Adventitious roots (ARs) are an important type of plant root and display high phenotypic plasticity in response to different environmental stimuli. It is known that photoreceptors inhibit darkness-induced hypocotyl adventitious root (HAR) formation by directly stabilizing Aux/IAA proteins. In this study, we further report that phytochrome-interacting factors (PIFs) plays a central role in HAR initiation by simultaneously inducing the expression of genes involved in auxin biosynthesis, auxin transport and the transcriptional control of root primordium initiation. We found that, on the basis of their activity downstream of phytochrome, PIFs are required for darkness-induced HAR formation. Specifically, PIFs directly bind to the promoters of some genes involved in root formation, including auxin biosynthesis genes YUCCA2 (YUC2) and YUC6, the auxin influx carrier genes AUX1 and LAX3, and the transcription factors WOX5/7 and LBD16/29, to activate their expression. These findings reveal a previously uncharacterized transcriptional regulatory network underlying HAR formation.