The general transcription factor TFIID is a core promoter selectivity factor that recognises DNA sequence elements and nucleates the assembly of a pre-initiation complex (PIC). The mechanism by which TFIID recognises the promoter is poorly understood. The TATA box binding protein (TBP) is a subunit of the multi-protein TFIID complex believed to be key to this process. We reconstituted transcription from purified components on a ribosomal protein gene and revealed that TFIIDΔTBP binds and rearranges the promoter DNA topology independent of TBP. TFIIDΔTBP binds ~200 bp of the promoter and changes the DNA topology to a larger extent than the nucleosome core particle. We show that TBP inhibits DNA-binding activities of TFIIDΔTBP and conclude that the complete TFIID complex represents an auto-inhibited state. Furthermore, we show that the DNA binding activities of TFIIDΔTBP are required for assembly of a PIC poised to select the correct transcription start site.