terms

  • Animals
  • DNA-Binding Proteins / genetics*
  • DNA-Binding Proteins / metabolism
  • Drosophila / embryology
  • Drosophila / genetics*
  • Drosophila / growth & development
  • Drosophila Proteins / genetics*
  • Drosophila Proteins / metabolism
  • Evolution, Molecular*
  • Gene Expression Regulation, Developmental / genetics*
  • Morphogenesis / genetics*
  • Regulatory Sequences, Nucleic Acid / genetics*
  • Species Specificity
  • Transcription Factors / genetics*
  • Transcription Factors / metabolism
  • Trichomes / genetics
  • Trichomes / growth & development*

Substances

  • DNA-Binding Proteins
  • Drosophila Proteins
  • Transcription Factors
  • ovo protein, Drosophila