Evolution of Eukaryotic RNA Polymerases

Abstract

Ribonucleic acid (RNA) polymerases are responsible for the transcription of deoxyribonucleic acid (DNA) into RNA. The number of protein subunits making up these enzymes has increased during evolution from 5 in Eubacteria to 12 in the common ancestor of Archaea and eukaryotes. Eukaryotes have three RNA polymerases, each transcribing a particular subset of genes. RNA polymerase I transcribes ribosomal RNA genes, RNA polymerase II transcribes messenger RNA genes and RNA polymerase III transcribes 5S and transfer RNA genes. Although RNA polymerase II is still made up of 12 subunits, the number of subunits has increased to 14 in RNA polymerase I and to 17 in RNA polymerase III. These new subunits originated from the permanent recruitment of pre‚Äźexisting general transcription factors. Interestingly, the evolution of the three eukaryotic RNA polymerases has been affected not only by adaptive forces but also by the nonadaptive forces due to the concerted evolution of the genes they transcribe.

Key Concepts:

  • The larger numbers of protein subunits found in RNA polymerases I and III, relative to RNA polymerase II, are due to the permanent recruitment of general transcription factors.

  • The three universal eukaryotic RNA polymerases have specific functional differences near their respective active sites.

  • During evolution, the three eukaryotic RNA polymerase have been selected to better perform their specific tasks.

  • The rate of evolution of RNA polymerases is proportional to the amount of homogenisation (concerted evolution) experienced by the genes they transcribe.

  • Nonadaptive processes therefore also affect the rate of evolution of RNA polymerase genes.

Keywords: RNA polymerase; general transcription factors; eukaryotic; evolution; concerted evolution; functional divergence; transcription; gene conversion; unequal crossingover

Figure 1.

Schematic representation of the evolution of the main cellular RNA polymerases. The five subunits present in eubacteria are coloured light blue, whereas the seven subunits that were added to form the ancestral core RNA polymerase are coloured dark blue. The other subunits present in some enzymes are coloured green, red and yellow, as indicated. The phylogeny depicted, with eubacteria being the sister group of Archaea and eukaryotes and with RNAPI being the sister group of RNAPII and III, is generally accepted as being most likely. The different branch lengths of RNAPI, II and III also represent their relative amino acid substitution rates.

Figure 2.

Schematic representation of types I and II sites in protein sequences. Type I sites are amino acid sites which are variable in one polymerase (here, RNAP I) but conserved in the other two polymerases. Type II sites which are amino acid sites are conserved but different between polymerases.

Figure 3.

Schematic representation of the expected and observed patterns of nucleotide variation between multigene family members. The nucleotides indicated are those that differ between genes and species. If duplicated genes evolve independently, we expect that each gene will acquire different nucleotides both within and between species. However, we observe that the genes of different species have different nucleotides, whereas the genes within species all share the same nucleotide substitutions. This indicates that, within a species, genes evolve in concert.

Figure 4.

Schematic representation of concerted evolution by unequal crossingover. Different numbers indicate different genes. Here, a single cycle of unequal crossingover either between sister chromatids or homologous chromatids, produces chromosomes with more homogenous duplicated copies, either because the number of genes is reduced or because given genes (here, gene 2) are duplicated.

Figure 5.

Schematic representation of concerted evolution by gene conversion between γ‐globin genes. A and B represent the two human chromosome 11 regions containing the two γ‐globin genes (γ1 and γ2). Coloured and black boxes represent the exons and white boxes represent the introns. Here, a single conversion has converted roughly 1000 bp of the γ2‐globin gene to the sequence of the γ1‐globin gene (black arrow). The numbers of nucleotide differences are given for each 100 bp intervals. Differences between the γ2 alleles are indicated in yellow and those between the γ1‐ and γ2‐globin genes are indicated in green. This figure is based on the data published by Slightom et al. .

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How to Cite close
Drouin, Guy, and Carter, Robert(Sep 2010) Evolution of Eukaryotic RNA Polymerases. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0022872]