Cis-regulatory evolution that caused change inwinglessexpression pattern associated with wing pigmentation pattern ofDrosophila

Abstract

AbstractGenetic mechanisms underlying the acquisition of new traits are an important topic in evolutionary developmental biology. Especially, the co-option of important regulatory genes potentially plays an important role in the gain of new traits. However, how the co-option occurs at the sequence level is still elusive.Drosophila guttiferahas a unique wing pigmentation pattern and this is newly gained via the evolution of the expression pattern ofwingless, which induces the pigmentation pattern formation. In this study, to reveal the changes in thecis-regulatory sequence which caused the co-option ofwinglessthat lead to the expression in a new place, we conducted transgenic EGFP reporter assays of alteredcis-regulatory sequences. As a result, the sequence was divided into regions needed to activate expression in the entire wing veins and a region required for repressing expression in excess parts. Comparisons with the homologous sequence ofDrosophila melanogastershowed that the repressive function of thecis-regulatory region is also possessed byD. melanogasterwhile the activating function is newly gained in a lineage leading toD. guttifera. Furthermore, a putative binding site of SMAD transcription factors is shown to be essential for activating expression but also existing in the homologous region ofD. melanogaster. Our results suggest that the pre-existing regulatory sequences in thecis-regulatory region coordinate with the newly gained sequences to acquire the new expression pattern ofwingless.Graphical Abstract