Abstract
Embryonic development relies on activating and repressing regulatory influences that are faithfully integrated at the core promoter of individual genes. In vertebrates, the basal machinery recognizing the core promoter includes TATA-binding protein (TBP) and two TBP-related factors. In Xenopus embryos, the three TBP family factors are all essential for development and are required for expression of distinct subsets of genes. Here, we report on a non-canonical TBP family-insensitive (TFI) mechanism of transcription initiation that involves mesoderm and organizer gene expression. Using TBP family single- and triple-knockdown experiments, α-amanitin treatment, transcriptome profiling and chromatin immunoprecipitation, we found that TFI gene expression cannot be explained by functional redundancy, is supported by active transcription and shows normal recruitment of the initiating form of RNA polymerase II to the promoter. Strikingly, recruitment of Gcn5 (also known as Kat2a), a co-activator that has been implicated in transcription initiation, to TFI gene promoters is increased upon depletion of TBP family factors. TFI genes are part of a densely connected TBP family-insensitive T-box-Otx2-Gsc interaction network. The results indicate that this network of genes bound by Vegt, Eomes, Otx2 and Gsc utilizes a novel, flexible and non-canonical mechanism of transcription that does not require TBP or TBP-related factors.
Highlights
The gene expression patterns underlying embryonic development are orchestrated by highly complex gene regulatory networks
TATA-binding protein (TBP) family-insensitive gene transcription in early Xenopus embryos TBP, TBP-like factor (TLF) and TATA-binding protein 2 (TBP2) are all essential for gastrulation and for transcription of partially overlapping subsets of genes in Xenopus laevis embryos (Jacobi et al, 2007; Jallow et al, 2004; Veenstra et al, 2000)
Induced transcripts were identified using statistical change calls (Wilcoxon P
Summary
The gene expression patterns underlying embryonic development are orchestrated by highly complex gene regulatory networks. The step-wise mechanism of transcription initiation is known to start with binding of TFIID, a complex of TATA-binding protein (TBP) and TBP-associated factors (TAFs). In this canonical mechanism of transcription initiation TBP binding represents a. The TBP family comprises TBP ( present in archaea and all eukaryotes), TBP-like factor (TLF; known as TBPL1/TRF2/TLP; present in all metazoans) and TATA-binding protein 2 (TBP2; known as TBPL2/TRF3; unique to vertebrates) (Akhtar and Veenstra, 2011). TBP, TLF and TBP2 regulate different subsets of transcripts during gastrulation and these transcripts functionally link TLF and TBP2 to the metazoan and vertebrate developmental programs (Jacobi et al, 2007)
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