Journal Article

Evolution of multisubunit RNA polymerases in the three domains of life

Grohmann, Dina, Werner, Finn

2011

Overview

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. RNA polymerase is an ancient enzyme that is present in all cellular life. Werner and Grohmann provide an evolutionary view of this enzyme by describing the differences and similarities in the three domains of life, and propose a hypothesis for the evolution of transcriptional regulation. 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.

• Publisher: Nature Publishing Group UK,Nature Publishing Group
• Subject: 631/181/735 / 631/326 / 631/337/572 / 631/45/535 / Amino acids / Archaea - classification / Archaea - enzymology / Bacteria / Bacteria - classification / Bacteria - enzymology / Biomedical and Life Sciences / Conserved Sequence / DNA-Directed RNA Polymerases - genetics / Enzymes / Evolution / Evolution, Molecular / Gene expression / Gene Expression Regulation, Enzymologic / Genes / Genetic aspects / Hypotheses / Infectious Diseases / Life Sciences / Medical Microbiology / Microbiology / Microorganisms / Models, Molecular / Parasitology / Phylogeny / Physiological aspects / Protein Structure, Quaternary / Proteins / review-article / RNA polymerase / RNA polymerases / Saccharomyces cerevisiae - classification / Saccharomyces cerevisiae - enzymology / Transcription factors / Transcriptional Elongation Factors - chemistry / Virology