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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 6. The Old and New Testaments of molecular biology describing evolution of multi-subunit RNAPs from the RNA-protein world to LUCA and branching to LECA. The red arrows indicate that LUCA may have eaten the RNA-protein world and that more modern organisms may have devoured and/or out competed LUCA. According to this description, eubacteria and archaea maintain similar features to LUCA. Higher order complexity in eukaryotic gene regulation developed around the CTD of RNAP II and chromatin, and these processes are posited to be strongly co-evolved.
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Figure 6: Figure 6. The Old and New Testaments of molecular biology describing evolution of multi-subunit RNAPs from the RNA-protein world to LUCA and branching to LECA. The red arrows indicate that LUCA may have eaten the RNA-protein world and that more modern organisms may have devoured and/or out competed LUCA. According to this description, eubacteria and archaea maintain similar features to LUCA. Higher order complexity in eukaryotic gene regulation developed around the CTD of RNAP II and chromatin, and these processes are posited to be strongly co-evolved.

Mentions: At the C-terminal end of its β’ type subunit (named Rpb1), RNAP II has an unusual repeat structure termed the CTD for carboxy terminal domain.9-15 In humans and other vertebrates, the consensus sequence YSPTSPS (Y = tyrosine; S = serine; P = proline; T = threonine) is repeated 52 times (some repeats are non-consensus; see below). The CTD repeat is the focus for high innovation in mRNA regulation in the eukaryotic lineage and has allowed eukarya to develop into myriad complex, multi-cellular organisms. This is the New Testament of evolution of life on earth from the perspective of RNAP structure, function, evolution and associated gene regulation (Fig. 6).16


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 6. The Old and New Testaments of molecular biology describing evolution of multi-subunit RNAPs from the RNA-protein world to LUCA and branching to LECA. The red arrows indicate that LUCA may have eaten the RNA-protein world and that more modern organisms may have devoured and/or out competed LUCA. According to this description, eubacteria and archaea maintain similar features to LUCA. Higher order complexity in eukaryotic gene regulation developed around the CTD of RNAP II and chromatin, and these processes are posited to be strongly co-evolved.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Figure 6: Figure 6. The Old and New Testaments of molecular biology describing evolution of multi-subunit RNAPs from the RNA-protein world to LUCA and branching to LECA. The red arrows indicate that LUCA may have eaten the RNA-protein world and that more modern organisms may have devoured and/or out competed LUCA. According to this description, eubacteria and archaea maintain similar features to LUCA. Higher order complexity in eukaryotic gene regulation developed around the CTD of RNAP II and chromatin, and these processes are posited to be strongly co-evolved.
Mentions: At the C-terminal end of its β’ type subunit (named Rpb1), RNAP II has an unusual repeat structure termed the CTD for carboxy terminal domain.9-15 In humans and other vertebrates, the consensus sequence YSPTSPS (Y = tyrosine; S = serine; P = proline; T = threonine) is repeated 52 times (some repeats are non-consensus; see below). The CTD repeat is the focus for high innovation in mRNA regulation in the eukaryotic lineage and has allowed eukarya to develop into myriad complex, multi-cellular organisms. This is the New Testament of evolution of life on earth from the perspective of RNAP structure, function, evolution and associated gene regulation (Fig. 6).16

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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