Genome-Scale Analysis of Programmed DNA Elimination Sites in Tetrahymena thermophila

Fass, Joseph N.; Joshi, Nikhil A.; Couvillion, Mary T.; Bowen, Josephine; Gorovsky, Martin A.; Hamilton, Eileen P.; Orias, Eduardo; Hong, Kyungah; Coyne, Robert S.; Eisen, Jonathan A.; Chalker, Douglas L.; Lin, Dawei; Collins, Kathleen

doi:10.1534/g3.111.000927

Genome-Scale Analysis of Programmed DNA Elimination Sites in Tetrahymena thermophila

Journal Article · Tue Nov 01 00:00:00 EDT 2011 · G3

DOI:https://doi.org/10.1534/g3.111.000927· OSTI ID:1627941

Fass, Joseph N. ^[1]; Joshi, Nikhil A. ^[2]; Couvillion, Mary T. ^[3]; Bowen, Josephine ^[4]; Gorovsky, Martin A. ^[4]; Hamilton, Eileen P. ^[5]; Orias, Eduardo ^[5]; Hong, Kyungah ^[3]; Coyne, Robert S. ^[6]; Eisen, Jonathan A. ^[3]; Chalker, Douglas L. ^[7]; Lin, Dawei ^[2]; Collins, Kathleen ^[3]

Univ. of California, Davis, CA (United States). Bioinformatics Core; DOE/OSTI
Univ. of California, Davis, CA (United States). Bioinformatics Core
Univ. of California, Davis, CA (United States). Genome Center
Univ. of Rochester, NY (United States). Dept. of Biology
Univ. of California, Santa Barbara, CA (United States). Dept. of Molecular, Cellular, and Cell Biology
J. Craig Venter Inst., Inc., Rockville, MD (United States)
Washington Univ., St. Louis, MO (United States). Dept. of Biology

Genetically programmed DNA rearrangements can regulate mRNA expression at an individual locus or, for some organisms, on a genome-wide scale. Ciliates rely on a remarkable process of whole-genome remodeling by DNA elimination to differentiate an expressed macronucleus (MAC) from a copy of the germline micronucleus (MIC) in each cycle of sexual reproduction. Here we describe results from the first highthroughput sequencing effort to investigate ciliate genome restructuring, comparing Sanger long-read sequences from a Tetrahymena thermophila MIC genome library to the MAC genome assembly. With almost 25% coverage of the unique-sequence MAC genome by MIC genome sequence reads, we created a resource for positional analysis of MIC-specific DNA removal that pinpoints MAC genome sites of DNA elimination at nucleotide resolution. The widespread distribution of internal eliminated sequences (IES) in promoter regions and introns suggests that MAC genome restructuring is essential not only for what it removes (for example, active transposons) but also for what it creates (for example, splicing-competent introns). Consistent with the heterogeneous boundaries and epigenetically modulated efficiency of individual IES deletions studied to date, we find that IES sites are dramatically under-represented in the 25% of the MAC genome encoding exons. As an exception to this general rule, we discovered a previously unknown class of small (,500 bp) IES with precise elimination boundaries that can contribute the 39 exon of an mRNA expressed during genome restructuring, providing a new mechanism for expanding mRNA complexity in a developmentally regulated manner.

View Accepted Manuscript (DOE)

Research Organization:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER). Biological Systems Science Division

Grant/Contract Number:: AC02-05CH11231

OSTI ID:: 1627941

Journal Information:: G3, Journal Name: G3 Journal Issue: 6 Vol. 1; ISSN 2160-1836

Publisher:: Genetics Society of AmericaCopyright Statement

Country of Publication:: United States

Language:: English

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59 BASIC BIOLOGICAL SCIENCES
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