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The σ enigma: bacterial σ factors, archaeal TFB and eukaryotic TFIIB are homologs.

Burton SP, Burton ZF - Transcription (2014)

Bottom Line: TFIIB and TFB each have two-five-helix cyclin-like repeats (CLRs) that include a C-terminal helix-turn-helix (HTH) motif (CLR/HTH domains).Four homologous HTH motifs are present in bacterial σ factors that are relics of CLR/HTH domains.Sequence similarities clarify models for σ factor and TFB/TFIIB evolution and function and suggest models for promoter evolution.

View Article: PubMed Central - PubMed

Affiliation: a Department of Biochemistry and Molecular Biology ; Michigan State University ; E. Lansing , MI USA.

ABSTRACT
Structural comparisons of initiating RNA polymerase complexes and structure-based amino acid sequence alignments of general transcription initiation factors (eukaryotic TFIIB, archaeal TFB and bacterial σ factors) show that these proteins are homologs. TFIIB and TFB each have two-five-helix cyclin-like repeats (CLRs) that include a C-terminal helix-turn-helix (HTH) motif (CLR/HTH domains). Four homologous HTH motifs are present in bacterial σ factors that are relics of CLR/HTH domains. Sequence similarities clarify models for σ factor and TFB/TFIIB evolution and function and suggest models for promoter evolution. Commitment to alternate modes for transcription initiation appears to be a major driver of the divergence of bacteria and archaea.

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A model for the genesis of life on earth focusing on multi-subunit RNAPs, GTFs and promoters. The red arrow indicates strong competition by eukaryotes suppressing mesophilic archaea. See the text for details.2
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f0007: A model for the genesis of life on earth focusing on multi-subunit RNAPs, GTFs and promoters. The red arrow indicates strong competition by eukaryotes suppressing mesophilic archaea. See the text for details.2

Mentions: Previously, a working model was proposed for genesis of life on earth that concentrated on the likely central roles of 2-DPBB type multi-subunit RNAPs found in bacteria, archaea and eukaryotes.2 The model gave insight into the RNA-protein world, LUCA, LECA and the role of the RNAP II CTD and its extensive interactome in evolution of eukaryote complexity. An updated version of the model that incorporates σ homology to TFB/TFIIB, promoter anchor DNA sequences and promoter evolution is shown in Figure 7. The concept of a 4-CLR/HTH PIF at LUCA enhances the model for radiation of bacteria with 4-CLR/HTH σ factors with 4 degenerate CLR/HTH repeats and archaea with 2-CLR/HTH TFB with 2 highly conserved CLR/HTH repeats. Bacterial σ factors, therefore, are posited to be most similar to a 4-CLR/HTH PIF in overall domain structure, and conserved archaeal TFB CLR/HTH repeats are posited to be most similar to PIF CLR/HTH domains in sequence. It is posited that bacteria and archaea are early radiations from LUCA that diverged largely because of their fundamental differences in GTFs and, therefore, their alternate approaches to genome interpretation. Bacteria became committed to σ factors for promoter recognition, and RNAP recruitment is tightly coupled to σ factor binding to core RNAP in bacteria. Co-evolution of bacterial σ factors and RNAP, therefore, is proposed to have driven streamlining to a simpler RNAP subunit structure (α2ββ’ω). Evolution of the bacterial promoters is posited to be driven by co-evolution with interacting σ CLR/HTH domains. Archaeal TFB is proposed to have lost 2-CLR/HTH domains from a 4-CLR/HTH PIF and gained a N-terminal Zn ribbon and B-reader region. In archaea, cooperation of TFB with TBP is posited to have allowed for the losses of 2-CLR/HTH domains from the PIF and the gain of the N-terminal Zn ribbon and B-reader. In initiation mechanisms, TFB-TBP GTFs appear less strongly coupled to archaeal RNAP than bacterial σ factors and bacterial RNAP. This difference in GTFs may have allowed archaea to retain a more ornate RNAP subunit structure than observed in bacteria.Figure 7.


The σ enigma: bacterial σ factors, archaeal TFB and eukaryotic TFIIB are homologs.

Burton SP, Burton ZF - Transcription (2014)

A model for the genesis of life on earth focusing on multi-subunit RNAPs, GTFs and promoters. The red arrow indicates strong competition by eukaryotes suppressing mesophilic archaea. See the text for details.2
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4581349&req=5

f0007: A model for the genesis of life on earth focusing on multi-subunit RNAPs, GTFs and promoters. The red arrow indicates strong competition by eukaryotes suppressing mesophilic archaea. See the text for details.2
Mentions: Previously, a working model was proposed for genesis of life on earth that concentrated on the likely central roles of 2-DPBB type multi-subunit RNAPs found in bacteria, archaea and eukaryotes.2 The model gave insight into the RNA-protein world, LUCA, LECA and the role of the RNAP II CTD and its extensive interactome in evolution of eukaryote complexity. An updated version of the model that incorporates σ homology to TFB/TFIIB, promoter anchor DNA sequences and promoter evolution is shown in Figure 7. The concept of a 4-CLR/HTH PIF at LUCA enhances the model for radiation of bacteria with 4-CLR/HTH σ factors with 4 degenerate CLR/HTH repeats and archaea with 2-CLR/HTH TFB with 2 highly conserved CLR/HTH repeats. Bacterial σ factors, therefore, are posited to be most similar to a 4-CLR/HTH PIF in overall domain structure, and conserved archaeal TFB CLR/HTH repeats are posited to be most similar to PIF CLR/HTH domains in sequence. It is posited that bacteria and archaea are early radiations from LUCA that diverged largely because of their fundamental differences in GTFs and, therefore, their alternate approaches to genome interpretation. Bacteria became committed to σ factors for promoter recognition, and RNAP recruitment is tightly coupled to σ factor binding to core RNAP in bacteria. Co-evolution of bacterial σ factors and RNAP, therefore, is proposed to have driven streamlining to a simpler RNAP subunit structure (α2ββ’ω). Evolution of the bacterial promoters is posited to be driven by co-evolution with interacting σ CLR/HTH domains. Archaeal TFB is proposed to have lost 2-CLR/HTH domains from a 4-CLR/HTH PIF and gained a N-terminal Zn ribbon and B-reader region. In archaea, cooperation of TFB with TBP is posited to have allowed for the losses of 2-CLR/HTH domains from the PIF and the gain of the N-terminal Zn ribbon and B-reader. In initiation mechanisms, TFB-TBP GTFs appear less strongly coupled to archaeal RNAP than bacterial σ factors and bacterial RNAP. This difference in GTFs may have allowed archaea to retain a more ornate RNAP subunit structure than observed in bacteria.Figure 7.

Bottom Line: TFIIB and TFB each have two-five-helix cyclin-like repeats (CLRs) that include a C-terminal helix-turn-helix (HTH) motif (CLR/HTH domains).Four homologous HTH motifs are present in bacterial σ factors that are relics of CLR/HTH domains.Sequence similarities clarify models for σ factor and TFB/TFIIB evolution and function and suggest models for promoter evolution.

View Article: PubMed Central - PubMed

Affiliation: a Department of Biochemistry and Molecular Biology ; Michigan State University ; E. Lansing , MI USA.

ABSTRACT
Structural comparisons of initiating RNA polymerase complexes and structure-based amino acid sequence alignments of general transcription initiation factors (eukaryotic TFIIB, archaeal TFB and bacterial σ factors) show that these proteins are homologs. TFIIB and TFB each have two-five-helix cyclin-like repeats (CLRs) that include a C-terminal helix-turn-helix (HTH) motif (CLR/HTH domains). Four homologous HTH motifs are present in bacterial σ factors that are relics of CLR/HTH domains. Sequence similarities clarify models for σ factor and TFB/TFIIB evolution and function and suggest models for promoter evolution. Commitment to alternate modes for transcription initiation appears to be a major driver of the divergence of bacteria and archaea.

Show MeSH