RRC ID 57397
Author Koshikawa S, Giorgianni MW, Vaccaro K, Kassner VA, Yoder JH, Werner T, Carroll SB.
Title Gain of cis-regulatory activities underlies novel domains of wingless gene expression in Drosophila.
Journal Proc. Natl. Acad. Sci. U.S.A.
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.
Volume 112(24)
Pages 7524-9
Published 2015-6-16
DOI 10.1073/pnas.1509022112
PII 1509022112
PMID 26034272
PMC PMC4475944
MeSH Animals Animals, Genetically Modified Drosophila / genetics* Drosophila / growth & development Drosophila Proteins / genetics* Drosophila melanogaster / genetics* Drosophila melanogaster / growth & development Enhancer Elements, Genetic Evolution, Molecular Gene Expression Regulation, Developmental Genes, Insect Genetic Complementation Test Molecular Sequence Data Species Specificity Wings, Animal / growth & development Wings, Animal / metabolism Wnt Proteins / genetics Wnt1 Protein / genetics*
IF 9.504
Resource
Drosophila E-14201