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Divergence of upstream regulatory pathways of the transcription factor  Doublesex  ( Dsx ) serves as a basis for evolution of sex-determining mechanisms in animals. However, little is known about the regulation of  Dsx  in environmental sex determination. In the crustacean  Daphnia magna , environmental sex determination is implemented by male-specific expression of the  Dsx  ortholog,  Dsx1 . Transcriptional regulation of  Dsx1  comprises at least three phases during embryogenesis: non-sex-specific initiation, male-specific up-regulation, and its maintenance. Herein, we demonstrate that the male-specific up-regulation is controlled by the bZIP transcription factor,  Vrille  ( Vri ), an ortholog of the circadian clock genes— Drosophila Vri  and mammalian  E4BP4/NFIL3 . Sequence analysis of the  Dsx1  promoter/enhancer revealed a conserved element among two  Daphnia  species ( D .  magna  and  D .  pulex ), which contains a potential enhancer harboring a consensus Vri binding site overlapped with a consensus Dsx binding site. Besides non-sex-specific expression of  Vri  in late embryos, we found male-specific expression in early gastrula before the  Dsx1  up-regulation phase begins. Knockdown of  Vri  in male embryos showed reduction of  Dsx1  expression. In addition, transient overexpression of  Vri  in early female embryos up-regulated the expression of  Dsx1  and induced male-specific trait. Targeted mutagenesis using CRISPR/Cas9 disrupted the enhancer on genome in males, which led to the reduction of  Dsx1  expression. These results indicate that  Vri  was co-opted as a transcriptional activator of  Dsx1  in environmental sex determination of  D .  magna . The data suggests the remarkably plastic nature of gene regulatory network in sex determination.

Co-option of the bZIP transcription factor Vrille as the activator of Doublesex1 in environmental sex determination of the crustacean Daphnia magna