title: Gain of cis-regulatory activities underlies novel domains of wingless gene expression in Drosophila.
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.
authors.affiliation: 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;
authors.forename: Shigeyuki
authors.initials: S
authors.lastname: Koshikawa
authors.affiliation: Laboratory of Molecular Biology, University of Wisconsin, Madison, WI 53706; Howard Hughes Medical Institute, University of Wisconsin, Madison, WI 53706;
authors.forename: Matt W
authors.initials: MW
authors.lastname: Giorgianni
authors.affiliation: Laboratory of Molecular Biology, University of Wisconsin, Madison, WI 53706; Howard Hughes Medical Institute, University of Wisconsin, Madison, WI 53706;
authors.forename: Kathy
authors.initials: K
authors.lastname: Vaccaro
authors.affiliation: Laboratory of Molecular Biology, University of Wisconsin, Madison, WI 53706; Howard Hughes Medical Institute, University of Wisconsin, Madison, WI 53706;
authors.forename: Victoria A
authors.initials: VA
authors.lastname: Kassner
authors.affiliation: Department of Biological Sciences, University of Alabama, Tuscaloosa, AL 35487;
authors.forename: John H
authors.initials: JH
authors.lastname: Yoder
authors.affiliation: Department of Biological Sciences, Michigan Technological University, Houghton, MI 49931.
authors.forename: Thomas
authors.initials: T
authors.lastname: Werner
authors.affiliation: Laboratory of Molecular Biology, University of Wisconsin, Madison, WI 53706; Howard Hughes Medical Institute, University of Wisconsin, Madison, WI 53706; carrolls@hhmi.org.
authors.forename: Sean B
authors.initials: SB
authors.lastname: Carroll
mesh_terms: D000818:Animals; D030801:Animals, Genetically Modified; D004330:Drosophila / Q000235:genetics* / Q000254:growth & development; D029721:Drosophila Proteins / Q000235:genetics*; D004331:Drosophila melanogaster / Q000235:genetics* / Q000254:growth & development; D004742:Enhancer Elements, Genetic; D019143:Evolution, Molecular; D018507:Gene Expression Regulation, Developmental; D017344:Genes, Insect; D005816:Genetic Complementation Test; D008969:Molecular Sequence Data; D013045:Species Specificity; D014921:Wings, Animal / Q000254:growth & development / Q000378:metabolism; D051153:Wnt Proteins / Q000235:genetics; D051155:Wnt1 Protein / Q000235:genetics*
chemical_list: D029721:Drosophila Proteins; D051153:Wnt Proteins; D051155:Wnt1 Protein; C432151:Wnt10 protein, Drosophila; C074622:wg protein, Drosophila
keywords: development; enhancers; gene regulation; novelty; pigmentation