Evolution of eukaryotic transcription: insights from the genome of Giardia lamblia

Abstract

The Giardia lamblia genome sequencing project affords us a unique opportunity to conduct comparative analyses of core cellular systems between early and late-diverging eukaryotes on a genome-wide scale. We report a survey to identify canonical transcription components in Giardia, focusing on RNA polymerase (RNAP) subunits and transcription-initiation factors. Our survey revealed that Giardia contains homologs to 21 of the 28 polypeptides comprising eukaryal RNAPI, RNAPII, and RNAPIII; six of the seven RNAP subunits without giardial homologs are polymerase specific. Components of only four of the 12 general transcription initiation factors have giardial homologs. Surprisingly, giardial TATA-binding protein (TBP) is highly divergent with respect to archaeal and higher eukaryotic TBPs, and a giardial homolog of transcription factor IIB was not identified. We conclude that Giardia represents a transition during the evolution of eukaryal transcription systems, exhibiting a relatively complete set of RNAP subunits and a rudimentary basal initiation apparatus for each transcription system. Most class-specific RNAP subunits and basal initiation factors appear to have evolved after the divergence of Giardia from the main eukaryotic line of descent. Consequently, Giardia is predicted to be unique in many aspects of transcription initiation with respect to paradigms derived from studies in crown eukaryotes.

Figure 1

Comparisons of transcription component divergence with organismal divergence. Graphical representation of component distance (amino acid replacements per position) plotted on the y-axis vs. organismal small subunit rRNA distance (nucleotide substitutions per position) plotted on the x-axis. Data points are coded as indicated in the key. Error bars, one standard deviation uncertanties derived from 10 bootstrap replicates of protein distance calculations, are not visible at this scale. The identity of the RNAP subunit or transcription factor is indicated in A–G.

Figure 2

Phylogeny of archaeal TFB, eukaryal TFIIB, and eukaryal BRF transcription factors. Archaeal TFB sequences are used as the outgroup. Support values for the class V consensus tree (see Methods) are indicated next to each branch present in >50% of the significant topologies. Branch lengths of the consensus tree were estimated using PAML. The scale bar represents 10 amino acid replacements per 100 positions. Abbreviated sequence identifiers are Drosophila melanogaster, Giardia lamblia, Homo sapiens, Methanococcus jannaschii, Saccharomyces cerevisiae, Schizosaccharomyces pombe, and Sulfolobus solfataricus.