Leading role of TBP in the Establishment of Complexity in Eukaryotic Transcription Initiation Systems

While both archaeal and eukaryotic transcription initiation systems utilize TBP (TATA box-binding protein) and TFIIB (transcription factor IIB), eukaryotic systems include larger numbers of initiation factors. It remains uncertain how eukaryotic transcription initiation systems have evolved. Here, we investigate the evolutionary development of TBP and TFIIB, each of which has an intramolecular direct repeat, using two evolutionary indicators. Inter-repeat sequence dissimilarity (dDR, distance between direct repeats) indicates that the asymmetry of two repeats in TBP and TFIIB has gradually increased during evolution. Interspecies sequence diversity (PD, phylogenetic diversity) indicates that the resultant asymmetric structure, which is related to the ability to interact with multiple factors, diverged in archaeal TBP and archaeal/eukaryotic TFIIB during evolution. Our findings suggest that eukaryotic TBP initially acquired multiple Eukarya-specific interactors through asymmetric evolution of the two repeats. After the asymmetric TBP generated the complexity of the eukaryotic transcription initiation systems, its diversification halted and its asymmetric structure spread throughout eukaryotic species. [Display omitted] •The evolutionary development of TBP and TFIIB was examined by using dDR and PD•dDR values showed that mutations generated the asymmetric structure of eukaryotic TBP•PD values showed that the diversification of eukaryotic TBP halted during evolution•TBP’s asymmetric structure led to the complexity of eukaryotic transcription systems Kawakami et al. examine the evolutionary development of TBP and TFIIB using two evolutionary indicators, dDR and PD. dDR shows that mutations generate the asymmetric structure of eukaryotic TBP. PD shows that the diversification of eukaryotic TBP halted during evolution. TBP’s asymmetric structure thus led to the complexity of eukaryotic transcription initiation systems.