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MBE Advance Access published online on January 23, 2006
Molecular Biology and Evolution, doi:10.1093/molbev/msj089
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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 December 14, 2005

Research Article

Evolution of Programmed DNA Rearrangements in a Scrambled Gene

Li Chin Wong 1 and Laura F. Landweber 2 *

1 Department of Molecular Biology, Princeton University, Princeton, New Jersey 08544, USA
2 Department of Ecology and Evolutionary Biology, Princeton University, Princeton, New Jersey 08544, USA

* To whom correspondence should be addressed.
Laura F. Landweber, E-mail: lfl{at}princeton.edu


  Abstract

Gene unscrambling in spirotrichous ciliates involves massive genome-wide DNA deletion and rearrangement events during development. During each sexual cycle, the somatic nucleus (macronucleus) regenerates from the germline nucleus (micronucleus). Development of the polyploid somatic genome requires programmed DNA deletion of micronuclear-limited intragenic non-coding sequences, and permutation and amplification of the protein-coding regions. Recent studies suggest that, despite novel insertions of endogenous transposon or foreign DNA into the germline genome, ciliates possess a whole-genome surveillance system that guides the recapitulation of a functional somatic genome. This renders the germline genome an extremely dynamic structure over evolutionary time. Here we describe the germline and somatic architectures of the gene encoding {alpha}-telomere binding protein in three early diverging species (Holosticha sp., Uroleptus sp. and Paraurostyla weissei) and trace the natural history of DNA rearrangements in this gene in six species, including three previously studied oxytrichids. Comparisons of homologous coding regions between earlier and later diverging species provide evidence for fusion of scrambled germline fragments as small as 24 bp during evolution, as well as simultaneous fragmentation and scrambling of the germline locus and shifting of the boundaries between coding and noncoding DNA, leading to distinct gene architectures in each species. We infer an evolutionary recombination pathway that passes through identified intermediate species and gives rise to the observed patterns in all known species, capitalizing on their unique DNA rearrangement machinery and germline flexibility.

Keywords: DNA rearrangement; gene scrambling; spirotrich; hypotrich; telomere binding protein; micronucleus.
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