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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 7. The CTD of RNAP II is partly analogous to a GPS for the transcription cycle. The RNAP II transcription cycle, which is centered on the CTD and its interactome, appears co-evolved with the eukaryotic cell cycle. The sequence of the 52 heptad repeat human CTD is shown. Non-consensus heptads are indicated by red letters.
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Figure 7: Figure 7. The CTD of RNAP II is partly analogous to a GPS for the transcription cycle. The RNAP II transcription cycle, which is centered on the CTD and its interactome, appears co-evolved with the eukaryotic cell cycle. The sequence of the 52 heptad repeat human CTD is shown. Non-consensus heptads are indicated by red letters.

Mentions: Yang and Stiller17 have recently completed a comprehensive analysis of the evolution of the RNAP II CTD. The CTD appears to be as old as the eukaryotic lineage, so the last eukaryotic common ancestor (LECA; ~1.6 to 2.1 bya) is likely to have had RNAP I, II and III and a multiple heptad (seven amino acid) repeat CTD on RNAP II. Initially, the CTD may have provided a scaffold for binding the spliceosome for co-transcriptional removal of introns from heterogeneous nuclear RNAs.17-19 With time, many additional functions have attached to the CTD scaffold (Fig. 7). All eukaryotes appear to have a CTD or a CTD remnant on RNAP II. In evolution of eukaryotic taxa, the CTD has been repeatedly amplified, partly or completely degenerated in sequence, in some organisms, and, in some cases, re-amplified as a heptad repeat. Just N-terminal to the CTD is a linker sequence that is rich in SP and may represent ancient degeneration of heptad repeat sequences. Interestingly, within the fungi and red algae, increased multi-cellular complexity appears to correlate with a more highly degenerate CTD, indicating that modification and degeneration of CTD repeats can be linked to co-evolution of interacting factors to support specific transcriptional functions and differentiation programs. By contrast, complex animals and plants remain fully dependent on a CTD that includes many consensus heptad repeats, indicating that, in these organisms, although some repeats can degenerate or adapt to specific interactions (as in fungi and red algae), the most complex CTD interactomes also require maintenance of a consensus heptad repeat interaction scaffold.17


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 7. The CTD of RNAP II is partly analogous to a GPS for the transcription cycle. The RNAP II transcription cycle, which is centered on the CTD and its interactome, appears co-evolved with the eukaryotic cell cycle. The sequence of the 52 heptad repeat human CTD is shown. Non-consensus heptads are indicated by red letters.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Figure 7: Figure 7. The CTD of RNAP II is partly analogous to a GPS for the transcription cycle. The RNAP II transcription cycle, which is centered on the CTD and its interactome, appears co-evolved with the eukaryotic cell cycle. The sequence of the 52 heptad repeat human CTD is shown. Non-consensus heptads are indicated by red letters.
Mentions: Yang and Stiller17 have recently completed a comprehensive analysis of the evolution of the RNAP II CTD. The CTD appears to be as old as the eukaryotic lineage, so the last eukaryotic common ancestor (LECA; ~1.6 to 2.1 bya) is likely to have had RNAP I, II and III and a multiple heptad (seven amino acid) repeat CTD on RNAP II. Initially, the CTD may have provided a scaffold for binding the spliceosome for co-transcriptional removal of introns from heterogeneous nuclear RNAs.17-19 With time, many additional functions have attached to the CTD scaffold (Fig. 7). All eukaryotes appear to have a CTD or a CTD remnant on RNAP II. In evolution of eukaryotic taxa, the CTD has been repeatedly amplified, partly or completely degenerated in sequence, in some organisms, and, in some cases, re-amplified as a heptad repeat. Just N-terminal to the CTD is a linker sequence that is rich in SP and may represent ancient degeneration of heptad repeat sequences. Interestingly, within the fungi and red algae, increased multi-cellular complexity appears to correlate with a more highly degenerate CTD, indicating that modification and degeneration of CTD repeats can be linked to co-evolution of interacting factors to support specific transcriptional functions and differentiation programs. By contrast, complex animals and plants remain fully dependent on a CTD that includes many consensus heptad repeats, indicating that, in these organisms, although some repeats can degenerate or adapt to specific interactions (as in fungi and red algae), the most complex CTD interactomes also require maintenance of a consensus heptad repeat interaction scaffold.17

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