Promoter bound Core Factor recruits Pol I/Rrn3, and loads DNA into the cleft of Pol I (A). At this stage, both Rrn7 N-terminal domain and A49 tandem winged helix domain are flexible. Pol I cleft is open to make room for loading of DNA. The intrinsic mobility of Core Factor upon Pol I engagement then ratchets upstream DNA against Rpb5. Promoter DNA melting occurs when Core Factor reaches a critical position where Rrn7 zinc ribbon/linker regions are stabilized on Pol I (1). This is likely a very transient state, allowing Pol I to recognize the initiation site in the template strand DNA and start synthesizing the RNA (B). Besides the well-accepted role for sensing the growing RNA length for its counterpart TFIIB in the Pol II PIC, Rrn7 likely plays an additional role in facilitating promoter opening by reaching into the RNA exit channel of Pol I and favoring the bending of DNA. During further translocation of Pol I along the promoter (2), the enzyme is acting more similarly as an elongation mode, with a more closed clamp. The gatekeeper linker helices in A49 between the dimerization and tandem winged helix domains presumably work as a ruler of the active site cleft, stabilizing upon clamp closing down while preventing escape of the downstream DNA (C). As RNA grows longer, the A49 tandem winged helix domain can also help displacing the Rrn7 zinc ribbon to clear the RNA exit channel. Subsequently, Pol I escapes the promoter and enters a processive elongation state (3). Pol I in its active, Rrn3 bound form is shown in gray, and Core Factor in green. Transparency and dotted outline indicate flexibility. Solid blue and cyan lines depict the DNA paths that has been experimentally observed [panels A–C revealed in this study; panel D shown in previous studies (Neyer et al., 2016; Tafur et al., 2016), while dotted blue and cyan lines in B and C represent the DNA paths in the preceding stages. In panel A, a hypothetical closed DNA path is depicted as dotted black/gray lines by naturally extending a B-form DNA from upstream Core Factor associated DNA. RNA molecule with growing length during initial stages of transcription is represented in red.