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MBE Advance Access published online on June 7, 2006
Molecular Biology and Evolution, doi:10.1093/molbev/msl032
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© The Author 2006. 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
Accepted May 25, 2006

Research Article

Genome Architecture Drives Protein Evolution in Ciliates

Rebecca A. Zufall 1, Casey L. McGrath 2, Spencer V. Muse 3, and Laura A. Katz 4 *

1 Department of Biological Sciences, Smith College; Current address: Department of Biology and Biochemistry, University of Houston
2 Department of Biological Sciences, Smith College; Current address: Program in Medical and Population Genetics, Broad Institute of Harvard and Massachusetts Institute of Technology
3 Bioinformatics Research Center and Department of Statistics, North Carolina State University
4 Department of Biological Sciences, Smith College; Program in Organismic and Evolutionary Biology, UMass-Amherst

* To whom correspondence should be addressed.
Laura A. Katz, E-mail: Lkatz{at}smith.edu


  Abstract

Studies of microbial eukaryotes have been pivotal in the discovery of biological phenomena, including RNA editing, self-splicing RNA and telomere addition. Here we demonstrate that genome architecture in ciliates, namely the extent of processing of somatic (macronuclear) genomes is associated with changing patterns of protein evolution. Using newly developed likelihood-based procedures for studying molecular evolution, we investigate six genes to compare: 1) ciliate protein evolution to that of three other clades of eukaryotes (plants, animals, and fungi) and 2) protein evolution in ciliates with extensively processed macronuclear genomes to that of other ciliate lineages. In five of the six genes, ciliates are estimated to have a higher ratio of nonsynonymous/synonymous substitution rates, consistent with an increase in the rate of protein diversification in ciliates relative to other eukaryotes. Even more striking, there is a significant effect of genome architecture within ciliates, as the most divergent proteins are consistently found in those lineages with the most highly-processed macronuclear genomes. We propose a model whereby genome architecture -- specifically chromosomal processing, amitosis within macronuclei, and epigenetics -- allows ciliates to explore protein space in a novel manner. Further, we predict that examination of diverse eukaryotes will reveal additional evidence of the impact genome architecture on evolution.


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