Evolutionary diversity and taxon-specific modifications of the RNA polymerase II C-terminal domain

Abstract

In model eukaryotes, the C-terminal domain (CTD) of the largest subunit of DNA-dependent RNA polymerase II (RNAP II) is composed of tandemly repeated heptads with the consensus sequence YSPTSPS. The core motif and tandem structure generally are conserved across model taxa, including animals, yeasts and higher plants. Broader investigations revealed that CTDs of many organisms deviate substantially from this canonical structure; however, limited sampling made it difficult to determine whether disordered sequences reflect the CTD's ancestral state or degeneration from ancestral repetitive structures. Therefore, we undertook, to our knowledge, the broadest investigation to date of the evolution of the RNAP II CTD across eukaryotic diversity. Our results indicate that a tandemly repeated CTD existed in the ancestors of each major taxon, and that degeneration and reinvention of this ordered structure are common features of CTD evolution. Lineage-specific CTD modifications appear to be associated with greater developmental complexity in multicellular organisms, a pattern taken to an extreme in fungi and red algae, in which the CTD has undergone dramatic to complete alteration during the transition from unicellular to developmentally complex forms. Overall, loss and reinvention of repeats have punctuated CTD evolution, occurring independently and sometimes repeatedly in various groups.

Keywords: development; parasitism; splicing; transcription.

Fig. 1.

CTD diversity in eukaryotes. The tree shows consensus relationships of the 205 eukaryotes with CTD sequences mapped to each taxon. Sequences are oriented with N-termini at the outer edge and C-termini toward the center. Most CTD sequences are shown from the first obvious heptad to the C-terminal end; those with few or without heptads are shown from a supposed first heptad position, based on typical linker lengths, to the C-terminal end (the same convention is used in other figures). The 22 chordates are collapsed into one branch as their CTD sequences are nearly identical; the same was done for the 19 saccharomycete species. The annotated CTD structure for each genus is shown around the tree. Genus names and their branches are shown in four different colors based on their CTD states (Materials and Methods); state 3, green; state 2, teal; state 1, purple; and state 0, red. Roots I and II reflect alternative rootings of the eukaryotic tree for character state analyses. The probability that the ancestor of descending clades in state 0 (completely disorganized CTD) or state 3 (mostly tandem repeats) are shown separately in red and green.