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MBE Advance Access published online on January 21, 2008
Molecular Biology and Evolution, doi:10.1093/molbev/msn017
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© The Author 2008. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution. All rights reserved. For permissions, please e-mail: journals.permissions@oxfordjournals.org

Research Article

The Essential Sequence Elements Required for RNAP II C-terminal Domain Function in Yeast and their Evolutionary Conservation

Pengda Liu1,*, Arno L. Greenleaf2 and John W. Stiller1

1 Department of Biology, East Carolina University, Greenville, NC 27858, USA
2 Department of Biochemistry, Duke University Medical Center, Durham, NC 27710, USA

* Corresponding author: Pengda Liu, Howell Science Complex N-108, East Carolina University, Greenville, NC 27858, USA. Office: 252-328-4899. Fax: 252-328-4178. Email: pl1126{at}ecu.edu

Received for publication November 19, 2007. Revision received January 10, 2008. Accepted for publication January 11, 2008.

The carboxyl-terminal domain (CTD) of eukaryotic RNA polymerase II is the staging platform for numerous proteins involved in transcription initiation, mRNA processing and general coordination of nuclear events. Concordant with these central roles in cellular metabolism, the consensus sequence, tandemly repeated structure and core functions of the CTD are conserved across diverse eukaryotic lineages; however, in other eukaryotes the CTD has been allowed to degenerate completely. Even in groups where the CTD is strongly conserved, genetic analyses and comparative genomic investigations show that a variety of individual substitutions and insertions are permissible. Therefore, the specific functional constraints reflected by the CTD's conservation across much of eukaryotic evolution have remained somewhat puzzling. Here we propose a hypothesis to explain that strong conservation in budding yeast, based on both comparative and experimental evidence. Through genetic complementation for CTD function, we identify two sequence elements contained within pairs of heptapeptides, "Y1-Y8" and "S2-S5-S9", which are required for all essential CTD functions in yeast. The dual requirements of these motifs can account for strong purifying selection on the canonical CTD heptapeptide. Further, in vitro analyses of GST-CTD fusion proteins as substrates for multiple CTD-directed kinases show reduced phosphorylation efficiencies with increased distance between functional units. This indicates that requirements of the RNAP II phosphorylation cycle are most likely responsible for the strong purifying selection on tandemly repeated CTD structure.

Key Words: RNAP II • CTD • kinase • phosphorylation • evolution


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