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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 early evolution of promoters based on a 4-CLR/HTH PIF. A) a 4-CLR/HTH PIF for initiation on a bidirectional primordial promoter. B) a 4-CLR/HTH PIF for initiation on a unidirectional primordial promoter with an anchor DNA sequence. The C-terminal CLR/HTH domain is shaded red to indicate that it binds anchor DNA. Bacterial -35 and archaeal/eukaryotic BREup DNA elements are posited to be relics of primordial anchor DNA sequences. TATAAT (Pribnow box) and TATAAAAG boxes are posited to be derived from AT-rich primordial promoter sequences. CLR/HTH domains are posited to separate from the upstream anchor in the downstream direction as the bubble opens.
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f0006: A model for early evolution of promoters based on a 4-CLR/HTH PIF. A) a 4-CLR/HTH PIF for initiation on a bidirectional primordial promoter. B) a 4-CLR/HTH PIF for initiation on a unidirectional primordial promoter with an anchor DNA sequence. The C-terminal CLR/HTH domain is shaded red to indicate that it binds anchor DNA. Bacterial -35 and archaeal/eukaryotic BREup DNA elements are posited to be relics of primordial anchor DNA sequences. TATAAT (Pribnow box) and TATAAAAG boxes are posited to be derived from AT-rich primordial promoter sequences. CLR/HTH domains are posited to separate from the upstream anchor in the downstream direction as the bubble opens.

Mentions: Homology among bacterial σ factors and archaeal/eukaryotic TFB/TFIIB suggests a simple model for a primordial initiation factor (PIF) and for promoter evolution based on a 4-CLR/HTH PIF at about the time of LUCA (Fig. 6). The 4-CLR/HTH PIF is posited to have arisen by duplication of a single CLR/HTH domain followed by subsequent duplication of the 2-CLR/HTH domains to form the 4-CLR/HTH factor. Because of the evolutionary path, σ CLR/HTH1.2 and CLR/HTH3.0-3.1 are most similar to TFB CLR/HTH1 (odd numbered repeats are most similar among σ and TFB), and σ CLR/HTH2.1-2.4 and CLR/HTH4.1-4.2 are most similar to TFB CLR/HTH2 (even numbered repeats are most similar among σ and TFB). In Figure 6A, a model is shown for a 4-CLR/HTH domain PIF supporting bi-directional initiation on an AT-rich negatively supercoiled primordial promoter. A 4-CLR/HTH domain PIF is hypothesized because it is difficult to imagine a 2-CLR/HTH domain PIF, resembling TFB/TFIIB, opening even negatively supercoiled AT-rich DNA without cooperation of additional GTFs. Because of powerful selection for promoter directionality, anchor DNA sequences are posited to have rapidly evolved near the upstream edge of the AT-rich segment (Fig. 6B). Bacterial -35 regions and archaeal/eukaryotic BREup are posited to be relics of primordial anchor DNA sequences (Figs. 3, 5 and 6B). The AT-rich primordial promoter is posited to have been compressed in evolution into the bacterial Pribnow box (TATAAT) and the archaeal/eukaryotic TATAAAAG box through co-evolution with RNAP and GTFs. According to this simple working model, promoters have not changed very much since the advent of DNA genomes at about the time of LUCA.Figure 6.


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

Burton SP, Burton ZF - Transcription (2014)

A model for early evolution of promoters based on a 4-CLR/HTH PIF. A) a 4-CLR/HTH PIF for initiation on a bidirectional primordial promoter. B) a 4-CLR/HTH PIF for initiation on a unidirectional primordial promoter with an anchor DNA sequence. The C-terminal CLR/HTH domain is shaded red to indicate that it binds anchor DNA. Bacterial -35 and archaeal/eukaryotic BREup DNA elements are posited to be relics of primordial anchor DNA sequences. TATAAT (Pribnow box) and TATAAAAG boxes are posited to be derived from AT-rich primordial promoter sequences. CLR/HTH domains are posited to separate from the upstream anchor in the downstream direction as the bubble opens.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

f0006: A model for early evolution of promoters based on a 4-CLR/HTH PIF. A) a 4-CLR/HTH PIF for initiation on a bidirectional primordial promoter. B) a 4-CLR/HTH PIF for initiation on a unidirectional primordial promoter with an anchor DNA sequence. The C-terminal CLR/HTH domain is shaded red to indicate that it binds anchor DNA. Bacterial -35 and archaeal/eukaryotic BREup DNA elements are posited to be relics of primordial anchor DNA sequences. TATAAT (Pribnow box) and TATAAAAG boxes are posited to be derived from AT-rich primordial promoter sequences. CLR/HTH domains are posited to separate from the upstream anchor in the downstream direction as the bubble opens.
Mentions: Homology among bacterial σ factors and archaeal/eukaryotic TFB/TFIIB suggests a simple model for a primordial initiation factor (PIF) and for promoter evolution based on a 4-CLR/HTH PIF at about the time of LUCA (Fig. 6). The 4-CLR/HTH PIF is posited to have arisen by duplication of a single CLR/HTH domain followed by subsequent duplication of the 2-CLR/HTH domains to form the 4-CLR/HTH factor. Because of the evolutionary path, σ CLR/HTH1.2 and CLR/HTH3.0-3.1 are most similar to TFB CLR/HTH1 (odd numbered repeats are most similar among σ and TFB), and σ CLR/HTH2.1-2.4 and CLR/HTH4.1-4.2 are most similar to TFB CLR/HTH2 (even numbered repeats are most similar among σ and TFB). In Figure 6A, a model is shown for a 4-CLR/HTH domain PIF supporting bi-directional initiation on an AT-rich negatively supercoiled primordial promoter. A 4-CLR/HTH domain PIF is hypothesized because it is difficult to imagine a 2-CLR/HTH domain PIF, resembling TFB/TFIIB, opening even negatively supercoiled AT-rich DNA without cooperation of additional GTFs. Because of powerful selection for promoter directionality, anchor DNA sequences are posited to have rapidly evolved near the upstream edge of the AT-rich segment (Fig. 6B). Bacterial -35 regions and archaeal/eukaryotic BREup are posited to be relics of primordial anchor DNA sequences (Figs. 3, 5 and 6B). The AT-rich primordial promoter is posited to have been compressed in evolution into the bacterial Pribnow box (TATAAT) and the archaeal/eukaryotic TATAAAAG box through co-evolution with RNAP and GTFs. According to this simple working model, promoters have not changed very much since the advent of DNA genomes at about the time of LUCA.Figure 6.

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