Phenotypic robustness conferred by apparently redundant transcriptional enhancers

NICOLÁS FRANKEL; GREGORY K. DAVIS; DIEGO VARGAS; SHU WANG; FRANCOIS PAYRE; DAVID L. STERN

NATURE

NATURE PUBLISHING GROUP

Año: 2010 vol. 466 p. 490 - 493

0028-0836

Genes include cis-regulatory regions that contain transcriptionalenhancers. Recent reports have shown that developmental genesoften possess multiple discrete enhancer modules that drive transcriptionin similar spatio-temporal patterns: primary enhancerslocated near the basal promoter and secondary, or ‘shadow’,enhancers located at more remote positions. It has been proposedthat the seemingly redundant activity of primary and secondaryenhancers contributes to phenotypic robustness. We tested thishypothesis by generating a deficiency that removes two newlydiscovered enhancers of shavenbaby (svb, a transcript of the ovolocus), a gene encoding a transcription factor that directs developmentof Drosophila larval trichomes. At optimal temperatures forembryonic development, this deficiency causes minor defects intrichome patterning. In embryos that develop at both low andhigh extreme temperatures, however, absence of these secondaryenhancers leads to extensive loss of trichomes. These temperaturedependentdefects can be rescued by a transgene carrying a secondaryenhancer driving transcription of the svb cDNA. Finally, removal ofone copy of wingless, a gene required for normal trichome patterning, causes a similar loss of trichomes only in flies lacking thesecondary enhancers. These results support the hypothesis thatsecondary enhancers contribute to phenotypic robustness in the faceof environmental and genetic variability.