Phenotypic robustness conferred by apparently redundant transcriptional enhancers

Nature. 2010 Jul 22;466(7305):490-3. doi: 10.1038/nature09158. Epub 2010 May 30.

Abstract

Genes include cis-regulatory regions that contain transcriptional enhancers. Recent reports have shown that developmental genes often possess multiple discrete enhancer modules that drive transcription in similar spatio-temporal patterns: primary enhancers located near the basal promoter and secondary, or 'shadow', enhancers located at more remote positions. It has been proposed that the seemingly redundant activity of primary and secondary enhancers contributes to phenotypic robustness. We tested this hypothesis by generating a deficiency that removes two newly discovered enhancers of shavenbaby (svb, a transcript of the ovo locus), a gene encoding a transcription factor that directs development of Drosophila larval trichomes. At optimal temperatures for embryonic development, this deficiency causes minor defects in trichome patterning. In embryos that develop at both low and high extreme temperatures, however, absence of these secondary enhancers leads to extensive loss of trichomes. These temperature-dependent defects can be rescued by a transgene carrying a secondary enhancer driving transcription of the svb cDNA. Finally, removal of one copy of wingless, a gene required for normal trichome patterning, causes a similar loss of trichomes only in flies lacking the secondary enhancers. These results support the hypothesis that secondary enhancers contribute to phenotypic robustness in the face of environmental and genetic variability.

Publication types

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

MeSH terms

  • Animal Structures / anatomy & histology
  • Animal Structures / embryology
  • Animals
  • DNA-Binding Proteins / genetics*
  • Drosophila Proteins / genetics*
  • Drosophila melanogaster / anatomy & histology
  • Drosophila melanogaster / embryology*
  • Drosophila melanogaster / genetics*
  • Drosophila melanogaster / growth & development
  • Enhancer Elements, Genetic / genetics*
  • Gene Expression Regulation, Developmental*
  • Larva / anatomy & histology
  • Larva / genetics
  • Larva / growth & development
  • Models, Genetic
  • Phenotype*
  • Temperature
  • Transcription Factors / genetics*
  • Transcription, Genetic / genetics*
  • Transgenes / genetics

Substances

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