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MBE Advance Access originally published online on June 7, 2006
Molecular Biology and Evolution 2006 23(9):1681-1687; 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

Research Article

Genome Architecture Drives Protein Evolution in Ciliates

Rebecca A. Zufall*,1, Casey L. McGrath*,2, Spencer V. Muse{dagger} and Laura A. Katz*,{ddagger}

* Department of Biological Sciences, Smith College; {dagger} Bioinformatics Research Center and Department of Statistics, North Carolina State University; and {ddagger} Program in Organismic and Evolutionary Biology, University of Massachusetts at Amherst

E-mail: lkatz{at}smith.edu.

Studies of microbial eukaryotes have been pivotal in the discovery of biological phenomena, including RNA editing, self-splicing RNA, and telomere addition. Here we extend this list by demonstrating that genome architecture, namely the extensive processing of somatic (macronuclear) genomes in some ciliate lineages, is associated with elevated rates of protein evolution. Using newly developed likelihood-based procedures for studying molecular evolution, we investigate 6 genes to compare 1) ciliate protein evolution to that of 3 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 5 of the 6 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 of genome architecture on molecular evolution.

Key Words: genome evolution • genome architecture • protein evolution • ciliate evolution


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