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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 8. Gene regulatory network (GRN) structures (blue arrows) and co-evolved processes (green arrows) for (A) eukaryotes and (B) eubacteria.
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Figure 8: Figure 8. Gene regulatory network (GRN) structures (blue arrows) and co-evolved processes (green arrows) for (A) eukaryotes and (B) eubacteria.

Mentions: Nuanced gene regulation in the eukaryotic lineage has been developed as a series of seemingly endless add-ons and adaptations: repression, anti-repression and anti-anti-repression, etc. Notably, many or most gene activation mechanisms in eukarya appear to be anti-repression mechanisms. Many or most key evolutionary RNAP II add-ons integrate with the CTD, which can be viewed as somewhat similar to, but somewhat more than, a global positioning system to monitor, locate and regulate progression of RNAP II through and beyond the transcription cycle of pre-initiation complex assembly, initiation, promoter escape, capping, promoter-proximal pausing, elongation, splicing, termination, RNAP II recycling, mRNA folding and decoration, and mRNA export and licensing for translation (Fig. 7).13-15,20 CTD-mediated control also allows sophisticated communication between the transcription apparatus and chromatin structure, layering a very complex and dynamic landscape on command and control. Many large and seemingly overly complex multi-subunit complexes, including many enzymes for protein modification/de-modification, interact with the CTD, RNAP II and/or chromatin to regulate the processes of gene readout. Such nuance could not develop primarily around sequence-specific DNA binding transcription factors, as in eubacteria (Fig. 8).6 Also, eubacteria and archaea utilize only a single RNAP for all RNA synthesis, so these organisms cannot as easily protect ribosomal, transfer and regulatory RNA synthesis from collateral damage resulting from otherwise disruptive modifications in gene expression that affect mRNA synthesis. The eukaryotic RNAP II apparatus and gene regulatory network, therefore, resemble a robustified Rube Goldberg device of endless add-ons, strengthened by many supporting pathways. In the eukaryote line, life is not robust because of elegant design or refinement; life is robust because of functional redundancy in add-ons.


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 8. Gene regulatory network (GRN) structures (blue arrows) and co-evolved processes (green arrows) for (A) eukaryotes and (B) eubacteria.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Figure 8: Figure 8. Gene regulatory network (GRN) structures (blue arrows) and co-evolved processes (green arrows) for (A) eukaryotes and (B) eubacteria.
Mentions: Nuanced gene regulation in the eukaryotic lineage has been developed as a series of seemingly endless add-ons and adaptations: repression, anti-repression and anti-anti-repression, etc. Notably, many or most gene activation mechanisms in eukarya appear to be anti-repression mechanisms. Many or most key evolutionary RNAP II add-ons integrate with the CTD, which can be viewed as somewhat similar to, but somewhat more than, a global positioning system to monitor, locate and regulate progression of RNAP II through and beyond the transcription cycle of pre-initiation complex assembly, initiation, promoter escape, capping, promoter-proximal pausing, elongation, splicing, termination, RNAP II recycling, mRNA folding and decoration, and mRNA export and licensing for translation (Fig. 7).13-15,20 CTD-mediated control also allows sophisticated communication between the transcription apparatus and chromatin structure, layering a very complex and dynamic landscape on command and control. Many large and seemingly overly complex multi-subunit complexes, including many enzymes for protein modification/de-modification, interact with the CTD, RNAP II and/or chromatin to regulate the processes of gene readout. Such nuance could not develop primarily around sequence-specific DNA binding transcription factors, as in eubacteria (Fig. 8).6 Also, eubacteria and archaea utilize only a single RNAP for all RNA synthesis, so these organisms cannot as easily protect ribosomal, transfer and regulatory RNA synthesis from collateral damage resulting from otherwise disruptive modifications in gene expression that affect mRNA synthesis. The eukaryotic RNAP II apparatus and gene regulatory network, therefore, resemble a robustified Rube Goldberg device of endless add-ons, strengthened by many supporting pathways. In the eukaryote line, life is not robust because of elegant design or refinement; life is robust because of functional redundancy in add-ons.

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