Format

Send to

Choose Destination
Proc Natl Acad Sci U S A. 2015 Jun 16;112(24):7524-9. doi: 10.1073/pnas.1509022112. Epub 2015 Jun 1.

Gain of cis-regulatory activities underlies novel domains of wingless gene expression in Drosophila.

Author information

1
Laboratory of Molecular Biology, University of Wisconsin, Madison, WI 53706; Howard Hughes Medical Institute, University of Wisconsin, Madison, WI 53706; The Hakubi Center for Advanced Research and Graduate School of Science, Kyoto University, Kyoto 606-8502, Japan;
2
Laboratory of Molecular Biology, University of Wisconsin, Madison, WI 53706; Howard Hughes Medical Institute, University of Wisconsin, Madison, WI 53706;
3
Department of Biological Sciences, University of Alabama, Tuscaloosa, AL 35487;
4
Department of Biological Sciences, Michigan Technological University, Houghton, MI 49931.
5
Laboratory of Molecular Biology, University of Wisconsin, Madison, WI 53706; Howard Hughes Medical Institute, University of Wisconsin, Madison, WI 53706; carrolls@hhmi.org.

Abstract

Changes in gene expression during animal development are largely responsible for the evolution of morphological diversity. However, the genetic and molecular mechanisms responsible for the origins of new gene-expression domains have been difficult to elucidate. Here, we sought to identify molecular events underlying the origins of three novel features of wingless (wg) gene expression that are associated with distinct pigmentation patterns in Drosophila guttifera. We compared the activity of cis-regulatory sequences (enhancers) across the wg locus in D. guttifera and Drosophila melanogaster and found strong functional conservation among the enhancers that control similar patterns of wg expression in larval imaginal discs that are essential for appendage development. For pupal tissues, however, we found three novel wg enhancer activities in D. guttifera associated with novel domains of wg expression, including two enhancers located surprisingly far away in an intron of the distant Wnt10 gene. Detailed analysis of one enhancer (the vein-tip enhancer) revealed that it overlapped with a region controlling wg expression in wing crossveins (crossvein enhancer) in D. guttifera and other species. Our results indicate that one novel domain of wg expression in D. guttifera wings evolved by co-opting pre-existing regulatory sequences governing gene activity in the developing wing. We suggest that the modification of existing enhancers is a common path to the evolution of new gene-expression domains and enhancers.

KEYWORDS:

development; enhancers; gene regulation; novelty; pigmentation

PMID:
26034272
PMCID:
PMC4475944
DOI:
10.1073/pnas.1509022112
[Indexed for MEDLINE]
Free PMC Article

Supplemental Content

Full text links

Icon for HighWire Icon for PubMed Central
Loading ...
Support Center