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The Old and New Testaments of gene regulation. Evolution of multi-subunit RNA polymerases and co-evolution of eukaryote complexity with the RNAP II CTD.

Burton ZF - Transcription (2014)

Bottom Line: The Old Testament: at their active site, one class of eukaryotic interfering RNAP and ubiquitous multi-subunit RNAPs each have two-double psi β barrel (DPBB) motifs (a distinct pattern for compact 6-β sheet barrels).Analysis of RNAP core protein motifs, therefore, indicates that RNAP evolution can be traced from the RNA-protein world to LUCA (the last universal common ancestor) branching to LECA (the last eukaryotic common ancestor) and to the present day, spanning about 4 billion years.The New Testament: in the eukaryotic lineage, I posit that splitting RNAP functions into RNAPs I, II and III and innovations developed around the CTD heptad repeat of RNAP II and the extensive CTD interactome helps to describe how greater structural, cell cycle, epigenetic and signaling complexity co-evolved in eukaryotes relative to eubacteria and archaea.

View Article: PubMed Central - PubMed

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

ABSTRACT
I relate a story of genesis told from the point of view of multi-subunit RNA polymerases (RNAPs) including an Old Testament (core RNAP motifs in all cellular life) and a New Testament (the RNAP II heptad repeat carboxy terminal domain (CTD) and CTD interactome in eukarya). The Old Testament: at their active site, one class of eukaryotic interfering RNAP and ubiquitous multi-subunit RNAPs each have two-double psi β barrel (DPBB) motifs (a distinct pattern for compact 6-β sheet barrels). Between β sheets 2 and 3 of the β subunit type DPBB of all multi-subunit RNAPs is a sandwich barrel hybrid motif (SBHM) that interacts with conserved initiation and elongation factors required to utilize a DNA template. Analysis of RNAP core protein motifs, therefore, indicates that RNAP evolution can be traced from the RNA-protein world to LUCA (the last universal common ancestor) branching to LECA (the last eukaryotic common ancestor) and to the present day, spanning about 4 billion years. The New Testament: in the eukaryotic lineage, I posit that splitting RNAP functions into RNAPs I, II and III and innovations developed around the CTD heptad repeat of RNAP II and the extensive CTD interactome helps to describe how greater structural, cell cycle, epigenetic and signaling complexity co-evolved in eukaryotes relative to eubacteria and archaea.

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Figure 3. A SBHM necessary to utilize a DNA template. The SBHM is inserted between β2 and β3 of the β subunit type DPBB and is a landing pad for conserved initiation and elongation factors in the three domains of cellular life: eubacteria (red), archaea (cyan), eukarya (purple). Coloring of the DPBBs is as in Figure 2.
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Figure 3: Figure 3. A SBHM necessary to utilize a DNA template. The SBHM is inserted between β2 and β3 of the β subunit type DPBB and is a landing pad for conserved initiation and elongation factors in the three domains of cellular life: eubacteria (red), archaea (cyan), eukarya (purple). Coloring of the DPBBs is as in Figure 2.

Mentions: The sandwich barrel hybrid motif (SBHM) embedded between the 2nd and 3rd β sheets of the β subunit type DPBB provides an interaction surface for initiation and elongation factors that are conserved in the three domains of life (Fig. 3).6 In eubacteria, sigma factors allow specific initiation from a DNA template. Sigma factors are related to TFB in archaea and TFIIB (RNAP II) and Brf-1 (RNAP III) in eukarya, factors that aid accurate initiation (two helix-turn-helix motifs are conserved) (http://jivarahasya.blogspot.com/).6 In eubacteria, during RNA polymer elongation, NusG factors bump sigma off of the SBHM. Remarkably, NusG relates to Spt5 in archaea and eukarya. Therefore, the machinery that allows use of a DNA template for initiation and elongation of transcription and its SBHM interaction surface on RNAP are conserved in evolution. This is remarkable preservation of interdependent and interacting protein structures and functions (Fig. 3). Figure 4 shows that yeast (Sc) RNAP II and eubacterial Thermus thermophilus (Tt) RNAP are highly conserved in core motifs, demonstrating their kinship.


The Old and New Testaments of gene regulation. Evolution of multi-subunit RNA polymerases and co-evolution of eukaryote complexity with the RNAP II CTD.

Burton ZF - Transcription (2014)

Figure 3. A SBHM necessary to utilize a DNA template. The SBHM is inserted between β2 and β3 of the β subunit type DPBB and is a landing pad for conserved initiation and elongation factors in the three domains of cellular life: eubacteria (red), archaea (cyan), eukarya (purple). Coloring of the DPBBs is as in Figure 2.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4215175&req=5

Figure 3: Figure 3. A SBHM necessary to utilize a DNA template. The SBHM is inserted between β2 and β3 of the β subunit type DPBB and is a landing pad for conserved initiation and elongation factors in the three domains of cellular life: eubacteria (red), archaea (cyan), eukarya (purple). Coloring of the DPBBs is as in Figure 2.
Mentions: The sandwich barrel hybrid motif (SBHM) embedded between the 2nd and 3rd β sheets of the β subunit type DPBB provides an interaction surface for initiation and elongation factors that are conserved in the three domains of life (Fig. 3).6 In eubacteria, sigma factors allow specific initiation from a DNA template. Sigma factors are related to TFB in archaea and TFIIB (RNAP II) and Brf-1 (RNAP III) in eukarya, factors that aid accurate initiation (two helix-turn-helix motifs are conserved) (http://jivarahasya.blogspot.com/).6 In eubacteria, during RNA polymer elongation, NusG factors bump sigma off of the SBHM. Remarkably, NusG relates to Spt5 in archaea and eukarya. Therefore, the machinery that allows use of a DNA template for initiation and elongation of transcription and its SBHM interaction surface on RNAP are conserved in evolution. This is remarkable preservation of interdependent and interacting protein structures and functions (Fig. 3). Figure 4 shows that yeast (Sc) RNAP II and eubacterial Thermus thermophilus (Tt) RNAP are highly conserved in core motifs, demonstrating their kinship.

Bottom Line: The Old Testament: at their active site, one class of eukaryotic interfering RNAP and ubiquitous multi-subunit RNAPs each have two-double psi β barrel (DPBB) motifs (a distinct pattern for compact 6-β sheet barrels).Analysis of RNAP core protein motifs, therefore, indicates that RNAP evolution can be traced from the RNA-protein world to LUCA (the last universal common ancestor) branching to LECA (the last eukaryotic common ancestor) and to the present day, spanning about 4 billion years.The New Testament: in the eukaryotic lineage, I posit that splitting RNAP functions into RNAPs I, II and III and innovations developed around the CTD heptad repeat of RNAP II and the extensive CTD interactome helps to describe how greater structural, cell cycle, epigenetic and signaling complexity co-evolved in eukaryotes relative to eubacteria and archaea.

View Article: PubMed Central - PubMed

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

ABSTRACT
I relate a story of genesis told from the point of view of multi-subunit RNA polymerases (RNAPs) including an Old Testament (core RNAP motifs in all cellular life) and a New Testament (the RNAP II heptad repeat carboxy terminal domain (CTD) and CTD interactome in eukarya). The Old Testament: at their active site, one class of eukaryotic interfering RNAP and ubiquitous multi-subunit RNAPs each have two-double psi β barrel (DPBB) motifs (a distinct pattern for compact 6-β sheet barrels). Between β sheets 2 and 3 of the β subunit type DPBB of all multi-subunit RNAPs is a sandwich barrel hybrid motif (SBHM) that interacts with conserved initiation and elongation factors required to utilize a DNA template. Analysis of RNAP core protein motifs, therefore, indicates that RNAP evolution can be traced from the RNA-protein world to LUCA (the last universal common ancestor) branching to LECA (the last eukaryotic common ancestor) and to the present day, spanning about 4 billion years. The New Testament: in the eukaryotic lineage, I posit that splitting RNAP functions into RNAPs I, II and III and innovations developed around the CTD heptad repeat of RNAP II and the extensive CTD interactome helps to describe how greater structural, cell cycle, epigenetic and signaling complexity co-evolved in eukaryotes relative to eubacteria and archaea.

Show MeSH