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Evolution of multisubunit RNA polymerases in the three domains of life

Nature Reviews Microbiology volume 9, pages 85–98 (2011)Cite this article

Subjects

Key Points

  • Multisubunit RNA polymerases (RNAPs) from the three domains of life are evolutionarily related, and this is reflected in the sequence and structure of their subunits, their interactions with transcription factors and their molecular mechanisms of action.

  • RNAP subunits contribute in distinct ways to enzyme function and facilitate assembly, catalysis, interaction with DNA and RNA, and regulation of RNAP activity.

  • The Rpo4–Rpo7 subunits of archaeal RNAP and the RPB4–RPB7 subunits of eukaryotic RNAPs constitute the stalk, which modulates the elongation and termination properties of these RNAPs but is not conserved in bacteria.

  • RNAP function is dependent on and regulated by exogenous transcription factors, some of which are universally conserved in evolution.

  • Transcription factors that enable transcription initiation in bacteria (σ-factors) and archaea and eukaryotes (TATA box-binding protein (TBP) and TFIIB) are not homologous.

  • Transcript cleavage factors in bacteria (GreB) and archaea and eukaryotes (TFIIS) are not homologous.

  • Non-homologous transcription factors can adapt a similar structure and can therefore interact with and regulate their cognate RNAPs using closely related molecular mechanisms.

  • NusG is the only RNAP-associated transcription factor that is universally conserved in evolution (NusG in bacteria, Spt5 in archaea and SPT5 in eukaryotes), indicating that regulation of transcription during elongation predated regulation of transcription initiation.

Abstract

RNA polymerases (RNAPs) carry out transcription in all living organisms. All multisubunit RNAPs are derived from a common ancestor, a fact that becomes apparent from their amino acid sequence, subunit composition, structure, function and molecular mechanisms. Despite the similarity of these complexes, the organisms that depend on them are extremely diverse, ranging from microorganisms to humans. Recent findings about the molecular and functional architecture of RNAPs has given us intriguing insights into their evolution and how their activities are harnessed by homologous and analogous basal factors during the transcription cycle. We provide an overview of the evolutionary conservation of and differences between the multisubunit polymerases in the three domains of life, and introduce the 'elongation first' hypothesis for the evolution of transcriptional regulation.

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Figure 1: The transcription cycle of the archaeal RNA polymerase.
Figure 2: Overall architecture of RNA polymerase.
Figure 3: Important structural and functional features of multisubunit RNA polymerases.
Figure 4: Transcription initiation — holo-RNA polymerase structures from bacteria and eukaryotes.
Figure 5: The architecture of the transcription elongation complex.
Figure 6: The transcript cleavage complex.
Figure 7: Universal evolutionary conservation of the elongation factor Spt4–Spt5 and NusG.
Figure 8: Emergence of transcription initiation factors in the three domains of life.

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Acknowledgements

We thank S. Gribaldo from the Institute Pasteur, Paris, France, for stimulating discussions on evolution and the inspiration for figure 8. We also thank K. S. Murakami for sharing unpublished results.

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  1. Division of Biosciences, RNA Polymerase Laboratory, Institute for Structural and Molecular Biology, University College London, Darwin Building, Gower Street, WC1E 6BT, London, UK

    Finn Werner & Dina Grohmann

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Correspondence to Finn Werner.

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Glossary

Last universal common ancestor

The last common ancestor of all three contemporary domains of life.

Transcription factor

A protein that transiently interacts with RNA polymerase, modulates its protein-, DNA- and RNA-binding or catalytic properties, and thereby regulates transcription.

Convergent evolution

The acquisition of the same trait in unrelated lineages.

Homologous

Pertaining to genes: derived from the same ancestor.

RNAP clamp

A flexible RNA polymerase (RNAP) domain that is predicted to move over the DNA-binding channel during open-complex formation.

Bridge and trigger helices

Flexible RNA polymerase motifs that unfold and refold repeatedly during nucleotide addition and translocation.

Double-psi β-barrel motif

A structural module in the two largest RNA polymerase subunits that reveals the common origin of these subunits and constitutes the active site.

Ribozyme

An enzyme made exclusively of RNA.

RNAi RNAP

An RNA polymerase (RNAP) involved in RNA interference (RNAi); it produces double-stranded RNA from aberrant single-stranded RNA templates to trigger RNAi.

Open-complex formation

The structural transition of RNA polymerase concomitant with the melting of DNA strands during initiation.

TATA box-binding protein

One of the two minimal transcription factors required for initiation by archaeal RNA polymerase (RNAP) and eukaryotic RNAPII. It binds to a sequence recognition motif in promoters that is called the TATA element or TATA box.

TFIIB

The second of the two minimal transcription factors required for initiation by archaeal RNA polymerase (RNAP) and eukaryotic RNAPII.

σ-factor

A bacterial transcription initiation factor that binds specific sequences in the promoter. Each σ-factor regulates the transcription of a specific set of genes.

−10 and −35 elements

Key sequence motifs of bacterial promoters that are recognized by the transcription factor σ70. Promoter strength is in part regulated by the strength of the interaction between σ70 and these elements.

Zn-ribbon domain

A domain found in many transcription factors, including TFIIB, TFIIS and TFIIE in eukaryotes (and TFB, TFS and TFE, respectively, in archaea). The aminoterminal Zn-ribbon domain of TFIIB and TFB interacts with the RNA polymerase (RNAP) dock domain and is important for efficient RNAP recruitment.

Paralogous

Pertaining to genes: separated by a gene duplication event.

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Werner, F., Grohmann, D. Evolution of multisubunit RNA polymerases in the three domains of life. Nat Rev Microbiol 9, 85–98 (2011). https://doi.org/10.1038/nrmicro2507

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