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The  knirps  ( kni ) locus encodes transcription factors required for induction of the L2 wing vein in  Drosophila . Here, we employ diverse CRISPR/Cas9 genome editing tools to generate a series of targeted lesions within the endogenous cis-regulatory module (CRM) required for  kni  expression in the L2 vein primordium. Phenotypic analysis of these ‘ in locus ’ mutations based on both expression of Kni protein and adult wing phenotypes, reveals novel unexpected features of L2-CRM function including evidence for a chromosome pairing-dependent process that promotes transcription. We also demonstrate that self-propagating active genetic elements (CopyCat elements) can efficiently delete and replace the L2-CRM with orthologous sequences from other divergent fly species. Wing vein phenotypes resulting from these trans-species enhancer replacements parallel features of the respective donor fly species. This highly sensitive phenotypic readout of enhancer function in a native genomic context reveals novel features of CRM function undetected by traditional reporter gene analysis.

CRISPR/Cas9 and active genetics-based trans-species replacement of the endogenous Drosophila kni -L2 CRM reveals unexpected complexity